Alfredo V.

Peretti ·
Lucía S. Calbacho-Rosa ·
Paola A. Olivero ·
Mariela A. Oviedo-Diego · David E. Vrech

Rules and
Exceptions
in Biology:
from Fundamental
Concepts
to Applications
Rules and Exceptions in Biology: from
Fundamental Concepts to Applications
Alfredo V. Peretti • Lucía S. Calbacho-Rosa
Paola A. Olivero • Mariela A. Oviedo-Diego
David E. Vrech

Rules and Exceptions in

Biology: from Fundamental
Concepts to Applications
Alfredo V. Peretti Lucía S. Calbacho-Rosa
Facultad de Ciencias Exactas Físicas y Facultad de Ciencias Exactas Físicas y
Naturales Naturales
Universidad Nacional de Córdoba. Instituto Universidad Nacional de Córdoba. Instituto
de Diversidad y Ecología Animal de Diversidad y Ecología Animal
(CONICET – UNC) (CONICET – UNC)
Córdoba, Córdoba, Argentina Córdoba, Córdoba, Argentina

Paola A. Olivero Mariela A. Oviedo-Diego

Facultad de Ciencias Exactas Físicas y Facultad de Ciencias Exactas Físicas y
Naturales Naturales
Universidad Nacional de Córdoba. Instituto Universidad Nacional de Córdoba. Instituto
de Diversidad y Ecología Animal de Diversidad y Ecología Animal
(CONICET – UNC) (CONICET – UNC)
Córdoba, Córdoba, Argentina Córdoba, Córdoba, Argentina

David E. Vrech
Facultad de Ciencias Exactas Físicas y
Naturales
Universidad Nacional de Córdoba. Instituto
de Diversidad y Ecología Animal
(CONICET – UNC)
Córdoba, Córdoba, Argentina

ISBN 978-3-031-55380-6    ISBN 978-3-031-55382-0 (eBook)

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To students and professionals curious to
question rules and value exceptions
in biology
To our families
Preface

Science is a changing system in which many currently accepted paradigms were

considered inadequate in the past. Likewise, it is accepted that well-established
explanations may be greatly modified in the near future. Many fields in the life sci-
ences, such as ecology, ethology, and evolution, are good examples of such change.
Robust explanations result from the identification of patterns that reflect general and
well-established rules. However, it is often the case that other patterns are excep-
tions or remain unclear.
It is crucial to clearly recognize the differences between what is established as a
general pattern and what is an exception, as interpretations in both cases have dif-
ferent implications from an evolutionary perspective. In the last 20 years, some
aspects of rules and exceptions have been studied in some organisms or contexts.
However, they have been partially analyzed. For example, by focusing only on laws
or the value of some abnormalities (teratologies), including useful biographies of
important scientists in the field. Reviews or articles also evaluated these compo-
nents, rules, and exceptions separately and limited to some papers on the theory of
biological laws and ecogeographic rules.
From this promising current scenario, we decided to work on a book that could
not only help fill a niche in the scientific education of pre- or postgraduate students,
but also help generate useful and valuable discussions among scientists working in
the life sciences and related disciplines. We explore rules and exceptions in biology,
and the criteria that have been used to establish such definitions and boundaries. We
analyze the dynamics between rules and exceptions, both due to changes in nature
and in scientific thinking. We also assess how criteria and concepts have changed
within disciplines, and what implicit biases may exist.
Studies of many groups of organisms are used as examples to illustrate some of
this interactive relationship and to provide new information to confirm, limit, or
refute concepts based on rules and exceptions in science. It is our hope that this
book will be a source of knowledge about how two seemingly opposite situations,
rule and exception, flow and interact from different scales of time, space, and taxa
in nature. This book took many years to write, mainly because we had to learn
aspects of biology not necessarily related to our specialty. As invertebrate

vii
viii Preface

zoologists, especially on arthropods, we can sometimes have a bias of examples, but

without neglecting globality. In fact, the examples in the book are not exhaustive,
but illustrative of the vast subject matter covered.
This book is intended for an international scientific audience: undergraduate stu-
dents (i.e., those doing honors projects), graduate students, postgraduate students,
and professional scientists. The book could be used as a reference source of ideas,
perspectives, and critical views of new directions for students of life sciences. Any
biologist, as well as scientists in related disciplines (e.g., biomedical researchers,
psychologists) with broad evolutionary interests, would be interested in the material
contained in the book.
Regarding the structure of the book, the first two chapters of the book are basic
introductions to the diversity of definitions of rules and exceptions in science and
other disciplines. They also relate the concepts of biological rules and exceptions to
ideas in epistemology and the philosophy of science. The third chapter explores the
basis of the dynamics between rules and exceptions from temporal, spatial, and
group perspectives, and the main directions of change between rules and exceptions
in different temporal, spatial, and organismic scenarios.
From Chap. 4–7, we explore situations of change between rules and exceptions
with illustrative examples from different areas of biology. Chapter 4 analyzes the
situation when a rule persists as a rule, both in biology and in scientific thinking.
Chapter 5 explores the world of exceptions. Because of the common underestima-
tion of exceptions and their value in biology, this chapter, together with Chap. 6,
which examines when exceptions become rules, is probably the heart of the book.
Indeed, it is where we emphasize the most. Chapter 7 looks at situations where rules
become exceptions. Chapter 8 presents illustrative cases of rule-exception transi-
tions beyond biology, including other sciences, the arts, and other areas of human
activity.
Chapter 9 offers a final overview and outlook, with some interesting tips and
suggestions for scientific approaches and practices.

Córdoba, Córdoba, Argentina  Alfredo V. Peretti

  Lucía S. Calbacho-Rosa
  Paola A. Olivero
  Mariela A. Oviedo-Diego
  David E. Vrech
Acknowledgments

Our first thanks go to Lars Kroener, Springer, who received and supported this pro-
posal throughout its long development. This book began to take shape after A. Peretti
was invited to give a presentation on rules and exceptions in sexual selection at a
Brazilian Ethology Congress in 2010, which later resulted in a chapter on the sub-
ject. Our first thanks go to Regina Macedo and Glauco Machado, who helped with
this first big step. Special thanks also go to Anita Aisenberg, who facilitated the
presentation of the first drafts of this book at the Uruguayan Zoology Congress in
2012. Thanks also to Carlos Cordero for encouraging A. Peretti to give a plenary
lecture on rules and exceptions in behavior at an international behavior course in
Mexico in 2015. We are very grateful to Alejandro Córdoba-Aguilar and Bill
Eberhard for supporting the realization and writing of this literary adventure.
We also thank our colleagues at the Laboratory of Reproductive Biology and
Evolution (LABRE, IDEA, CONICET-UNC) for their input and feedback with
extremely helpful comments during the writing and reading of the book, especially
Franco Cargnelutti. Special thanks are due to those who provided us with original
photographic material from their research, including Matías Izquierdo, Darko
Cotoras, Andrea Coccuci, Gabriel De Simone, Otto Bylén Claesson, Sergio
Rodríguez, and Franco Peretti-Plazas, who helped in the preparation of some of the
first versions of the figures. We are also thankful to the following people for com-
ments and suggestions on ideas and contents of this book: Franco Cargnelutti,
Matias Izquierdo, Alejandra de Lourdes Ceballos, Anita Aisenberg, Eileen Hebets,
and Alex Córdoba-Aguilar. We are indebted to our families for their immeasurable
support throughout this work.
We gratefully acknowledge the support of the Consejo Nacional de Investigaciones
Científicas y Tecnológicas (CONICET) of Argentina, the Secretaría de Ciencia y
Técnica de la Universidad Nacional de Córdoba (SECYT), and the Agencia Nacional
de Promoción Científica y Técnica de la Argentina (ANCYPT).

ix
Contents

Part I Establishing Criteria and Theoretical Possibilities

1  Big World of Rules? ����������������������������������������������������������������������������    3
A
1.1 Introduction��������������������������������������������������������������������������������������    4
1.2 What Is a Rule?��������������������������������������������������������������������������������    5
1.2.1 Some Basic Hierarchical Levels of Rules in Biology����������   11
1.3 Searching for Universal Rules in Biology����������������������������������������   15
1.3.1 The Phenomenon of Emergence ������������������������������������������   15
1.3.2 On Some More Holistic Approaches������������������������������������   16
1.3.3 Biological Complexity: Controversial Rules������������������������   18
1.3.4 The General Systems Theory and Systems Biology
Perspective����������������������������������������������������������������������������   18
1.4 Presence of Rules According to Levels and Areas of Biology ��������   19
1.4.1 On “Minuscule” Rules: Certainties Even
in the Narrowly Defined��������������������������������������������������������   19
1.4.2 Laws, Rules, and Patterns ����������������������������������������������������   21
1.4.3 Visiting Some Witness Cases������������������������������������������������   22
1.5 Linking Rules with Epistemology: Changing Paradigms����������������   26
1.6 Evolutionary Theory as a Driving Force for Changes
in Biological Rules����������������������������������������������������������������������������   28
1.7 On Mathematics and Contingency: Does It Weaken
Evolutionary Predictions? ����������������������������������������������������������������   30
1.8 Possible “Principles” on the Nature of Biological Rules?����������������   32
1.9 Key Concepts and Ideas in This Chapter������������������������������������������   35
References��������������������������������������������������������������������������������������������������   35

xi
xii Contents

2  Small World of Exceptions?����������������������������������������������������������������   41

A
2.1 Introduction��������������������������������������������������������������������������������������   42
2.2 What Is an Exception?����������������������������������������������������������������������   43
2.2.1 They Are in Our Daily Life��������������������������������������������������   44
2.2.2 Does the Scientific Method Ignore What Is Nothing
or Even a Little “Repeatable?” ��������������������������������������������   48
2.3 Waiting for Exceptions According to Rule Levels����������������������������   49
2.4 The “Exceptional” from the Point of View of Exceptions����������������   50
2.4.1 An “Exceptional” Example? The Rapid
Evolution of HIV������������������������������������������������������������������   51
2.5 Exceptions: Single-Trait or Multitrait? ��������������������������������������������   52
2.6 “Invisible” Exceptions: Outliers in a Population������������������������������   54
2.7 Outliers: Those Underestimated Exceptions������������������������������������   56
2.7.1 An Outlier Hiding a Spider’s Secrets������������������������������������   59
2.8 Key Concepts and Ideas in This Chapter������������������������������������������   61
References��������������������������������������������������������������������������������������������������   61
3 
Associations and Dynamics Between Rules and Exceptions����������������   65
3.1 Introduction��������������������������������������������������������������������������������������   66
3.2 Complementary Concepts When Focusing on Rules and
Exceptions����������������������������������������������������������������������������������������   66
3.2.1 On Terms and Their Synonyms Related to the
Normal and the Abnormal����������������������������������������������������   66
3.2.2 Singularity: Each Living Being is Unique����������������������������   67
3.2.3 Are There Rules for Predicting the Occurrence or
Type of Exception? ��������������������������������������������������������������   68
3.3 Three Perspectives on the Dynamics Between Rules
and Exceptions����������������������������������������������������������������������������������   69
3.3.1 The Possibility of Mixed Patterns����������������������������������������   69
3.4 Main Directions of the Changes ������������������������������������������������������   70
3.4.1 “Conservative” Rules and Exceptions?��������������������������������   71
3.4.2 Movements of Rules “With Continuous
Distribution” ������������������������������������������������������������������������   71
3.5 Key Concepts and Ideas in This Chapter������������������������������������������   78
References��������������������������������������������������������������������������������������������������   79

Part II Exploring Rules and Exceptions from Life Sciences

4 
When THAT Rule Almost Persists as THAT Rule��������������������������������   83
4.1 Introduction��������������������������������������������������������������������������������������   84
4.2 Flexibilizing and Enriching Fixed Ideas: A Brief Historical
Timeline in Genetics and Evolution��������������������������������������������������   85
Contents xiii

4.3 What Is a Biological Species: Is There a Rule?��������������������������������   89

4.4 Biological Rules: Some Historical Changes and Limitations����������   93
4.4.1 Analysis of Some Examples ������������������������������������������������   93
4.5 Key Concepts and Ideas in this Chapter ������������������������������������������ 107
References�������������������������������������������������������������������������������������������������� 108
5 
When THAT Exception Persists Almost as THAT Exception�������������� 115
5.1 Introduction�������������������������������������������������������������������������������������� 117
5.2 Teratologies: Aberrations Revalorized���������������������������������������������� 120
5.2.1 Defining Teratologies, Subjectivities, and
the Relationship Between Concepts������������������������������������� 120
5.2.2 Utility of Teratologies in Evolution�������������������������������������� 121
5.2.3 Factors That Can Generate Teratological Traits�������������������� 123
5.2.4 Invertebrate Teratologies������������������������������������������������������ 125
5.2.5 Some Examples of Teratologies in Plants���������������������������� 129
5.3 Treasure Your Exceptions ���������������������������������������������������������������� 132
5.3.1 Temptation to Generalize When Encountering
an Interesting Exception ������������������������������������������������������ 133
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing
Strategies������������������������������������������������������������������������������������������ 134
5.4.1 Exceptional Animal and Plant Groups���������������������������������� 135
5.4.2 Extraordinary Phenomena���������������������������������������������������� 159
5.4.3 Evolutionary and Ecological Exceptions������������������������������ 180
5.5 Key Concepts and Ideas in This Chapter������������������������������������������ 191
References�������������������������������������������������������������������������������������������������� 192
6 
Focusing on Dynamics: When an Exception Becomes a Rule������������� 223
6.1 Introduction�������������������������������������������������������������������������������������� 225
6.2 E-R Changes by Nature’s Action������������������������������������������������������ 227
6.2.1 At Crucial Moments of Biological Evolution���������������������� 227
6.2.2 Perspectives and Cases of when “Oddities”
Become the Pattern �������������������������������������������������������������� 252
6.2.3 A More Bidirectional E-R Dynamic in the Short
Term: Facultative Organisms������������������������������������������������ 267
6.3 E-R Changes Due to Human Activity on Nature������������������������������ 271
6.3.1 Exotic Groups that Become Local Pests������������������������������ 271
6.3.2 A Look at the Disease Cycle and the Role of Man�������������� 278
6.3.3 Influence of Environmental Pollution and Climate
Change���������������������������������������������������������������������������������� 288
6.3.4 Manipulating Organisms to a Destination���������������������������� 293
xiv Contents

6.4 E-R Changes Due to Modifications in Scientific

Interpretations ���������������������������������������������������������������������������������� 308
6.4.1 Key Factors Associated with Change������������������������������������ 308
6.4.2 Some Case Histories of E - R Change by Scientific
Vision������������������������������������������������������������������������������������ 310
6.5 Key Concepts and Ideas in This Chapter������������������������������������������ 351
References�������������������������������������������������������������������������������������������������� 353
7 
Focusing on Dynamics: When a Rule Becomes an Exception������������� 405
7.1 Introduction�������������������������������������������������������������������������������������� 406
7.2 R-E Changes Due to Nature’s Own Action�������������������������������������� 407
7.2.1 Reductions and Disappearances of Characters
and Interactions�������������������������������������������������������������������� 407
7.2.2 From Dominant to Rarities and Major Extinctions�������������� 414
7.3 Human-Induced R-E Changes over Nature�������������������������������������� 425
7.3.1 Reduction or Loss of Changing Capacity in Living
Organisms ���������������������������������������������������������������������������� 425
7.3.2 In Humans: Reduction of Human Integration
to Natural Dynamics ������������������������������������������������������������ 429
7.3.3 Toward the Extinction of Organisms as a Massive
Phenomenon (“Folding” Life Diversity)������������������������������ 432
7.3.4 Climate Change and its Effect on the Dynamics
of R to E�������������������������������������������������������������������������������� 441
7.4 R-E Changes Due to Modifications in Scientific
Interpretations ���������������������������������������������������������������������������������� 448
7.4.1 Key Factors Linked to Change���������������������������������������������� 449
7.4.2 With “Potential” of R-E by the Change
in Interpretations ������������������������������������������������������������������ 461
7.5 Key Concepts and Ideas in this Chapter ������������������������������������������ 465
References�������������������������������������������������������������������������������������������������� 466
8 Beyond Biology���������������������������������������������������������������������������������������� 489
8.1 Introduction�������������������������������������������������������������������������������������� 490
8.2 R&E in Sciences More Closely Related to Biology ������������������������ 491
8.2.1 Medicine and Related Sciences�������������������������������������������� 491
8.2.2 Physics Miscellaneous���������������������������������������������������������� 501
8.2.3 Chemical Miscellanea���������������������������������������������������������� 503
8.2.4 Geological and Related Notes���������������������������������������������� 506
8.2.5 Astronomy Miscellany���������������������������������������������������������� 507
8.3 R&E in Other Knowledge Disciplines���������������������������������������������� 511
8.3.1 Social and Related Sciences������������������������������������������������� 511
8.4 R&E Search on Subjective/Controversial Topics ���������������������������� 514
8.4.1 Art and Culture �������������������������������������������������������������������� 514
8.4.2 Sports������������������������������������������������������������������������������������ 520
8.4.3 Religions and Beliefs������������������������������������������������������������ 521
8.5 Key Concepts and Ideas in this Chapter ������������������������������������������ 522
References�������������������������������������������������������������������������������������������������� 523
Contents xv

9 
Overview and Final Prospects���������������������������������������������������������������� 531
9.1 Perspectives on Potential Applications �������������������������������������������� 532
9.2 On a more Theoretically Scientific Level ���������������������������������������� 533
9.2.1 Strengthening Publications on Rarities�������������������������������� 533
9.2.2 Appreciating the Dynamism Between R and E�������������������� 534
9.2.3 Avoiding Bias in Scientific Education���������������������������������� 535
9.3 On a Human–Nature Relationship Level������������������������������������������ 536
9.3.1 The Vindication of Singularity and Otherness���������������������� 536
9.3.2 Direct Applications of Exceptions
and R<->E Dynamism���������������������������������������������������������� 538
9.3.3 Modifications and Environmental Risks
of R<->E Dynamism������������������������������������������������������������ 540
9.3.4 Applications of R<->E Dynamism on a more
Holistic Level������������������������������������������������������������������������ 541
References�������������������������������������������������������������������������������������������������� 543

Index������������������������������������������������������������������������������������������������������������������ 545
About the Authors

Alfredo Vicente Peretti is Principal Researcher of the

Consejo Nacional de Investigaciones Científicas y
Técnicas de la Argentina, Instituto de Diversidad y
Ecología Animal (CONICET-­ IDEA) and Associate
Professor of the Departamento de Diversidad Biológica
y Ecología, Facultad de Ciencias Exactas Físicas y
Naturales, Universidad Nacional de Córdoba, Argentina.
His main area of interest and research is zoology, with
emphasis on invertebrates. He works in behavior, ecol-
ogy, and evolution, particularly in the field of reproduc-
tive biology using arthropods as models.

Lucia Calbacho-Rosa is Associate Researcher of the

Consejo Nacional de Investigaciones Científicas y
Técnicas de la Argentina, Instituto de Diversidad y
Ecología Animal (CONICET-­IDEA). Her main areas of
research are behavior, reproductive biology, sexual
selection, and studies of genital morphology using
arthropod species as a model.

xvii
xviii About the Authors

Paola Andrea Olivero is an Assistant Researcher of

the Consejo Nacional de Investigaciones Científicas y
Técnicas de la Argentina, Instituto de Diversidad y
Ecología Animal (CONICET-­ IDEA) and Associate
Professor in general biology at the Facultad de Ciencias
Exactas, Físicas y Naturales of the Universidad Nacional
de Córdoba, Argentina. Her research field is related to
the study of the reproductive biology, analyzing the
behavior during courtship and patterns of differential
paternity in arachnids and insects.

Mariela Oviedo-Diego is Postdoctoral Fellow at the

Consejo Nacional de Investigaciones Científicas y
Técnicas de la Argentina, Instituto de Diversidad y
Ecología Animal (CONICET-­ IDEA) and vocational
teacher in Entomology at the Facultad de Ciencias
Exactas, Físicas y Naturales, Universidad Nacional de
Córdoba, Argentina. Her research has focused on sexual
behavior, the study of pre- and postcopulatory charac-
ters and reproductive interference in different arachnid
species.

David Eduardo Vrech is Associate Researcher at the

Consejo Nacional de Investigaciones Científicas y
Técnicas de la Argentina, Instituto de Diversidad y
Ecología Animal (CONICET-­ IDEA) and Assistant
Professor specializing in invertebrate biology at the
Facultad de Ciencias Exactas, Físicas y Naturales,
Universidad Nacional de Córdoba, Argentina. His pri-
mary research areas encompass sexual selection, repro-
ductive biology, and the investigation of sperm
competition across arachnid groups.
 Part I
Establishing Criteria and Theoretical
Possibilities
Chapter 1
A Big World of Rules?

Everyday life weaves us, daily, a spider’s web in our eyes

—Oliverio Girondo

Contents
1.1 Introduction 4
1.2 W hat Is a Rule? 5
1.2.1 Some Basic Hierarchical Levels of Rules in Biology 11
1.3 Searching for Universal Rules in Biology 15
1.3.1 The Phenomenon of Emergence 15
1.3.2 On Some More Holistic Approaches 16
1.3.3 Biological Complexity: Controversial Rules 18
1.3.4 The General Systems Theory and Systems Biology Perspective 18
1.4 Presence of Rules According to Levels and Areas of Biology 19
1.4.1 On “Minuscule” Rules: Certainties Even in the Narrowly Defined 19
1.4.2 Laws, Rules, and Patterns 21
1.4.3 Visiting Some Witness Cases 22
1.4.3.1 Classification of Living Beings 22
1.4.3.2 Behavior and Communication 22
1.4.3.3 Rules and Basic Plant Patterns 24
1.4.3.4 When It Is Still Difficult to Establish Rules: The Case of
“Ecological Genomics” 26
1.5 Linking Rules with Epistemology: Changing Paradigms 26
1.6 Evolutionary Theory as a Driving Force for Changes in Biological Rules 28
1.7 On Mathematics and Contingency: Does It Weaken Evolutionary Predictions? 30
1.8 Possible “Principles” on the Nature of Biological Rules? 32
1.9 Key Concepts and Ideas in This Chapter 35
References 35

© Springer Nature Switzerland AG 2024 3

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_1
4 1 A Big World of Rules?

Abstract To establish criteria and theoretical possibilities for rules and exceptions
in biology, it is helpful first to analyze what a rule is, as well as its many variants.
This chapter presents some hierarchical levels of rules in biology, with examples of
the most comprehensive and the most restrictive. In both contexts, we discuss the
concepts of laws, rules, and patterns and how these boundaries are not always so
clear. The topic of the search for universal laws in biology is introduced. In this
context, the phenomena of emergence, biological complexity, and others are men-
tioned. We analyze when there are smaller rules, limited to a certain field within
biology. We see as some introductory examples when there are rules of behavior,
ecology, and evolution. We also discuss the links between rules and epistemology,
especially regarding paradigm shifts.

1.1 Introduction

The “plasticity” of ideas, hypotheses, and theories in science is a fact. As Kuhn

(1996) classically analyzed, the so-called paradigms change over time. Science is
the opposite of a static system, or at least it should be, as dogmas tend to remain
unchanged in time and space. There is a consensus in the scientific community that
changes are bound to occur in science. However, the open-mindedness to such
changes, which implicitly recognizes the flexibility of knowledge, differs among the
different areas of expertise. The “Kuhnian” basis of the construction of a paradigm,
its subsequent acceptance during a particular time (i.e., normal science), and finally,
its crisis that will lead to its fall and replacement by new ideas (i.e., scientific revolu-
tion) (Kuhn, 1996; Bussard, 2005) are a fluid cycle. This change is understood and
accepted, but with different tones, emphases, or perspectives in each discipline. The
history of science in general, and biology in particular, is full of examples of infor-
mation sets and concepts that became paradigms at one time in the past and are no
longer valid today.
Likewise, much of the information obtained throughout humanity’s history was
due to the development of science. The contribution of scientific knowledge led to
currently accepted ideas and concepts that might have been rejected or not even
imagined in the past. This fact is evident in areas of modern biology such as genet-
ics, molecular and evolutionary biology, nanotechnology, and quantum physics. A
classic example is the field of sexual selection, which was almost “dormant” for
approximately a century after the publication of the first edition of “The Origin of
1.2 What Is a Rule? 5

Man and Selection in Relation to Sex” (Darwin, 1871). This oblivion, in large part,
was due to the moral conditioning of the time about the view of “sex” and, there-
fore, its role as a critical factor in the evolution of living beings (Gould & Gould,
1989; Birkhead, 2000). Sexual selection was revisited in animals after several years,
and its presence in plants has been almost ignored until very recently (Andersson,
1994; Moore & Pannell, 2011). The change of view on a scientific concept from
being “not acceptable” to “acceptable” and vice versa, as we shall see, may be due
to multiple reasons. Among them, the nature of biology itself, specifically biologi-
cal evolution, may have played a preponderant role. In other situations, the change
is more linked, as we said, to modifications in scientific interpretation due, for
example, to advances in research techniques and technologies, differences in social
biases, and schools of thought, among others.

1.2 What Is a Rule?

In this context, how can we define a rule? Definitions are inherently challenging as
they frequently lack an ingredient, making them somewhat odious, but here, they
become necessary for what we will analyze in this book. As we will see, allusions
to the rule often link to its antonym; in other words, they are more defined by what
it is not than by what it is. In this problem, it is interesting to keep in mind that for
a given fact or concept, we will have, on the one hand, the rule and, on the other
hand, what is an exception to it. Undoubtedly, there is no single definition of “rule”
(Box 1.1). Nevertheless, for practical purposes, we can summarize a rule as “a gen-
eralized statement that describes what is true in most or all cases” (The American
Heritage®, Dictionary of the English Language, 2003). The notion of the rule leads
us almost directly to the definition of “scientific law” as “a scientific statement that
claims a constant relationship between two or more variables or factors, each of
which represents (at least partially and indirectly) a property of concrete systems”
(Honderich, 1995). It is crucial to consider that, depending on the scientific disci-
pline, there will be a plethora of terms closely associated with the term rule, such as
“norm,” “pattern,” and “law” (Box 1.1). Indeed, they can be synonymous, although
each meaning will have its own level of “applicability,” as we will see below. In the
natural sciences, a scientific law is “a rule that relates events that have a joint, usu-
ally causal, occurrence.”
6 1 A Big World of Rules?

License: own creation

1.2 What Is a Rule? 7

While rules play a crucial role in constructing scientific theories, their enuncia-
tion in the biological sciences is generally less frequent compared to other scientific
disciplines such as chemistry and physics (Fig. 1.1a). Dhar & Giuliani (2010)
arrange biological, chemical, and physical events into trait levels and, along with
them, the rules or laws of those levels (Fig. 1.1b). The enunciation and acceptance
of rules apply to basic levels, such as the atomic or cellular levels. However, they
can also be done for higher levels involving organisms or interactions between them
(e.g., ecology and communities).

aa

Fig. 1.1 Levels of analysis in science. (a) Interrelation between scientific disciplines with differ-
ent degrees of inclusiveness/competence in their rules. (b) Level of organization associated with
the level of rules and the scientific discipline that includes them. License: own creation. Free
images from Pixabay. (Modified from Dhar & Giuliani, 2010)
8 1 A Big World of Rules?

One might question whether there are scientific disciplines devoid of rules or
those that are so dynamic over time that articulating them becomes a waste of time.
A narrow approach could limit the application of laws only to the so-called “hard”
sciences, such as physics, chemistry, or mathematics. Indeed, it is often postulated
that biology need not have any fundamental laws of its own since all the basic laws
of biology are simply a subset of the fundamental laws of physics (Wayne, 2020).
However, biology presents itself as a complex of disciplines and subdisciplines that
have been and still are difficult to catalog, summarize, or encompass in just laws of
physics. Many are bodies of hypotheses and theories that are gradually being
demonstrated.
In many cases, although they do not acquire the name of “law” in common sci-
entific language, they are implicitly taken as such in practice. In other words, basic
principles are continuously sought in biology beyond physics (e.g., laws of thermo-
dynamics). For example, the integration of biological phenomena in an evolution-
ary framework of living beings and the selection processes involved (natural,
sexual).
On the other hand, biology poses diverse, complex, changing, and often unpre-
dictable scenarios. Understanding how random historical events shape evolutionary
processes is a critical goal of evolutionary biology (Harms & Thornton, 2014). In
this context, Gould’s (1989) reviews of the phenomenon of contingency in biology
(i.e., what may or may not happen in nature), such as meteorite falls and volcanic
eruptions, are classic. Some of these events have been key in biological evolution,
for example, in great extinctions. To this must be added the intrinsic contingency,
such as factors inherent to the molecules that make up the organism and the low
probability of repeating the same mutations that have formed them or helped them
to their current behavior and sensitivity. Biology differs from physics in this respect
as to what could happen if history were rewound about what to foresee or not and
whether the same chain of random events would repeat itself.
In this sense, evidence shows that the inherent complexity of proteins makes evo-
lution deeply dependent on intrinsic random events of very low probability. This is
the conclusion that Harms & Thornton (2014) arrived at after analyzing the evolu-
tion of cortisol specificity in the ancestral glucocorticoid receptor. After examining
numerous potential evolutionary paths for the protein, they discovered no alternative
mutations that could have given rise to the current protein, apart from the two toler-
ant mutations it already possesses. They concluded that the evolution of the ancestral
glucocorticoid receptor was strongly dependent on improbable and nondeterministic
events, and this contingency arose from the intrinsic biophysical properties of the
protein. We will return to the phenomenon of contingency throughout this chapter.
As far as we know, biological concepts and predictions apply only to our planet.
The same is not true of physics and perhaps chemistry, whose more “encompass-
ing” laws allude to contexts beyond the confines of the Earth. Exobiology, whose
main objective is the study of the possibilities of extraterrestrial life, tries to propose
analogous situations in other worlds from the knowledge of our biological history
and evolution. However, it is limited because the options could vary in different
places of the universe. That is where scientific speculation can border on fantasies,
1.2 What Is a Rule? 9

with hypotheses that are not falsifiable or difficult to test. Nevertheless, exobiology
exists as a discipline and is valued for its potential to attempt such extrapolation in
a very sui generis scientific framework.
Given the abundance of exceptions in biology, it becomes pertinent to pause and
ponder upon a seemingly self-evident question: Is it meaningful to formulate, estab-
lish, and apply laws, as well as their more nuanced manifestations such as rules,
patterns, or regularities? This perspective would be aligned with that of an orthodox
physicist who might harbor some skepticism toward biology due to the challenge of
identifying general laws in this field of science directly and above all, devoid of
exceptions or with exceptions that are minimal in nature.
The truth is that biology is a “flexible” science because its object of study, living
beings, demands this flexibility. However, it is not because of this characteristic that
it does not fail to recognize the existence of patterns and principles, which translate
into different levels of rules or laws. One cannot expect, naively perhaps, the absence
of exceptions. However, we will see below specific, very comprehensive, or general
laws in biology where exceptions should not be expected to exist.
For any attempt to propose rules in biology, in addition to the inherent flexibility,
it is important to consider that the primary driver of the evolutionary process in biol-
ogy is the interpopulation variability within a species, primarily arising from the
occurrence of random mutations.
In that case, we are facing a scenario more challenging than in the so-called
“hard sciences” but also a frustrating one if we want to meet it with the same meth-
odologies, epistemological approaches, and study perspectives. If we add to this
“cocktail” the different “layers” or levels of study in biology (e.g., from the micro-
scopic to the macroscopic), and not only from the cellular to the organismic but also
at the level of communities and ecosystems, the challenge we face is much more
significant. Therefore, we have to approach biology’s study of rules, patterns, and
laws with a less orthodox and more inflexible view and perspective. We must main-
tain scientific rigor in their accuracy, evaluation, and application, but we must be
adaptable to the presence of variants of the rules that we can establish. However, it
is crucial to avoid falling into a false dichotomy that either denies the existence of
principles or indiscriminately accepts everything with exceptions. It is important to
strike a balance by critically evaluating generalizations that may be incorrectly
imposed, such as extrapolating findings from one model of a living being to another.
By doing so, we can avoid overlooking critical analysis and ensure that principles
are appropriately formulated and applied.
On this subject of what is a rule, it is good to remember that Charles Darwin, in
The Origin of Species, already deals with the issue of laws in nature. Today, we can
say that, since that work and subsequent associated articles, the theory of natural
selection is a central axis in any idea about biological evolution (something that we
will return to in the following paragraphs when we refer to laws of biology at more
globalizing levels). Darwin recalls an ancient principle of natural history: “Natura
non facit saltum” (nature does not proceed by leaps—, i.e., nature varies continu-
ously and not in an abrupt manner), to reinforce that the theory of natural selection
would apply both to present-day organisms and to past times, known or unknown.
10 1 A Big World of Rules?

Darwin emphasizes that organic beings were formed according to two great
laws: “unity of type” and “conditions of existence.” The first alluded to the fact that
there is a general concordance in the structure observed in beings of the same kind,
while the second law alludes to the conditions in which these beings inhabit; that
is, it is directly connected with the adaptation of organisms to their abiotic and
biotic environments. He then points out that this second law is wholly included in
the “principle of natural selection.” He concludes by saying, “the law of the condi-
tions of existence is the superior law because, through the inheritance of previous
variations, it includes the law of the unity of type.” In essence, this perspective
establishes a hierarchy between these two laws, expressing an opinion that one law
encompasses the other, as they are mutually causative and consequential. This
comprehensive viewpoint, specifically in the context of evolution, allows for a
more holistic understanding. In addition to reinforcing his postulate of natural
selection, the most exciting thing is that he reinvents these laws, reinterprets them,
and does not discard them; in any case, he explains them better with his study and
innovative perspective. He discarded dogmas that touch upon concepts such as the
divine origin of organic beings, recognizing them not as laws but rather as outdated
beliefs.
Let us move on a hundred years later. We have another great naturalist, postulat-
ing principles. However, these principles take the form of “problems” or questions,
serving to address specific uncertainties prevalent during the study of animal behav-
ior at that time. It is worth noting that such “problems” are inherent to any field of
biology, reflecting common challenges faced in scientific inquiry. The naturalist’s
name was Niko Tinbergen, the great Dutch ethologist, who, in the early sixties,
postulated the “four problems” for studying animal behavior (Tinbergen, 1963). A
couple of years earlier, Ernst Mayr had already laid the foundations in his look at
proximate and ultimate causes, extended to ecology and the potential for any study
of biological phenomena (Mayr, 1961). Within this framework of seeking regulari-
ties or laws through the examination of problems, the study of animal behavior
encompasses a wide range of perspectives and methodological approaches. These
approaches vary depending on the specific questions being addressed, such as inves-
tigating proximate causes related to physiology and ontogeny or exploring ultimate
reasons connected to adaptive function and evolution. The distinction between
proximate causes (how and when) and ultimate causes (why and wherefore) guides
the diverse avenues of research within the field (Bateson & Laland, 2013).
These differences in approach between the immediate and nonimmediate,
although interdependent (Sherry, 2005), mean that among biologists themselves,
there may be certain biases or criticisms depending on the type of questions their
study addresses. Studies with questions focused on patterns and mechanisms that
are more “exact” to observe and measure (e.g., proximate causes) will have a differ-
ent value than those with “less exact” questions or hypotheses that are more difficult
to falsify (e.g., ultimate causes). For example, a physiologist focused on how a trait
is expressed during ontogeny would consider his conclusions more robust than
those reached by a behavioral ecologist focused on the adaptive function of that
trait. On the other hand, the latter would see the conclusions of the former as more
1.2 What Is a Rule? 11

limited and perhaps reductionist. Thus, specific rules could be considered “stron-
ger” (would they add up to a few exceptions?) in disciplines oriented to studying
proximate causes, such as molecular biology and physiology, more directly influ-
enced by physics and chemistry. However, mistakenly, those enunciated for the
organismic level and ultimate causes (e.g., certain branches of ecology, taxonomy,
natural history, evolution) may be seen as “less strict” rules (can they add up to more
exceptions?). Fortunately, this has been changing over time. There are already
ample examples of how immediate and ultimate causes interrelate and nurture each
other in approaches and information (Kirschner & Gerhart, 2006) and make the
orthodoxy of a different valuation of one or the other no longer so helpful today
(Laland et al., 2011, 2013).
Our planet functions as a whole, an interactive system whose key components
are living beings. This perspective, as we know it today, was contemplated by
Lovelock’s famous “Gaia hypothesis” (1985), which states that life can transform
the biosphere, fostering and maintaining environmental conditions suitable for
itself, with modification of the environment. Beyond the scope, controversies, and
limitations of this hypothesis, it is important to address the fact that what we know
about biology would necessarily have to consider in any study the existence of inter-
action within an “integrated whole.” Thus, wanting to dissect biology into rules and
concepts that define it is challenging, and there is a significant risk of falling into
reductionism.
Thus, biology invites us to incorporate other visions for a more critical under-
standing. In that context, we will then examine the phenomenon of “emergence,”
which implies that there will be properties at certain levels of organization that can-
not be predicted simply by the properties exhibited at lower levels (Emmeche et al.,
1997). For many, this is a valuable perspective on tracing universal patterns to all of
biology, in particular, because it connects to a more holistic view of nature. For
example, holism has been embedded in developing new disciplines and theoretical
frameworks in recent decades, such as evo-devo and phenotypic plasticity (Pigliucci,
2014). In this book, we will go a step further, examining the nature and role of
exceptions in detail. We will describe whether the presence of rules is fundamental
for the biological system studied. In addition, we will review whether some instances
were omitted as part of rules due to errors in our appreciation of what the rule
should contemplate.

1.2.1 Some Basic Hierarchical Levels of Rules in Biology

We can only see some of the rules at the same level. There are differences in that
each rule encompasses specific given biological phenomena or groups of phenom-
ena (note: understand the term “phenomenon” as referring to a pattern, a mecha-
nism, or a process, as the case may be). Thus, we have different levels of rules
according to their degree or limit of competence. For this reason, it would not
make sense to consider a rule that explains everything. In any case, it would do so
12 1 A Big World of Rules?

from a general perspective since later, when diving in detail into the components,
we would have other, more specific rules. For example, as shown in Fig. 1.1, we
could start from integrative laws in biology, such as the group of laws of Mendelian
inheritance, to laws or rules about specific aspects of nature, such as the almost
fixed patterns of reproduction of a given clade or ways of performing instinctive-
based behavior. We will see later how these rules can still vary and not be
so framed.
Between one rule of a globalizing level and another more restricted one, there
is a potentially broad spectrum of other rules for the intermediate levels. In other
words, the jump or interval from one level to another often ends up being “opera-
tive.” This criterion means that these ranges and limits are generally established by
the researchers themselves, markedly influenced by the variability existing in liv-
ing beings (variability embodied mainly as the “bricks” necessary as a basis for
biological evolution). Thus, plotting or diagramming the interaction between lev-
els or their degree of inclusion can be challenging, and any attempt, whether illus-
trative or mathematical, will be minimal. However, as seen in Fig. 1.1, one way is
to plot these interactions as concentric circles from one level to another. As we will
see later, this graph has its basis in one of the classic ideas of scientific thought, its
construction, and change, which Imre Lakatos put forward. Later, we will see that
this illustration is limited when we examine the differences and dynamics between
rules and exceptions. However, it is valid, as far as this first excursion into the
world of rules is concerned, where we will first focus on the most global levels
(level I). It is often not easy for scientists to define which laws we could unfail-
ingly postulate as “safe” for biology, which we can say encompass biology as
a whole.
It has been mentioned that only three fundamental laws can be established for
biology (Box 1.2) since these would undoubtedly cover the totality of living beings
(Trevors & Saier Jr., 2010). Interestingly, the first of these laws asserts that biology
is not separate from other sciences that provide the foundational knowledge for it,
specifically chemistry and physics (Wayne, 2020). On its own, this first law of biol-
ogy would not enable an extraterrestrial entity to comprehend the essence of what
characterizes biology within our living system. However, an implicit law holds
value in being explicitly stated.
1.2 What Is a Rule? 13

Modified from Trevors & Saier Jr. (2010) and Dhar & Giuliani (2010). License: Own
Creation

The second of these universal laws of biology is that all living things are covered
by membranes. Here, it already focuses on something very characteristic of biology
by mentioning systems defined by their coverings, as is the case with cells and
membranes. This biological characteristic does not deny, of course, that physics is
excluded. Note that there is still no mention of DNA or RNA, i.e., a law that does
not highlight genetics. It could well have been posed as a universal law, also one that
we mention that all organisms are formed in their genetic composition by one and
the other. Nevertheless, that has not been the case.
14 1 A Big World of Rules?

The last of the laws makes explicit that all living beings have appeared through
an evolutionary process. It may be the law that reading it already reflects the exis-
tence of more than a form, a process that contains all living beings without excep-
tion, biological evolution (this, of course, also has a basis in physics and chemistry).
In other words, no organism arises by spontaneous generation, the creation of a
superior being, or appears from nothing by pure chance (even if this is an essential
ingredient before the beginning of the process when mutations are generated by
chance).
After seeing these three laws of biology, one is left with the desire to try to estab-
lish another one of equal importance, such as the genetics we mentioned. In any
case, the last of the laws indirectly contemplates the genetic basis in the evolution-
ary process, although not explicitly in its statement. Therefore, it is a problem to
limit biology to the scope of other basic sciences, such as physics and chemistry; in
fact, it is much more than the action or “sum” of these. It does not deny them, but its
dynamism exceeds both.
In this framework, biological theories are undoubtedly put forward, and they add
up to a level almost parallel to that of laws or principles in the aforementioned “level
I.” For example, the theory of evolution is the most comprehensive. Even with its
controversies in variants and details, as we will see later (e.g., greater or lesser
emphasis on the role of chance in mutations and the importance of epigenetics), it
is the paradigm that nucleates and organizes. It establishes a hierarchy among the
rest of the rules explicitly about biology (Ruíz & Ayala, 1998). In this sense, just as
we show concentric circles that indicate for biology the degree of inclusion of the
different levels of laws it presents, biology itself is at the center of the discussion
concerning other sciences. They encompass and influence it in their laws and rules
(Fig. 1.1a, white arrow).
Thus, we could go from the center, with biology, to the periphery, with chemis-
try, and above it, physics, and finally encompassing (or well on a par?) mathematics.
This relative directionality can be dual between biology and chemistry due to bio-
logical feedback in specific chemical processes (Fig. 1.1a, black arrow). For exam-
ple, living organisms produce rather complex molecules, such as DNA or RNA, not
outside the sphere of biology. Additionally, living organisms produce complex
chemical compounds, such as proteins, fats, and oils. It can then be added to chem-
istry in sensu stricto (inorganic and organic) those compounds not found in the
foundations of the periodic table of chemistry (biological chemistry). The biologi-
cal contribution to the atmosphere is clear since living organisms emit oxygen and
carbon dioxide molecules due to photosynthesis (still with incipient physiological
machinery) and respiration. Methane produced by the digestion and excretion of
urate and associated nitrogen-based compounds (a product of protein degradation in
many animal diets) is also added. Therefore, it is evident that the concentrations of
these gases in the atmosphere differ from what only strictly chemistry would pro-
vide outside of the biological (Fig. 1.1a, an arrow with dotted lines).
We could suggest a first concept regarding the feasibility of the occurrence of
rules. The probability of occurrence, approach, or application (depending on the
emphasis) of rules (general, globalizing) will be directly proportional to the range
1.3 Searching for Universal Rules in Biology 15

of coverage and influence of the latter; therefore, being more feasible in physics and
less, progressively, in the other sciences that it influences as in biology. The truth is
that biology, and in particular, the field of organisms (e.g., ecology, natural history,
behavior), is often seen in a reductionist way. For example, biology is an area of
science that hardly presents, at least in a clear way, principles that can summarize
and explain its characteristics comprehensively. However, this is different for biolo-
gists. Of course, more care must be taken in “generalizations” ‘because there is
more inherent variability in their patterns when dealing with living beings’ (e.g.,
limitations in stating the rules, the scope of the rules, and the possibility of excep-
tions). Indeed, the components of the organization of living beings, such as the
existence of species, populations, communities, and ecosystems, undoubtedly add
up to more complex levels. This complexity shows us that biology does not result
only from the sum of the effects of other sciences, such as physics and chemistry.
This implicit complexity of living systems makes the appearance of exceptions,
such as oddities in behaviors and morphologies, much more probable.
This perspective is encompassed within systems biology, which aims to explore,
in an interdisciplinary manner, the interactions between internal and external pro-
cesses within organisms and even beyond them. Unlike the classical scientific
method, which is based on the rejection of hypotheses, systems biology is based on
mathematical modeling of the processes of interest, which allows us to obtain predic-
tions of the state of that process (Tavassoly et al., 2018). This perspective opens the
door to detecting the presence of modellable patterns, which can be stated as rules.
In addition, this approach also favors the discovery of exceptions at certain levels.

1.3 Searching for Universal Rules in Biology

1.3.1 The Phenomenon of Emergence

Suppose we were behaving truly strictly and contemplated biology only from phys-
ics and chemistry. In that case, we could ask ourselves with much skepticism: Are
there no other laws for biology than those three already mentioned and those from
physics? We could reasonably consider for level I (or even a regulator of this, as a
“level 0”) the phenomenon of emergence. Emergence is a process where larger enti-
ties, patterns, and regularities emerge through interactions between smaller or sim-
pler entities that do not exhibit such properties (Bunge, 2003; Sawyer, 2005; Bizzarri
et al., 2020). In other words, and broadly speaking, the concept of emergence con-
siders that a whole is more than the sum of its parts (Francescotti, 2007; Bizzarri
et al., 2020). Emergence, of course, is not limited to living beings but also encom-
passes forms and patterns observed in abiotic components of the planet (and per-
haps of the universe?). As far as biology is concerned, the phenomenon of life as
studied in this science is commonly perceived as an “emergent” property of inter-
acting molecules, something that, in general terms, is already studied in chemistry
and which, in turn, reflects the particle interactions studied in physics. Thus, biology
16 1 A Big World of Rules?

could have a “Law of Emergence” that characterizes it as an area of science as a

whole, at least in terms of structural patterns (i.e., “form”).
Life itself could be considered an emergent phenomenon. Life is the most signifi-
cant source of complexity if we look at the progression of evolution, from the micro
to the macroscopic, as well as historical events (e.g., from the initial RNA and DNA
emergence to the more complex systems of communities and ecosystems). An
attempt is made to frame elements inherent to all living beings that define them in
their form and evolution. If we see life as a system with different levels, we need a
hierarchy of analysis to accurately describe the system (Emmeche et al., 1997). It
would be imprecise to look for a law that encompasses the whole system since the
relationships are dynamic between the constituent elements and change with the
level of systemic organization (Bizzarri et al., 2020). In other words, laws that
describe relationships at lower levels may need to be revised to describe relation-
ships at higher levels. Therefore, a law defined as a set of causal relationships
between the phenomena studied may only hold at some levels (Bizzarri et al., 2020).
On the other hand, there are emerging “structures” in many groups of living beings,
such as colonies and massive coordinated groupings, which can form true “superor-
ganisms” (Wilson & Sober, 1989; Hölldobler et al., 2009). Such is the case of the
conformation of something very complex, such as colonies of ants, bees, organized
flocks of birds, or schools of fish (swarming patterns). Thus, the phenomenon of emer-
gence can be at level I and at lower levels. The “theory” of emergence is something
that many physicists endorse. However, it is also controversial and has a tumultuous
history in science and philosophy (Pigliucci, 2014). This author highlights, “even if
emergence is only an epistemic phenomenon, there are good reasons to take it seri-
ously, for example, because it points to theoretical or methodological deficiencies that
make rigid reductionism unfeasible in practice if not in principle as such.” We find
patterns and regularities that repeat in nature, such as the ramifications of a circulatory
system, of a tree or a river, as well as analogies based on the Fibonacci series present
in the concentric helical structures in the arrangement of petals in a sunflower, shell of
a nautilus, water whirlpool, and spiral galaxy (Lüttge & Souza, 2019).
It is interesting to note that evolutionary theory and emergence theory are not
mutually exclusive visions but are based on different approaches that complement
each other. The theory of emergence does not attempt to explain evolution. However,
it shows the analogy between forms by arguing that there are emergent patterns in
common, repeated in both abiotic and biotic contexts and perhaps extending beyond
the planet.

1.3.2 On Some More Holistic Approaches

Connected with the emergence and within the framework of more general prin-
ciples, attempts have been made to obtain one that best encompasses all or at
least many of nature’s phenomena. This goal led to a “search for the holy grail.”
1.3 Searching for Universal Rules in Biology 17

An example is when attempts are made in science to explain opposite patterns

from the viewpoint of Eastern philosophy, even using concepts from the phi-
losophy of the Tao. For instance, the bestselling book “The Tao of Physics,”
authored by Fritjof Capra in the mid-1970s, highlights the parallels between
certain issues in modern physics, such as wave–particle duality, and the con-
cepts presented in the Tao philosophy, including the notion of complementary
opposites represented by Yin and Yang (Capra, 1975). It draws analogies
between these domains, showcasing the interconnectedness and shared princi-
ples between Eastern philosophy and physics. As much appreciated as strongly
criticized, the same author later took this vision to other books with an integral
look at the emergence and holism of life (Capra, 1996). Subsequently, in col-
laboration with Pier Luigi Luisi (Capra & Luisi, 2014), the author has shifted
their focus to biology within the framework of systems theory, including com-
plex systems. This approach emphasizes a holistic perspective and the concept
of emergence, which offers an integrative understanding of the organization of
life across various aspects and levels. While the value of these contributions
may be subject to debate, it is undeniable that they exemplify a nontraditional
pursuit of universal patterns.
In the same sense, there are other works with holistic approaches, always with a
bias toward oriental philosophy over the classical positivist scheme. Undoubtedly,
this approach already places these essays at the “limit” of science, even more than
what could be questioned in Capra’s contributions. We can mention as examples of
these approaches the study, with a more philosophical look, by Poggi & Ohsawa
(1986) on “The Order of the Universe” and the work of Barry (1993). Barry pro-
poses a holistic theory or vision of the universe to arrive at something that encom-
passes “almost” everything and, as he says, tries to integrate science, psychology,
and religion. Both studies are just two examples in a vast bibliography of such
approaches. At the level of the biological sciences, the Gaia idea of Lovelock and
Margulis (1974) is not different from these holistic views. These authors suggest
that living organisms interact synergistically with their inorganic environment in a
complex, self-regulating system. At first, it was a very controversial idea, branded as
teleological and somehow going against the principles of natural selection.
Nevertheless, certain modifications have been introduced with the assistance of
other disciplines, which have enhanced the robustness of the idea. However, it is
important to note that despite these refinements, criticisms of the concept still
persist.
To recapitulate, these are interesting approaches, but they are beyond the
scope of this book since they pretend to be all encompassing. Here, we will
examine, from the level of biology itself, its rules and exceptions, not above it.
At the end of the book, we will come back to this and see to what extent what we
analyze here is indirectly connected to complement these holistic “suprabiologi-
cal” views.
18 1 A Big World of Rules?

1.3.3 Biological Complexity: Controversial Rules

Defining complexity is challenging and has significant differentiating biases

depending on the domain under consideration (Chambers, 2015). Complexity is an
attribute of systems that alludes to the interrelatedness of the system’s components.
“Complex” should not be confused with “complicated,” which would be something
intricate that is difficult to understand. Complex systems are usually simple and not
complicated (Weaver, 1991; Adami, 2002; Bizzarri et al., 2020). Complex systems
form a functional “whole” with interdependent and variable parts. These systems
make up most of the world, from individual living beings to social systems and
many natural systems. The components proper to a complex system self-organize to
form potentially evolving structures exhibiting a hierarchy of emergent system
properties.
Controversies over what rules might be posited for biology sometimes become
very acrimonious. For example, McShea & Brandon (2010) explicitly postulated in
the title of their book “Biology’s First Law: The Tendency for Diversity and
Complexity to Increase in Evolutionary Systems” that the first law of biology would
be the increase in (taxonomic) diversity along with progressively greater complex-
ity in organisms, seeing both components as “a whole” on an evolutionary scale.
The idea postulated by McShea & Brandon (2010) is based on records and compari-
sons of how phylogenetic patterns and somatic complexity are associated over evo-
lutionary time. However, it has received several criticisms, most notably one on the
revision of the book by Bromham (2011), that almost tears the whole idea to shreds.
This author compares some phylogenies and the expected increase in complexity
that should occur with the increase in biological diversity, not finding clear support
for the rule proposed by McShea & Brandon (2010).
What is certain is that everything referred to as complexity is connected and
framed in a theory on which progress is being made (Chambers, 2015; Bizzarri
et al., 2020). Taking into account the ongoing discussions surrounding the role of
increasing complexity in biology, while also acknowledging the importance of sim-
plification within that framework (as discussed in Chap. 2), it becomes evident that
the quest to establish comprehensive laws for biology can be both enticing and pas-
sionate. However, it is important to recognize that such an endeavor is not without
controversy and valid questions, making it a challenging and debatable task.

1.3.4 The General Systems Theory and Systems

Biology Perspective

The issue of principles in biology has been addressed by Green (2015) in a review
that focuses on design principles in the context of general systems theory and sys-
tems biology. Her detailed analysis demolishes the false premise of other observers
seeing biology as a discipline lacking principles due to the variability, contingency,
1.4 Presence of Rules According to Levels and Areas of Biology 19

and complexity of living systems. Some researchers suggest that generalizations

can be made but that these are related to the hard sciences or are processes that
describe contingent outcomes of evolution (Beatty, 1995). This apparent shortcom-
ing of biology does not make it weak as a scientific discipline but separates it from
other fields (Green, 2015). Contingency would not be a rule in biological systems
either, and in fact, there are examples where generalizations can be seen. Recall, for
example, the universality of the genetic code in all living beings or the use of ATP
as energy currency in physiology. We also know that there are general theories, such
as the cell theory and the predator–prey theory of the Lotka–Volterra model, among
others. Thus, Green suggests that generalizations can be made in biology without
generating a reductionism that threatens the discipline’s autonomy. She also distin-
guishes different types of generalizations and highlights constraint-based general-
ity, a kind of generalization resulting from restrictions on systems to show other
configurations or behaviors. Thus, a group of systems shares characteristics through
formalized dependency relations, although the restrictions limit and make specific
possible spaces. The restrictions make it easier for the biologist to understand the
reason for the presence or absence of patterns in nature. Generalization in sciences
such as biology is possible, but considering its particularities and knowing that the
level of generalization may never be compared with other, more complex sciences.
This divergence creates an opportunity for generalizations with certain precautions,
where the presence of exceptions prompts a reassessment. Such a reassessment is
not necessarily negative but rather invites the generation of new ideas and construc-
tive relationships within and between disciplines. It encourages a fresh perspective
and fosters innovation by embracing the potential for novel insights that arise from
exceptions and deviations from generalizations.

1.4 Presence of Rules According to Levels and Areas

of Biology

1.4.1 On “Minuscule” Rules: Certainties Even

in the Narrowly Defined

The general principles in biology should be approached with a perspective of “flex-

ibility” that is more pronounced compared to other “hard” sciences. That is, know-
ing that there will be logical limitations in the case of not being able to cover 100%
of the variability presented by organisms. Variations and rarities will be found at
more restricted levels of the norms or regularities surrounding us. Returning to
Fig. 1.2, we are more likely to encounter daily changes at the levels encompassed
by I (e.g., II, III, IV). In this sense, an analysis of rules and principles is sufficient
for the general, as summarized in the works cited above, or whether it would be
worthwhile to delve into these much more specific levels. Ultimately, whether we
acknowledge it or not, the inherent nature of the natural world forces us to engage
20 1 A Big World of Rules?

Fig. 1.2 Levels of rules taking into account their degree/limit of inclusiveness or competence

with rules at lower levels, regardless of our inclination or interest in doing so. They
are not perhaps made explicit as “laws” (a term for a more globalizing level) but as
“regularities” or “patterns” depending on the preferred term in the area of biology
in which we find ourselves. Thus, for example, if we were to take a level II, we
would zoom in on specific details of the surrounding world, such as the rules known
as “eco-geographical,” which will be discussed in Chap. 4.
On the other hand, at a more “modest” but no less critical level, there are affirma-
tions from tested hypotheses, which then remain as rules of a lower level (e.g., III,
IV). They are “mini rules” compared to those already mentioned, which are of
greater scope. In short, within a specific discipline, the researcher usually does not
question or consider the applicability of level I rules but takes them for granted. For
example, we focus on an entomologist and specialist in reproductive biology. In that
case, he will not consider whether insects have a cuticle and six legs since these are
implicit rules (synapomorphies) to which they all conform. However, he will con-
sider more complicated things, such as those referring to the mating success of
males. For example, remember that as a “rule,” it is common for sperm precedence
in insects to favor the second male generally or that they tend to be a very promiscu-
ous group. These “mini rules” on which the researcher bases arguments and new
questions are vital foundations for advancing knowledge. For example, let us imag-
ine that suddenly someone was to point out that, at the moment of sperm transfer,
the male of the dragonflies under study no longer grabs the female by the dorsal part
of her thorax (i.e., the “mini rule” for mating in these insects). In contrast, the male
stands beside the female without physical contact and only mates with the coupling
of the aedeagus, which they use to transfer sperm. This observation would be a
novelty in this sublevel of their biology. This mini rule would not be taken for
granted by the researcher as it has been done thus far.
Therefore, all levels will have certainties when starting an investigation or orient-
ing oneself to discover something that fits or does not fit into all that is known for
that particular level. Interestingly, the rules have mainly emerged from studies per-
formed more than a century ago and, in many cases, in publications that were not
written in English. Therefore, it is expected that there may have been some misrep-
resentations of the original study and statements over time because the original
1.4 Presence of Rules According to Levels and Areas of Biology 21

work needed to be read or translated correctly. This problem brings us to a central

question. How much time has to pass before a rule begins to be questioned or
refuted? Refuted because it is considered erroneous or because of the appearance of
many exceptions to the original idea. A simple and obvious answer is that the more
time passes, the more likely these changes will occur. The social and scientific con-
text, changes in the discipline itself, or the knowledge of other associated areas,
among other factors, would also be added to the moment of its postulation, as we
will discuss later.

1.4.2 Laws, Rules, and Patterns

Box 1.1 summarizes various synonyms for rules, from laws to patterns and theories
or principles. Although they are taken as synonyms, each word has its own specific-
ity. As a scientist, it is necessary to pay attention to its meaning to express oneself
adequately. Additionally, terms from other sciences, such as mathematics, are
included, which are linked to those shown in the table as the main ones, for exam-
ple, theorems and axioms. The most widely accepted meanings are shown, although
it is clearly difficult to reach a consensus on which one or ones are more in line with
each level. However, it could be considered that the laws belong to level I, rules to
level II, and patterns (or “regularities”) to level III. Theories would be closer to level
I, although with potential components of level II concerning the presence of excep-
tions. The “fundamental” laws of biology, such as those exposed in previous para-
graphs (Box 1.2), do not accept exceptions. Just try to imagine that living organisms
that did not follow the laws of physics and chemistry were not composed of a mem-
brane at the cellular level or had not undergone any evolutionary process during
their existence or those of their ancestors. If exceptions to this level of core laws
appear, we would be in serious trouble as a science.
Thus, together, these fundamental laws form a scientific paradigm (along the
lines of Khun) or a central nucleus (following Lakatos), which in turn are covered
by other principles that will eventually be modified sooner or later, either by
advances in scientific knowledge or by biological evolution itself. Beyond these
epistemological components, what is certain is that at more specific and limited
levels, such as rules, we can already see the presence of exceptions. At this level, the
variability inherent to biological systems has an impact on “continuous” situations
or cases with qualitative “ranges” that deviate from an average value or “norm.”
This pattern is valid even if we limit ourselves to a rigorous statistical appreciation
rather than an epistemological one. We must be clear that those exceptions are not
due to misinterpretations of the rule’s statements (explicit and implicit) or its range
of coverage in the study system.
Finally, we will have the patterns or, if you will, “regularities” of a lower level
(below III), which are not usually expressed in the papers as rules. Even if they are
implicit rules, in practice, this term is not used for a more limited level of study.
However, these regularities are observed as “modal” (i.e., not fixed) ways of pre-
senting a particular event or state.
22 1 A Big World of Rules?

1.4.3 Visiting Some Witness Cases

1.4.3.1 Classification of Living Beings

When taxonomic keys are made for determining species or other taxonomic catego-
ries, the elements used indirectly trace differences between the groups included.
Plesiomorphies and apomorphies summarize patterns and regularities that give enti-
ties to a taxon. The “volatility” that the history of taxonomy may have had was
partly based on not having adequately contemplated characters, patterns, and regu-
larities that reflected genuine phylogenetic relationships. Currently, the degree of
taxonomic error has decreased since not only phenotypic characters are used to
establish homologies but also a practical and powerful component is added, namely,
molecular analyses (Yang & Rannala, 2012; Lee & Palci, 2015).
Even so, morphology aspects are essential to define (as a level I rule) a particular
group. For example, “all cnidarians are diploblastic.” In other words, their layers are
composed of ectoderm and gastrodermis (endoderm). Indeed, the mesoderm has yet
to appear on this evolutionary scale, as it will later appear in flatworms. None of the
more than 11,000 species of cnidarians is known to be triploblastic (Giribet &
Edgecombe, 2020; Schierwater & DeSalle, 2021). Thus far, there would be no
exception to this level I rule in this phylum. Thus, this apomorphy of the phylum
Cnidaria is intrinsically a rule. It has stayed the same with either the historical time
of our knowledge of biology or evolutionary time. Examples such as this could be
listed for all invertebrate taxa, vertebrates, plants, fungi, protists, and bacteria,
among other groups (Fig. 1.3). In each clade, a set of characteristics will allow us to
arrive at a general statement covering all the species contained in it. Exceptions to
this high level of rules are not expected in general. However, we will see in the next
chapter that they can appear, which has evolutionary and phylogenetic importance.

1.4.3.2 Behavior and Communication

Behavior is fascinating as a source for analyzing the possibility that it involves, and
serves to exemplify, different levels of rules. Within animal communication, court-
ship in animals occupies a special place due to the richness and complexity of the
signals involved during male–female interactions. It is clear that in each species, the
sexual behavioral repertoire is not composed of a series of random or highly vari-
able patterns but of “modally” established or stereotyped patterns. Indeed, courtship
serves directly or indirectly as a prezygotic mechanism of specific recognition and
interspecific isolation. However, in addition to having functions for specific recog-
nition, the evolution of courtship and sexual behavior is undoubtedly under sexual
selection pressures such as mate choice (Andersson, 1994; Houck & Arnold, 2003;
Kallman et al., 2015). Then, despite behaviors being stereotyped, it is expected that,
for example, males will show high behavioral plasticity or exhibit courtship patterns
that vary in intensity, which may lead to exceptions to the stereotypes expected for
their species. Curiously, the exception may be an “extreme” within a quantitative
1.4 Presence of Rules According to Levels and Areas of Biology 23

Fig. 1.3 Major rules in metazoan phylogeny. Animal phylogeny with phyla at the tips and major
clades indicated at nodes. (Modified from Giribet & Edgecombe, 2020). Characteristics that group
major clades are indicated in colors and can be considered “rules” for the groups considered.
Free images from https://www.phylopic.org

gradient, i.e., not something “separate” from other values on a continuum. However,
to our eyes, it may be perceived as something qualitatively discrete and different
from the rest.
An example of this behavioral plasticity can be observed in scorpions of the spe-
cies Bothriurus bonariensis, distributed in South America (Mattoni & Acosta, 2005;
Ojanguren-Affilastro, 2005). Like most species in this group, these scorpions have an
elaborate courtship consisting of ritualized behaviors (Peretti, 1993). However, there
are differences in behavioral patterns between populations of the species, where
males may vary the frequency and duration of some stimulatory behaviors (Olivero
et al., 2015). Even when individuals from two different populations interbreed, males
may modulate their behavior according to the “demands” of an exotic female from
another population. This example shows us that although there is a courtship pattern
that would represent the rule in these scorpions’ reproductive behavior, there are
exceptions that allow populations to continue interbreeding with each other.
On a more globalizing level, could a law referring to communication be added
to all living beings? One could be that “every living being communicates,” at least
24 1 A Big World of Rules?

with its peers (Scott-Phillips, 2008). The organism may exchange information with
other individuals of its species, colony, and even with other species in contexts of
predation or defense. This communication could be basic, including tactics and
chemistry, for example, in significantly lower organisms and then in higher evolu-
tionary levels gradually enriched with displays of rituals, stereotyped body move-
ments, and other much more complex ones. The question worth asking is: If a living
being does not communicate, would it not be a living being? For example, do algae
or plants also communicate? Recent work has shown how plants communicate, a
topic we will address further in Chap. 6. We could draw rules from behavior that
approach level I (Fig. 1.2) for all living beings. This option, however, requires men-
tal flexibility to appreciate these new insights. Fortunately, it was formed in recent
years (e.g., communication used to be an attribute of animals, but not of plants or
even lower organisms such as bacteria—Keller & Surette, 2006; Won et al., 2020).
Suppose we focus, for example, on language in humans. In that case, it is known
that all cultures handle a specific scheme of symbolism, a form of writing (whether
graphic or based on a conventional alphabet in its form) derived from a language and
the words that compose it. We could then say that there is a law of universality of
language that governs the current human species in terms of “the existence of a lan-
guage in all cultures” (Pozzo & Soloviev, 2011). This does not admit an exception as
such, except for teratological cases in which an individual cannot assimilate the lan-
guage patterns of his or her culture (e.g., problems in the pre and/or postnatal develop-
ment of Broca’s and Wernicke’s areas) (Pozzo & Soloviev, 2011). At another level of
analysis, within each language, we can find rules, such as grammatical and ortho-
graphic rules. Exceptions that might occur in particular contexts could be accepted. In
turn, at more specific levels, we could find patterns of written expression that are more
specific to certain populations, up to the formation of deviations or dialects. These
more restricted patterns do not reject the previous levels of rules but add or modify
certain aspects of the language that make them even more labile and changeable from
one territory to another. Even if we focus on “nonverbal” communication (Duncan Jr.,
1969), we also recognize constitutive elements that are repeated in different cultures
and that could allow us to extract laws or rules, at least in general (e.g., facial expres-
sions). Already at a more limited level of each village culture, specific patterns of
“nonverbal” communication, such as what we have already mentioned above for “ver-
bal” communication, could be seen as exceptions to these rules (Jena, 2020).

1.4.3.3 Rules and Basic Plant Patterns

In addition to more recent striking topics, such as the communication we will dis-
cuss later, specific rules and patterns can be found in plants, which can be assigned
to certain levels. For example, a level I rule for the Plant Kingdom is that they are
characterized by being autotrophic species capable of producing food from inor-
ganic matter. They possess chloroplasts and related organs and use a pigment called
chlorophyll to take light energy from the sun and use it for photosynthesis (Curtis
et al., 2008). If an organism of this Kingdom does not photosynthesize, then it
1.4 Presence of Rules According to Levels and Areas of Biology 25

implies the presence of exceptions. Some plant species are not photosynthesizing
but parasitic at different levels (Nickrent & Musselman, 2004; Nickrent, 2020).
Examples are Epifagus americana, Monotropa uniflora, and plants of the genera
Cuscuta and Rafflesia (Hidayati & Walck, 2016).
From this basis, we can examine more punctate things that will ultimately, as
always, end up being the synapomorphies that characterize and give meaning to a
given clade. For example, algae may be cellular or tissue-forming and photosynthe-
sizing, but they do not have xylems such as vascular plants or the ability to tolerate
environments far from water (Curtis et al., 2008). The same could be the case at the
level of particular characteristics for marchantiophyta or liverworts (pores instead
of stomata and elateria to disseminate spores), bryophytes or mosses (sugar and
water transporting cells, gametophyte with multicellular rhizomes, capsule with
operculum where the spores come out), phyllicophytes or ferns (compound leaf
with leaflets on both sides, young leaves rolled in a spiral, sporangia on the under-
side of the leaves, antheridia formed by a superficial cell that has an apical cell as an
operculum), spermatophytes (stem with secondary growth, branching from buds in
the leaf axils, ovule formed by female gametophyte, nurturing substance and tegu-
ment, male gametophyte highly reduced), and in turn among spermatophytes, on
gymnosperms (male and female reproductive structures in cones, ovules on the
upper side of the scales of the female cone, male gametes carried by the pollen tube
to the ovocell) and angiosperms (complex compound flowers, ovule protected by a
carpel that will form the fruit, reduced pollen grain with three haploid cells, female
gametophyte also reduced in the form of an embryonic sac, complex wood with
vessels and supporting structures, phloem that helps the circulation of sugars)
(Curtis et al., 2008). Therefore, a series of patterns can be recognized that conform
to the level I rules in each case. Suppose we find exceptions to the rule that sum-
marizes the characteristics of each plant form. In that case, they could be teratologi-
cal or evolutionary-derived traits.
Plants also have evolutionary processes and characteristics that were only
recently considered present in animals, such as sexual selection (Stephenson &
Bertin, 1983; Cocucci et al., 2014) or, as we previously said, communication
(Karban, 2015). Indeed, plants demonstrate the presence of such patterns and mech-
anisms with their particularities. It is not by chance that many of the most striking
plants are those with solid interactions with animals, such as those subject to coevo-
lution by pollination, including cases of mimicry (e.g., in orchids) (Schaefer &
Ruxton, 2009). In a phylogenetic framework, many of these species are actual “tax-
onomic exceptions” within a clade, as we will see in Chaps. 5 and 6.
The point is that wanting to define sharp divisions at the phenotypic and behav-
ioral level between plants and animals has been challenging (Weller, 1955; Paps,
2016; Glibert et al., 2019). One noticeable trait is that referring to photosynthesis or
not. However, it is now known that what concerns the ability to move, communi-
cate, or better yet, the “form” each group uses in each Kingdom is insufficient to
make such a division. Fungi are a clear example of this difficulty when classifying
due to multiple “intermediate” characteristics, something we will go deeper into in
Chap. 5. Better knowledge about the origin and function of many “rare” aspects of
26 1 A Big World of Rules?

plants has gradually made this functional difference between them and animals
somewhat “fainter” (Lloyd, 2011). It should be recalled that in the past, sponges and
cnidarians were even included in the Kingdom Plantae. These animals were con-
fused with plants mainly due to their immobility (or low mobility), “branched”
body appearance (with rhizomes and stems), and colorations (e.g., green in many of
them due to symbiont algae). Aristotle, Pliny the Elder, and other ancient naturalists
believed that sponges were plants precisely because they were sessile and had little
detectable movement. It was not until 1765 that John Ellis first observed an actively
provoked water current within their bodies, and they came to be considered animals
(Ellis, 1765; Ruppert & Barnes, 1996).

1.4.3.4 When It Is Still Difficult to Establish Rules: The Case

of “Ecological Genomics”

When talking about rules, we need to remember that many of them are “under con-
struction,” i.e., we are still trying to integrate evidence from nature that will allow us
to establish them as rules per se. These situations occur particularly in relatively new
areas of the biological sciences, such as evolutionary developmental biology (aka
Evo-Devo) or a new field, ecological genomics (Van Straalen & Roelofs, 2011;
Raghavender, 2021). The problem lies in the fact that, with a broader view, research-
ers detect exceptions to the “potential” rules they try to identify in their models. For
example, in their study on “exceptions to the parallel genetic basis,” Elmer & Meyer
(2011) argue that “the many exceptions suggest we do not yet have any rule.” They
reach this conclusion by analyzing numerous cases of parallelism and convergence in
evolution, finding that there are too many exceptions. There must be many more cases,
such as the one cited, perhaps some of which we still need to discuss or have yet to be
made public in the scientific community. That is, rules are still “cooking” from bodies
of ideas and data. Through more detailed analysis, on par with a more integrative
vision, researchers identify so many exceptions that, in the end, they consider it pre-
mature to define a particular rule. Indeed, the situations where previously established
rules are later revised or refuted, as discussed in the previous items, or others under
construction, as well as the influence of exceptions, are closely connected with episte-
mological concepts. At this point, it will be helpful to review below some of the most
classical epistemological frameworks linked to the general problem of rules in science.

1.5 Linking Rules with Epistemology: Changing Paradigms

The changes in scientific thinking and methodologies over time have been the object
of the study of epistemology. The ideas proposed by Khun, Lakatos, and Feyerabend
come from authors contemporary to each other at a time of much debate about the
foundations of modern scientific thought. This book aims not to elaborate on the
theory of scientific thinking in biology. Nevertheless, we will review some valuable
1.5 Linking Rules with Epistemology: Changing Paradigms 27

concepts to detect, evaluate, and discuss the presence of regularities and exceptions
in biology as an essential part of its nature. From this, we will contemplate its
dynamics and draw valuable conclusions in basic and applied research.
The ideas about scientific thinking of these authors and others have been somewhat
exposed (and learned) as “opposites” when they are not mutually exclusive, at least in
their totality. As we have previously stated, the “Khunean” paradigm encompasses
ideas about rules and theories. Indeed, when we speak of rules, we refer directly or
indirectly to a body of ideas that are part of scientific thought for a given time (Kuhn,
1970). As we will see in Chap. 2, crises and paradigm shifts in biology are associated
with modifications in what are considered to represent the rules and their exceptions.
In a certain way, the “Lakatian” scientific research program was reflected when in
Fig. 1.2, we plotted “levels” of rules. As he says, it would be a complication in science
if essential laws of biology were demolished (Lakatos, 1978). This connects with the
“moment of crisis” postulated by Khun. Likewise, the scientific system becomes more
labile as “real” exceptions (i.e., not the product of misinterpretations or slight extrapo-
lations of the author’s original ideas) accumulate, resulting in principles of the central
core behaving as parts of the protective belt (i.e., “variables”).
In every discussion in scientific thought, the so-called construction of “para-
digms” (as well as their strengthening, weakening, and renewal) takes place at any
level of observation. Feyerabend was disruptive in his ideas. He postulated scientific
anarchism, highlighting the limitations of a structure that wants to regulate or con-
trol processes and mechanisms, such as society or scientific thought (Feyerabend,
1993). Some consider that the anarchism proposed by Feyerabend was more a call
for attention than premises to tear down any basis of science.
The idea that rules and exceptions are separate entities can be dismissed. In other
words, we should always expect all laws, rules, or associated terms to have excep-
tions. Therefore, the point is not to uphold a naive belief that rules do not have
exceptions, especially when discussing biological rules that are not at level I.
In contrast, the aim is to highlight the dynamic coexistence of rules and excep-
tions. This component, dynamics, is critical in a science such as biological sciences,
which, by its very evolutionary basis, implies modifications of patterns. Moreover,
the value of exceptions alone, even if we were sure that they would never increase
in number or qualification to overthrow a preexisting rule, deserves to be high-
lighted to advance further studies on rarities in biology. In other words, to know
“what is” an exception, one must define and show something of the vast and contro-
versial universe of rules. In the next chapter and Chap. 5, exceptions will have their
presentation.
It is important to highlight the significant influence of confirmation bias in sci-
ence. Confirmation bias is the tendency of people to seek or interpret information in
a way that supports their current beliefs (Nelson & McKenzie, 2009; Oswald &
Grosjean, 2012; Mercier, 2016). This bias is constantly at play when evaluating
whether a rule is confirmed in a study. This can occur either by confirming the rule
in its entirety or by modifying it according to new evidence to make it more “modal”
(i.e., not so black and white). As we will return to later, exceptions are sometimes
not perceived if the researcher has confirmation bias. Indeed, the researcher might
28 1 A Big World of Rules?

unintentionally design the experimentation methodology or interpret the results “to

confirm” the rule, pattern, or hypothesis that supports his preestablished ideas
(Oswald & Grosjean, 2012). It is expected that students, who still need to exercise
the critical view toward ideas and information they are incorporating, tend to fall
into this bias. For example, a student may focus all his/her attention on analyzing
how the data from the study “fit” with what is “already known” (e.g., comparing it
to current paradigms, influential papers, fashionable topics in the discipline, ortho-
dox mentors, etc.) instead of using them to critically analyze them objectively and
relativize their hypotheses. A colleague used to tell us: “There is nothing better than
overthrowing a previous traditional theory or idea with the contribution of your
data.” This opinion connects with Kuhn’s classic ideas about the “crisis” moments
that precede a change in a given paradigm (Kuhn, 1970; Andresen, 1999; Anand
et al., 2020). We will return to the issue of confirmation bias later.
The reaction of researchers to changes in their postulates can be very variable,
ranging from acceptance to a fierce defense of their previous ideas. Here, we will
highlight the positive side of being receptive to change. For example, we see how
recently the physicist Juan Maldacena managed to unify quantum mechanics and
relativity with his studies embodied in String Theory (Maldacena & Susskind,
2013). Interestingly, this scientist claims, “if my theory is disproved, it would still be
a scientific advance.” This comment is a precious synthesis of open-mindedness
and the view that potential changes are the key to scientific progress. Some people
believe that all scientific evidence is valuable, whether it refutes or supports a
hypothesis, is significant or not. However, there is an implicit bias among research-
ers with a false premise that if the idea or working hypothesis is refuted, the data
obtained have no scientific validity or are useless. This conclusion is a prejudice that
must be eradicated, and the valuing of “negative data” in science should be promoted.
In the field of biology, Ruppert & Barnes (1996) end their chapter on Perspectives
in Phylogeny, in their classic book on Invertebrate Zoology, with an encouraging
paragraph for students and specialists: “We encourage students interested in the his-
tory of life to critically evaluate our cladogram and any others they encounter. Let
us welcome new ideas but let us analyze them carefully.” Ultimately, these open
ways of thinking promote the study of everyday phenomena in biology from differ-
ent perspectives and encourage us not to see rules and exceptions as watertight
compartments but as subjects to a dynamism that is worth discovering and analyz-
ing in detail.

1.6 Evolutionary Theory as a Driving Force for Changes

in Biological Rules

There is one point, at least in biology, that has had historical implications for the
changes in rules, postulates, and patterns that were initially proposed: the discovery
of an evolutionary background. Systems biology was a developing field before
Darwin’s Origin of Species provided a unifying framework. At that time, taxonomy
1.6 Evolutionary Theory as a Driving Force for Changes in Biological Rules 29

was the most relevant discipline, and it is evident currently that the lack of an evo-
lutionary basis has become a significant weakness. Symbolically, it would be like
building a house without a foundation or building it on the sand. There are plenty of
examples around us to illustrate what we have mentioned.
For example, on a walk around our city’s lake, we observed a pair of mallards
(Anas platyrhynchos). The male of this species has bright green colors on his neck
with a white collar. The female, on the other hand, exhibits duller colors. These dif-
ferences in the phenotype of the sexes, known today as sexual dimorphism, could
only be explained by Darwin’s work. As a result of sexual selection, males possess
these colors as ornaments to be chosen by females. In other cases, armaments, such
as horns, are used for competition between males to access females. These ideas
were not embodied in a theory or paradigm at the time of Linnaeus. Linnaeus’s defi-
nition of species was based on morphological similarities, so it should not be strange
that he classified males and females of the same species as belonging to different
species.
Something similar happened with other taxonomists and animal groups, with
iconic examples of animals such as the anglerfish (Cryptopsaras couesii). This fish
inhabits from 500 m depth in all oceans (Shimazaki & Nakaya, 2004). The male of
this fish species was elusive to researchers, who later realized that it was tiny and
resembled a sperm sac attached to the female’s body. This pattern is known as sex-
ual parasitism and is related to the difficulty of mating in deep environments (Vieira
et al., 2013). Another example is the argonauts Argonauta argo, pelagic octopuses
that live in warm oceans. Members of this group exhibit marked sexual dimorphism
with dwarf males that are difficult to find in the wild. Females are capable of secret-
ing a calcareous structure to care for their eggs. Conversely, males do not produce
this structure and present an extremely long hectocotylus or copulatory arm
(Battaglia et al., 2021). This example of sexual dimorphism in animals shows how
“certainties” in specific disciplines, such as taxonomy, are relatively labile.
Currently, everything is “easier” to understand with the contribution of molecu-
lar genetics. Many changes in the valid names of species and changes to synonymy
have been promoted by the lack of a solid basis within a framework of biology (e.g.,
evolution before Darwinian times) or on specific biology of the group (e.g., species
with coloration polymorphism). Another iconic example is the so-called “birds of
paradise.” These birds, which are very common in Oceania, were believed to come
from a heavenly place. The natives of these lands gave the explorer Fernando de
Magallanes specimens without legs, as they had cut them off to make decorations.
Magallanes did not understand this, as he did not speak the native language.
Magallanes took the specimens to Europe, and a “logical” explanation was con-
structed as to why they had no legs: these birds flew continuously in the sky and
only settled down to die (it was believed that they came from paradise and fed on
dew) (Beehler, 1989; Kirsch, 2006). Indeed, Linnaeus classified the great bird of
paradise with the specific name “apoda”: Paradisaea apoda (Kirsch, 2006), a sig-
nificant error considering that we are talking about the father of taxonomy. A total
absence of basic knowledge about the biology of the organism and much imagina-
tion were factors that played a significant role in this misunderstanding.
30 1 A Big World of Rules?

In his excellent book “The Discovery of Animals” (1982), Herbert Wendt shows
many classic examples of misinterpretations of various iconic animals regarding
their origin and initial taxonomic position. Examples include the birds of paradise,
stories of the discovery of monkeys, and the legends of unicorns and sea monsters.
All of them had been initially contemplated without an evolutionary paradigm. This
lack of a rigorous scientific observation method made many considered authentic,
even for hundreds of years. If we pay attention to the years of those initial findings,
they all date from an almost “primitive” stage of biological sciences. Currently,
some aspects linked to cryptozoology can “replicate” a certain degree of imagina-
tion as it existed in those times.
However, today, it is easy to criticize these “mistakes” from our position with a
vast knowledge of evolutionary biology, phylogeny, taxonomy, and molecular and
developmental biology. We are still determining how many mistakes made today,
while establishing a rule, will be studied and ironically criticized a century from
now. Imagine we could travel back in time, without any present knowledge, and see
in a Precambrian time that the unique aquatic life we find there could later move
onto land or even into the air. It would be absurd. The idea of an “amphibian” would
not even be in our minds, much less life in a desert or the flight of an organism
called a dragonfly, pterodactyl, seagull, or bat. These pre-Darwinian historical
examples help us to understand how biology changed in its fundamental bases.
These changes occurred thanks to evolutionary ideas to such an extent that, as we
have already seen, they are proposed as one of the three fundamental laws of biol-
ogy (100% level I). Because of evolution itself, biology brings a series of often
unpredictable changes, which contrasts with other “hard” sciences such as physics
or chemistry.

1.7 On Mathematics and Contingency: Does It Weaken

Evolutionary Predictions?

In mathematics, there are theorems, which consist of a proposition that can be logi-
cally proved from an axiom or from other theorems that were proven in advance
(Manoukian, 2012). Thus, once stated, a theorem will not be proven in the short or
medium term. Recently, the English mathematician Andrew J. Wiles was awarded
for proving Fermat’s theorem, one of the greatest mysteries of modern mathematics
(Kleiner, 2000; Hellegouarch, 2001). Fermat was a great mathematician who noted
in the margin of a book that he had figured out how to solve his theorem but did not
have enough space to detail it. Thus, the challenge among mathematicians began to
solve such a problem. It took them 350 years to solve it. Fermat’s theorem is used
in Internet encryption, and solving the theorem will enable the development of new,
more secure forms of encryption. In physics, there are many examples of predic-
tions that take time to demonstrate. In the 1930s, Albert Einstein predicted the exis-
tence of gravitational waves (Einstein & Rosen, 1937). However, it was only in
2016 that their existence could be demonstrated, in this case in the teamwork of
1.7 On Mathematics and Contingency: Does It Weaken Evolutionary Predictions? 31

great global scope at the level of research and costs, in the scientific project working
with the instrument called the Laser Interferometer Gravitational-Wave
Observatory (LIGO).
In the two examples mentioned above, a result is predicted and eventually proven.
This raises the question of whether biology is on a different plane, in another scien-
tific context, or whether the same can be done. That is, it could be supported by
hypotheses that can be falsified in the short term and by much more speculative
theoretical bodies that will be confirmed only in the medium or long term.
Meanwhile, this will be provisionally accepted by the scientific community as a
“rule pending verification.”
For example, within the world of morphology, Olson (2012) analyzed animal
teratologies as parts of a morphospace in the form of a range of “morphological
possibilities.” Much of the empty morphospace can come to be imagined, although
not always possible (e.g., because of ontogenetic constraints), although others might
come to be predicted. An example on a much smaller scale was the moth predicted
by Darwin upon encountering the orchid Angraecum sesquipedale from Madagascar.
Because of its unusual morphology and based on plant–pollinator coevolution, that
portion of morphospace was imagined and predicted by Darwin; years later, the
moth was found. These examples and the notion of morphospace will be further
elaborated in Chap. 5.
There are an increasing number of studies in mathematical biology where mod-
els are applied to specific problems, practical to predict certain behaviors of the
phenomenon under analysis. However, we are still far from what the “hard” sci-
ences can predict in their respective fields. Paradoxically, or perhaps not, this limita-
tion, or rather, this close and necessary link with the almost immediate factual,
makes biology especially interesting and exciting. The wrong label of “less exact”
science is a biased perspective from observers coming from other disciplines.
Perhaps we are currently concerning the use of models and their predictions, as
Linnaeus was with those species with remarkable sexual dimorphism in his time.
That is, learning and waiting for new theoretical, conceptual frameworks that pro-
vide further cohesion to the tremendous existing biological diversity, at the level of
patterns and mechanisms, in any of its branches.
It should be noted that at this point, what we comment on is where Gould’s
(1989) postulates on the phenomenon of “contingency” in biological evolution
invites us to reflect on what is possible and feasible at the level of causes and conse-
quences. For example, if we rewind the past and repeat the evolutionary process of
a particular ancestral taxon from the beginning, it will likely not lead to the taxa and
lineages that we know today. This situation is because contingency is a potentially
robust factor in the evolutionary process, among other reasons, due to the improb-
ability of tolerable mutations repeating themselves in the same way during their
repetition.
Extrinsic contingencies have also been vital in partly shaping what we see in
evolution. Evolution would have followed another course if those events had not
occurred or did occur but with a slightly different impact. Although questionable,
contingency and its role in biology relativize some “certainties” of what evolution
32 1 A Big World of Rules?

was and would be if situations could be replicated on or outside the planet.

Interestingly, could contingency be a concern for physics or chemistry (excluding
biochemistry) if their histories for certain phenomena (compounds) could be traced
back to their beginnings? Certainly not. This finding might be relevant since we
might have other concentrations of chemicals on the Earth today. Nevertheless,
would the components of the periodic table of elements be any different? Would
there be organic compounds that are currently unknown, while others that are known
would no longer appear in the “new Table”?
For physics, it is postulated that in “other” universes, there could be other laws
that govern it. For example, matter would behave differently from the one we cur-
rently know. In biology, however, the impact of “rare” events would seem much
more robust since evolution is a constant process and permeable to such extrinsic
contingencies, in addition to the low probability of tolerable mutations as intrinsic
causes. This situation marks a new difference between biology and the “hard” sci-
ences regarding the predictability of future phenomena.
It is interesting to note that if a contingency is held to be a fundamental factor in
biological evolution, then life itself and many subsequent evolutionary events have
arisen more through “exception” than “norm” types of processes. Furthermore, as
we will see in the next chapter, even leaving aside the “contingency” factor and its
predictions, we will find that exceptions are still at the origin of many (if not all)
evolutionary processes.

1.8 Possible “Principles” on the Nature of Biological Rules?

We have seen definitions, approaches, schools of thought, and general and biologi-
cal examples of “rules.” As we have said, they are not static but rather dynamic.
Especially in biology, rules are not fixed elements. They are modified to a greater or
lesser extent and can be rejected. As we will see below, changes can occur in a
“time” context. For example, in the historical study of biology, something is easily
understood from the epistemological approach. However, changes in the scope of
rules also usually occur in a “time” context inherent to biology, such as evolutionary
history.
Furthermore, this occurs in the context of “space,” where the vast geography of
our planet may mean that rules cannot be applied everywhere. To these two contexts,
we add the “group” context, where in the following chapters, we will see how certain
rules may or may not apply to some specific clades within a given taxon. In this
framework, the question arises: Can we posit “laws,” principles, and norms for the
dynamics between rules and exceptions in biology? If so, could these also encompass
other areas of knowledge, such as physics and chemistry? In this scenario of ques-
tions, if we play with the duality “rule-exception” and its fundamental dynamics, we
could posit different postulates according to the dynamics of rule and exception.
1. Every current pattern or rule began as a rarity or exception, respectively: In
evolutionary terms, this makes sense because adaptations that spread in a
1.8 Possible “Principles” on the Nature of Biological Rules? 33

population and species do not arise simultaneously and massively in all individuals.
In contrast, the basis of evolution (sometimes not so explicitly stated) is that evolu-
tionary change begins at the individual level. Indeed, this occurs in any phenotypic
expression. Initially, it had a frequency of occurrence that was not the one that exists
today, in the case that it has become the typical pattern or rule for the group.
Applying this principle to other sciences, such as physics, may be more compli-
cated. For example, light did not vary in nature over the evolutionary time of the
universe. The same could be said of gravity as a phenomenon, even if its values
change in specific sectors of the universe. In chemistry, it could be applied to com-
pound abundance in the history of the universe and the Earth. Additionally, the pres-
ence or absence of certain compounds underwent variations, for example, in organic
compounds, such as those that in the “primordial soup” emerged as the organic
precursors of life (various carbon compounds), aspects that we will see in Chaps.
6 and 8.
On the other hand, this first principle would invite us to think in any of the three
contexts (time, space, or group) about “rigid” alternatives such as 2. Every current
exception always was an exception: this may be accurate as well since it does not
mean that something that is a rarity as phenomenon or process, in some time, space
or group, becomes at some point a rule (or pattern if we speak of initial rarities). 3.
The opposite principle is that every current exception will become a rule: This pos-
tulate is similar to 1. However, that one points to the past and implies rules initially
arise from exceptions but does not predict every exception will be a rule (or became
one at some point in the past). It is a necessary condition, but not the only one.
Another principle to take into account in a potential discussion to refute or accept
is 4. Every current pattern or rule always was a pattern/rule: that is, nothing
changed since the beginning of biology as such, since the emergence of the first liv-
ing being or if the rule in question is restricted to a taxon, in the evolutionary history
of the same. It sounds strange and challenging to sustain this since the spontaneous
generation of an organism or a creationist principle comes to mind if it is accepted.
Even if the origin of a process or phenomenon was not on our planet, its actual
beginning could be traced elsewhere in the universe. This postulate could be sus-
tained if one accepts the theory of life as a phenomenon coming from space, as
exobiology might suggest, for example, brought here by a comet (we will return to
this subject in Chap. 7). In this more “static” framework, option (2) exception–
exception (i.e., a current exception always was in the past) may be more plausible.
In contrast, the rule–rule option would be little or not at all sustainable in evolution-
ary terms. The caveat would be the three fundamental laws of biology, which we
discussed in the previous sections since they refer to patterns and principles inherent
to the existence of all living beings that occurred at the time of the origin of all life
that we are analyzing today.
A prediction in this analysis could be that 5. Every current pattern or rule will
become an exception sooner or later: either in space or in a space and group com-
bination. Again, it is not easy to hold this prediction in general terms as a global
principle or law for all of biology. However, it could apply to specific evolutionary
biodiversity contexts. A particular pattern could become rare in the future without
34 1 A Big World of Rules?

necessarily leading to its disappearance. The cases of species extinctions serve as an

example, as we will see in Chap. 7. In the context of the history of science and sci-
entific postulates, it may also sound strange that all the current rules will be main-
tained the same for hundreds of years. In any case, they will be adapted and molded
to new data sources, even more so in biology.
In contrast, they may also be discarded and replaced by antagonistic ideas. In any
case, as discussed in the epistemological aspects of the rules, it is feasible that a
central “core” of the paradigm will survive. Therefore, of these postulates, the latter
is the most complicated and risky to pose.
Principle 1 is the most feasible in biological evolution and even from the view of
scientific ideas. It is the main contribution of what we will analyze in this book, an
idea linked to classical epistemological postulates.
Summing up all that has been said up to this point: is it possible to develop a
comprehensive framework, such as a “Theory of Rules and Exceptions” or a
“Theory of Rule-Exception Dynamism,” that illuminates the interplay between
these seemingly opposing concepts and how they mutually influence each other
within the context of time, space, and specific groups? This dynamic relationship,
which remains largely unexplored, invites us to reframe our understanding of nature
in general and biology in particular. Continuing our exploration, we observe that,
similar to the examples of systems theory and emergence, our search for patterns
and their contextualization in different temporal, spatial, and group contexts plays a
crucial role. These proposed theories, centered on biological evolution and encom-
passing biodiversity and various biological aspects, reside within the epistemologi-
cal realm of ideas, laws, and scientific thought. However, it is important to note that
attempting to accomplish such a task is premature. The subsequent chapters of this
book will provide a more comprehensive framework and pave the way for further
studies on this captivating subject.
Finally, a point that we have mentioned and is worth noting is whether the probabil-
ity of exceptions, i.e., the occurrence of exceptions according to the type of rule, could
be predicted. We could expect each type of rule to offer a particular “tapestry,” a more
or less flexible scenario for the occurrence of exceptions. For example, if we focus on
level I of rules, perhaps it will be more common to expect exceptions since we are
dealing with something that can hardly contemplate the totality of the multiple varia-
tions of what is stated in the rule (whether explicit or implicit for science). However,
if these rules are not simple generalizations but allude to essential aspects of life, then
exceptions should not occur. From the above, could the probability of occurrence of
exceptions be inversely proportional to the rules’ level (i.e., the degree of inclusion)?
In other words, for a level I rule with a significant degree of proven inclusion, the prob-
ability of exceptions is lower compared to medium- or low-level rules. In the latter
cases (II, III), exceptions are more likely to occur. The intuitive thought would be the
opposite, that more exceptions are expected in generalizations, which could be con-
fused or taken as a synonym for a level I rule with a high degree of inclusion.
In contrast, at finer or more specific levels, by the mere fact of being more cir-
cumscribed, fewer exceptions are expected. However, if the comprehensive rules
have arisen from an exhaustive analysis of reality, once they have been established,
References 35

it may be rare for them to present exceptions. It is a controversial point that requires
analyzing the intuitive and counterintuitive nature of both options in concrete facts.
We leave it here and will indirectly revisit this question through examples through-
out the book.

1.9 Key Concepts and Ideas in This Chapter

• Rules are general practical concepts or constructs that allow us to describe reality.
• In biology, the effects of rules seem to be more labile due to the plastic charac-
teristics of life, emergence, and contingency effects associated with living
systems.
• Comparatively, the sciences associated with biology do not seem to have the
conceptual and encompassing strength of phenomena that disciplines such as
physics and, to a lesser extent, chemistry show.
• It should be noted that there are basic precepts and robust central-level theories
for life itself, such as that all living things follow the laws of physics and chem-
istry, all living organisms consist of membrane-covered cells, and all organisms
have arisen from and are affected by evolution.
• The theory of evolution constitutes a globalizing rule of first degree for all liv-
ing things.
• In an epistemological framework, some currents of scientific thought follow in
part the logic of evolutionary theory to explain changes in scientific paradigms.
Some epistemological cycles are similar to the rise and decay of species in nature.
• There is intrinsic importance in rule-exception duality. Exceptions are often seen
as unimportant but have proved to be essential in comprehensively understand-
ing biology.

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Chapter 2
A Small World of Exceptions?

Insisting on rules would not have improved things, they would

have interrupted the process
—Paul K. Feyerabend, 1978

Contents
2.1 Introduction 42
2.2 W  hat Is an Exception? 43
2.2.1 They Are in Our Daily Life 44
2.2.2 Does the Scientific Method Ignore What Is Nothing or Even a Little
“Repeatable?” 48
2.3 Waiting for Exceptions According to Rule Levels 49
2.4 The “Exceptional” from the Point of View of Exceptions 50
2.4.1 An “Exceptional” Example? The Rapid Evolution of HIV 51
2.5 Exceptions: Single-Trait or Multitrait? 52
2.6 “Invisible” Exceptions: Outliers in a Population 54
2.7 Outliers: Those Underestimated Exceptions 56
2.7.1 An Outlier Hiding a Spider’s Secrets 59
2.8 Key Concepts and Ideas in This Chapter 61
References 61

Abstract When rules are mentioned in biology, the opposite concept of exceptions
immediately arises. In this chapter, we analyze the existing definitions of what an
exception is in general and in life sciences. We give examples that invite us to reflect
on the richness and complexity of exceptions since it is not just an absolute concept,
but there can be gradients of types of exceptions depending on the type of rule to
which they are linked. We mention what exceptions mean in everyday life and what
value they have in the scientific field. We also comment on the concept of exception,
which is extended to what is considered exceptional in terms of biological charac-

© Springer Nature Switzerland AG 2024 41

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_2
42 2 A Small World of Exceptions?

teristics. In this context, single and multiple trait exceptions and the implications of
population outliers are discussed.

2.1 Introduction

When we think of exceptions, even outside the scientific field, we think of rare
events or situations that indirectly reinforce the pattern, that is, what is typical or
normal. Something like this happens every time. Let us begin to illustrate this topic
using a curious city anecdote. In the city of Córdoba, Argentina, we observe the
sculpture carved in marble of a polar bear, which has, between its front paws, caught
a fish, possibly a salmon. This sculpture, the “bear” as it is called there, has a long
local history. It was commissioned by the Argentine painter Roberto Juan Viola and
the Spanish sculptor Alberto Barral on the occasion of the inauguration of a bridge
that crosses the Suquía River in the city at the end of the 1940s. The problem was
that the bridge was named “Antártida Argentina,” and it was planned to place an
animal representative of the Antarctic region on one of the bridge’s ends. There
were applauses when the statue was unveiled, but one of the then Mayor’s advisors
came up to him and whispered in his ear that there were no bears in Antarctica!
Well, that sculpture was removed from the place, the name of the bridge was not
changed to “Ártico Argentino” (because it would also be inaccurate), and, unfortu-
nately, they did not put a penguin sculpture instead. The bear statue began a journey
of almost six decades through various city places and squares until finally falling
into what is perhaps its final place, gardens outside the city museum of contempo-
rary art. The statue’s history has given rise to extensive notes and a recent book in
which all the anecdotes summarized here are described in detail (Lavezzo, 2013).
This curious domestic history shows what an exception in the anecdotal history
of a society is. First, bears inhabiting Antarctica would have been an exception. The
presence of such a sculpture in a city of the Southern hemisphere, wandering for
decades, was a total rarity, a strangeness for those who saw it without knowing the
original story. How many rarities will there be in other cities? Minimal stories of
local events marked in the popular unconscious, enrich the collection of domestic
histories, which are no less striking for that. The truth is that the rare, the excep-
tional, always attracts or repels us, but it is not indifferent to us. As we will see later,
this response is also observed in the scientific field, where the oddities, whatever
their nature, attract our attention powerfully, or, in contrast, we directly ignore them
and do not even notice them. It is like a “black and white” our position toward
exceptions, a fact that is reflected in the value or not that we give to them in science,
and in the case of biology, especially in crucial fields such as developmental biol-
ogy, ecology, and the evolution of organisms and systems.
2.2 What Is an Exception? 43

2.2 What Is an Exception?

The definition has many options, but they coincide with what is central. We could
say that an exception is “something excluded from, or not in accordance with the
general rule, principle, or class” (Collins English Dictionary, 2003) (Box 2.1). If
we pay attention to this definition, it is self-evident that it has no independent or
absolute entity since it is intimately linked to the definition of its opposite, i.e., the
rule. Therefore, a definition of rule and a definition of exception become antonyms
and, at the same time, “mutually necessary” opposites to give an entity and com-
plete the understanding of what each of them alludes to. Interestingly, the definition
of an exception, as in the case of rules, exists “before” any analysis of its existence
in a given discipline. These basic definitions apply to the sciences, the arts, sports,
and other areas of knowledge and human activities.

License: own creation.

44 2 A Small World of Exceptions?

2.2.1 They Are in Our Daily Life

The truth is that “rule” and “exception” are closely related concepts that scientists
have in mind during their routine research. This “keeping in mind” can be formally
embodied in expressions (laws, statements of patterns, and predictions) or more
implicitly or intuitively. During our research, we use samples either in descriptive or
experimental work, where we measure parameters of selected variables (e.g., traits
such as size, length, width, height, and weight). Moreover, it is in these factors that
we then see how they do or do not conform to a “norm” and whether we have outli-
ers or “exceptional” cases. The problem is that if the latter is not conspicuous or
“striking” to the observer, they may go unnoticed. There is a sensory bias that often
allows us to appreciate what the rule is, perhaps because it is the majority and it may
be the easiest thing to perceive. At the same time, if the oddities or exceptional cases
are not aberrant, they are barely detected and often ignored. We will return to spe-
cific cases of extreme values in Chap. 5 when we analyze the nature and types of
exceptions.
Interestingly, from areas such as positive psychology (e.g., coaching strategies
and leadership), the value of feeling “exceptional,” for example, to be out of the
“norm” of the masses, is valuable and promoted. In addition to belonging to being
part of a social group, here, the value of individuality is promoted, whether in per-
sonal life, at work, or in social life.
Therefore, we are not indifferent to exceptions if they are marked in the reference
pattern and indicate a highly valued quality in society. This situation has been used
by advertising, marketing, and fields nourished by striking oddities but synonymous
with positive, healthy individuality above the common. This attracts us both to feel
(and be?) different and to make a difference over the rest. In the history of humanity,
not only in science but also in politics, art, and sport, the exceptional has been a
synonym for “success”, geniality, superlative, and promoter of resounding changes.
Sports idols, i.e., the “best in the world at...” are exceptions to the rule. In other
words, the rest of us are not the best in that measured parameter. Later, we will dis-
cuss the question of to what extent something or someone is exceptional as a
“whole” or only because of a single “one variable.” In Fig. 2.1, we see just a few
media examples of athletes who are or were considered the best of the best, undis-
puted, i.e., “exceptional.” For example, the fastest man in the world, the tennis
player who has won everything, the Olympic super medalist, or the best in basket-
ball are always highlighted. Each of these outstanding individuals represents an
extreme of the best. They can be considered a stereotype of the ideal in that sport.
If we pay attention, everything goes hand in hand with the concept of “almost”
perfection. Hence, idolatry because we see these “idols” as invincible. In other
words, perfection is the opposite of mistakes and failures. For this reason, when
these idols “fail” at what they excel at, society stops projecting its dreams onto
them, often projects its failures, and may not forgive them for their mistakes. Society
condemns how someone “exceptionally unique” can cease to be so from one
moment to the next. The case of the great footballer Lionel Messi, for example,
2.2 What Is an Exception? 45

a b

c d

Fig. 2.1 Exceptional athletes. Some of the best athletes in their disciplines. (a) Soccer player, Leonel
Messi. (Credits: Tasnim News Agency). (b) Olympic sprinter, Usain Bolt (Credits: Erik van Leeuwen)
(c) Olympic swimmer, Michael Phelps (in the middle) (Credits: White House photo by Eric Drape).
(d) Olympic tennis player, Serena Williams. (Credits: Edwin Martinez from The Bronx).
Licenses via Wikimedia Commons and GNU free documentation. (a) Leonel Messi. License: CC
BY 4.0. https://creativecommons.org/licenses/by/4.0, via Wikimedia Commons. https://es.wikipe-
dia.org/wiki/Lionel_Messi#/media/Archivo:Argentina_vs_mexico_messi_vs_alvarado.jpg. (b)
Usain Bolt. License: GNU free documentation license. https://es.wikipedia.org/wiki/
Archivo:Usain_Bolt_100_m_heats_Moscow_2013.jpg. (c) Michael Phelps. License: Public
Domain. https://es.m.wikipedia.org/wiki/Archivo:Michael_Phelps_Ryan_Lochte_Laszlo_Cseh_
medals_2008_Olympics.jpg. (d) Serena Williams. License: CC BY 2.0 https://creativecommons.
org/licenses/by/2.0, via Wikimedia Commons. https://commons.wikimedia.org/wiki/File:Serena_
Williams_US_Open_2013.jpg

reflects this duality. In his golden era at FC Barcelona, Messi won many national
and international trophies. In the Argentinian national team, however, he was unable
to achieve the same level of performance, which is why he was fiercely attacked by
fans and many critics in his country. It must have been a difficult time for Messi.
The media forgot that this great player is not only an “idol,” but also a living being
and not perfect.
46 2 A Small World of Exceptions?

Furthermore, the working environment at his club was different from that of the
national team. So in this case, a behavior or conduct (i.e., in this case, the outstand-
ing ability to play football) that was almost perfect in one context (at FC Barcelona)
was not comparable in another (in the Argentinian national team). However, the
criticism and attacks changed dramatically after he directed the Argentinian national
team, which won three trophies, beating their former champions in the process:
Brazil at the 2021 Copa América, Italy, at the 2022 Copa de Campeones Conmebol-­
UEFA Finalissima, and France at the 2023 FIFA World Cup. The environment at
these tournaments was also like that of FC Barcelona and Messi could feel at home
there. With his performance, he has once again shown that he is far more than just a
normal footballer. We could list other cases of athletes whose peak performance
depends heavily on the context; it is therefore not their sole responsibility to be or
not to be “exceptional” in all situations.
In the case of women, it is even more remarkable. When talking about the female
athlete and all the challenges she faces because she is a woman, all the social con-
structs about gender roles are included, and how these have generated stereotypes
and expectations that “should” be followed. Although in recent years, there has
been significant progress in gender parity in sports, the media continues to offer a
stereotyped image of women, which also has an impact on public opinion. Even so,
physical beauty is an essential characteristic of women in sports and not men
(Mujika-Alberdi et al., 2021). Moreover, the same occurs in the case of mother-
hood (Ferrer et al., 2022). Therefore, we are talking about situations that could be
considered double exceptions. For example, an outstanding woman in sports will
not be an exception only because of her different sporting abilities but also in terms
of a break in the “mandates” of her assigned role as a woman within society.
However, we can still count on many exceptional women in this field, such as
Martina Navrátilová, Serena Williams, Simone Biles, Annika Sörenstam, and Marta
Vieira da Silva.
In the field of the arts, musicians such as Mozart, Beethoven, Wagner, Chopin,
Clara Schumann, Fanny Mendelssohn, and Barbara Strozzi or painters such as Van
Gogh, Dalí, Picasso, and Frida Kahlo are examples of the impact generated by being
in front of “exceptionally good” beings in “that” which they do in an incredible way.
The word “genius” implies, by definition, to be someone different from the rule, to
be an exception. The Oxford Languages dictionary defines genius as “exceptional
intellectual or creative power or other natural ability” or “an exceptionally intel-
ligent person or one with exceptional skill in a particular area of activity.” As we
can see in both definitions, words such as exceptional and exceptionally undoubt-
edly refer to qualities outside the performance of individuals in the society from
which this genius comes.
On the other hand, taking the Olympic Games as an example, the news highlights
the fastest runner, such as the Great Usain Bolt, or the fastest swimmer, such as
Michael Phelps, but not the slowest, the least skilled. That is, we do not know or are
not made aware of the “other” extreme. In this case, the one who arrives last at the
finish line can be considered a circumstantial extreme for that discipline and that
edition of the Olympic Games but does not represent the true extreme. The bias is
2.2 What Is an Exception? 47

due to the implicit social condemnation that being last is equivalent to total failure,
even if you have been to the Olympic Games. It may not be disclosed so as not to
stigmatize that person. Are there people faster than Bolt running or Phelps swim-
ming? We do not know, and the Olympic Games bring together a group that has
passed numerous filters and has wanted to dedicate themselves professionally to
these activities. In short, sports, arts, and sciences highlight the best, but we need to
know or be interested in the “worst,” the other side of the spectrum, according to the
respective canons in each discipline. Someone might ask: why know and divulge
who was the slowest? As scientists, we want to know or have it on par with the best.
Considering also the “worst” would allow us to analyze, for example, the causes of
the differences between the “excellent vs. poor” extremes at the level of genetic and
environmental variables translated into physical or psychological qualities.
Therefore, there is an impressive bias in humans to “show” the best and consciously
or unconsciously hide the “worst” individuals; is not it interesting to highlight the
weaknesses of our species?
Exceptions among humans can also have a connotation opposite to the extreme
admiration or idolatry we have discussed. That is, the exception is linked to what
produces “aversion” or abhorrence. There is a gradient of traits among humans, be
they behavioral or physical, and canons established by societies of what is beautiful
and what is ugly. Imagine a pendulum moving from the positive (admiration) to the
other extreme of the negative (aversion). Then, we can see how fabled characters
such as Frankenstein’s monster, demons, malformations, and historical characters
who have committed crimes can all fall into being socially considered negative
exceptions, “rejectable” or certainly not “admirable” abnormalities.
Moreover, someone who is a “genius” in one variable or area of life may be
unacceptable in others. In the past, oddities have been considered (consciously or
unconsciously) “negative” in many societies. This bias has led, in many cases, to
xenophobia, racism, discrimination, and crimes. In short, this has been experienced
in many stages of human history, from Sparta (where according to Plutarch, sick or
disabled babies were sacrificed—Penrose, 2015; but see Hurst, 2008) to Nazism,
which combined the rejection of everything that did not conform to the concept of
rule, which, according to the canons, was the Aryan stereotype.
We know that, fortunately, erroneous and fanatical look has been changing and
our contemporary look as a society is far from that of yesteryear. Everything that
represents not only minorities but even more true rarities is currently contemplated
differently. In the novel “The Elephant Man” by Bernard Pomerance or the charac-
ter Quasimodo (pun for “almost human”) in “Notre Dame de Paris” by Victor Hugo,
situations associated with the duality of the concept of physical beauty on the one
hand and spiritual beauty on the other are reflected. These stereotypes draw atten-
tion to how society tends to focus mainly on the former. The “Elephant Man” was
the nickname given to John Merrick. This English citizen became famous due to his
terrible malformations (Proteus syndrome), as his moral, ethical, and intellectual
values far surpassed the qualities of many of his contemporaries. Unfortunately,
Merrick lived condemned to general rejection and was exhibited at numerous fairs
as a “freak” until even after his death. Merrick wrote of himself and completed a
48 2 A Small World of Exceptions?

poem by Watts: “Is true that my form is something odd/But blaming me is blaming
God; Could I create myself anew/would not fail pleasing you. If I could reach from
pole to pole/Or grasp the ocean with a span, I would be measured by the soul/The
mind’s the standard of the man.” (Adapted from Isaac Watts’s “False Greatness.”)
Exceptions shock us, and many atrocities have been committed against what we
consider strange and different, often supported by pseudoscientific (or incomplete)
arguments. This view is not only toward other human beings but also animals (e.g.,
toward animals taken as monsters, as associated with witchcraft, such as black cats,
owls, spiders, and bats). In a neutral framework (i.e., neither negative nor positive),
the exceptions often promote their gathering in written compendiums or public rec-
ognitions that include awards for what is extreme in some quality. One example is
the famous Guinness Book, which includes thousands of disciplines, characteris-
tics, facets, and the most unusual records. These refer to fields in which the protago-
nists, whether humans, animals, or plants, could fall into categories of teratologies
or exceptions attractive to our anthropic bias. Everything is finally about surpassing
sporting records, breaking records, expressing this or that ability or quality, and
gathering everything that is “outstandingly exceptional.”

2.2.2 Does the Scientific Method Ignore What Is Nothing or

Even a Little “Repeatable?”

This fundamental question goes hand in hand with another, more specific question
for this book: are exceptions significant for biology? We mean “important” both for
biology itself and for the scientists who study it in its different disciplines. The
answer is a resounding Yes! Exceptions are often the starting point for many changes
in forms, behaviors in organisms, and systems in evolution. In other words, they are
the initial kick-off or “raw material” for traits that will later be consolidated.
As we will see later, typically, we will not find only one type of exception but
several. We can find levels or, instead, a gradient in the same way as when we
referred to rules earlier. We can identify exceptional cases from interspecific or
higher “interclade” degrees. Another more circumscribed level will be the intraspe-
cific level. For example, individuals deviate from the characteristic pattern of their
species. Even more, restricted in terms of level, there may be population patterns,
and within them are the exceptions. It is like viewing the world using a telescope, a
magnifying glass, or a microscope regarding the organismic levels of biological
systems. Therefore, some exceptions may attract our attention more than others
(conditioned by a particular sensory bias), while many exceptions may not even
have been discovered. Biology, by its very nature of organismic diversity, from bac-
teria to plants and animals of all evolutionary levels, added to eco-geographical and
temporal variability, offers us a wide range of these exceptions of different gradients
or levels. If we add, as we will highlight later, the influence of a man on climate
change, we will have the potential diversity for more variants to occur within a
given pattern or norm, which can become very high.
2.3 Waiting for Exceptions According to Rule Levels 49

The essence of exceptions is to be unusual, either in the frequency of occurrence

with what is expected (something more quantitative within a continuum) or radi-
cally different forms of the pattern (something more qualitatively different). This
characteristic implies that they should be taken into account in more detail by the
scientific method. Based on statistics and probabilities of occurrence to define pat-
terns, the scientific method does not necessarily contemplate highlighting what is
rare as a fundamental piece of the descriptions, at least in daily practice judging by
what is reflected in most scientific publications. The scientific method classically
relies on experimentation and the “repeatability” of facts, phenomena, and data
taken in control vs. experimental/s groups after this or that treatment until a sample
size (n) is reached. However, it is obviously in the very nature of the exception not
to be repeatable or to be repeatable in a very low or even not precisely the same way
in case it depends on several variables. This characteristic finally results in the fact
that exceptions “do not fit” in the logical foundations of the scientific method, at
least the conventional one (i.e., positivism vs. a more holistic view which, on the
contrary, does consider them more). We will address part of this problem when we
discuss exceptions from the statistical analysis of biological data.
In a way, the scientist’s gaze tends to recognize patterns, requiring a much more
detailed look to detect exceptions. On many occasions, exceptions can be recog-
nized, although their subsequent analysis is generally truncated, exposing their exis-
tence as marginal and without much biological relevance. Without devaluing the
identification, study, and comparison of rules, the challenge is to become more com-
mitted as researchers to avoid overlooking or hiding (because they are not consid-
ered essential) biological exceptions. In this way, it would be possible to have
integrative approaches for a better understanding of biological phenomena.

2.3 Waiting for Exceptions According to Rule Levels

In the previous chapter, we analyzed a certain degree of hierarchy regarding the

level of “influence” between sciences such as mathematics, physics, chemistry, and
biology. It is interesting to consider the “probability” of exceptions in each of these
scientific areas (Fig. 1.2a). In principle, this probability will be inversely related to
the level of influence of the science one refers to. Thus, they would be null within
Physics, something more common in Chemistry, and even more so in Biology.
These differences then translate into why we expect a higher occurrence of excep-
tions in specific sciences, particularly in the life sciences, and not so in others. This
tendency is reflected in greater or lesser confidence in the enunciation of rules in
these sciences.
Thus, in mathematics and physics, there would be no significant objections to the
search for rules that can govern all physical phenomena. Chemistry also, although
it may have some minor cases where specific chemical rules do not apply. Finally,
biology challenges with the power or not to propose comprehensive laws (the most
“universal”) (e.g., those of Mendel or Hardy–Weinberg in genetics) due to the
50 2 A Small World of Exceptions?

existence of exceptions, which by default are expected to occur in most cases. The
exception to this would be the case of the level I rules and the fundamental laws of
biology discussed in the previous chapter, which are worth reiterating. Within the
framework of these, there would be no exceptions. However, as we have already
shown, it has yet to be possible to postulate rules and the existence of recognizable
patterns for many situations in various biological disciplines. In any case, the key is
to contemplate that exceptions will occur, as we have already mentioned, according
to the level of influence (I, II, and others) of the rule posited.
This greater feasibility of proposing rules, more generalizable and comprehen-
sive laws in physics and much less in biology, could also be seen, on another level,
for example, among the disciplines of biology in terms of the probability that excep-
tions can occur. Thus, those disciplines framed in molecular and cellular biology,
having a more direct connection with physics–chemistry and at the same time being
the bases of the disciplines of organismic biology, could be the ones that presentin
comparison with the lattera lower number of exceptions. A level I rule of biology
that we have already discussed that all organisms are defined by cells with mem-
branes comes from molecular and cell biology. However, those rules that are more
labile in terms of rule rigidity, such as those from the field of ecology and behavior,
would be more subject to possible exceptions. Indeed, in these biological disci-
plines, interindividual and even intraindividual variabilities in time and space are a
central aspect of their essence.

2.4 The “Exceptional” from the Point of View of Exceptions

When we refer to exceptions, rarities, and abnormalities, we limit ourselves to facts,

groups, processes, and events that refer to something that deviates from the rule in
a strict, visible sense. However, we could also include cases and situations related to
this concept, although not strictly speaking. Thus, adverbs of frequency are used in
examples such as “this organism always flies fast,” “this process seldom, occasion-
ally fast/often, frequently slow,” or “this animal is rarely big among its group.”
Additionally, when mentioning something such as “this group is exceptional” or
“that biological system is exceptional because of such a quality,” we refer to the use
of the term exceptional. However, we could replace it with related terms, such as
rarely or abnormally, to describe the frequency of a particular characteristic or
adjective (big or small, slow or fast, high or low).
Therefore, if we were to pay attention within the book to all these variants derived
from the concept of exception, we could come across an endless universe of exam-
ples. This point does not invalidate the more limited analysis of striking, direct, or
drastic cases of exceptions. In any case, this complexity makes the problem richer
and shows an almost continuous gradient of which we may not yet be aware regard-
ing the boundaries between rules and exceptions. Our flexibility in analyzing bio-
logical phenomena is necessary. Otherwise, reductionism will not allow a more
holistic view to emerge.
2.4 The “Exceptional” from the Point of View of Exceptions 51

2.4.1 An “Exceptional” Example? The Rapid

Evolution of HIV

Concerning what has been said about terminology linked to exceptions, we can take
a specific case close to humans at the evolutionary level. When illustrating cases of
rapid evolution, perhaps the example of what happens with HIV is presented as an
exceptional case. Reference is made to the fact that the evolution of this virus is
“exceptionally” rapid (Hutchinson, 2001; Ridley, 2004). Indeed, the evolution of
HIV takes place within the body of an individual and is, comparatively, exception-
ally rapid compared to most other viruses.
This microcosm of mutations, natural selection, and finally adaptation (in this
case, drug resistance) simulate what occurs at the macroevolutionary level in other
organisms. Even a relatively small change at the mutational level quickly translates
into an adaptive process of the virus to the 3TC drug. Elements such as having a
high default mutation rate, a large population size in the host, and a high recombina-
tion rate strongly favor such exceptionally rapid evolution (Ridley, 2004). However,
much remains to be clarified. For example, more needs to be known about the
molecular mechanisms used in viral replication and the strategies adopted by the
virus to evade host immune surveillance (Becerra et al., 2016). For example, a
mutant “Tat” protein has recently been found to inhibit the infection of human cells
by strains of various HIV-1 subtypes (Rustanti et al., 2017).
This rapid change due to a high level of mutations is standard in RNA viruses
compared to DNA viruses (Holland et al., 1982; Steinhauer & Holland, 1987).
Indeed, other RNA viruses, such as Ebola or influenza viruses, are also challenging
to treat due to their high mutational rate (Hoenen et al., 2015; Harding & Heaton,
2018). These are rarities from the perspective of evolutionary speed that invite us to
analyze why such a high mutational rate and associated aspects compare them with
that of other viruses or pathogens. In this sense, these RNA viruses share the fact
that they do not have a highly developed proofreading process (Elena & Sanjuán,
2005). This characteristic results in these “errors” due to mutations not being cor-
rected, thus increasing the genetic diversity of the virus variants and their possible
recombinations, which is essential for rapid evolution. Indeed, genetic variants
coexist in the virus population, “cooperating” to cause a more significant effect,
virulence, on the host than if only one existed (Fraser et al., 2014). Selection will
occur in that population of coexisting variants as “a whole” rather than on an indi-
vidual variant. These variants end up giving identity to a given population in terms
of composition, functioning, and virulence. The term “quasispecies” has been
applied to many of them due to their unique profile (Domingo et al., 1985; Najera
et al., 1995; Eigen & Biebricher, 2018).
Therefore, HIV and many other RNA viruses are biological exceptions to other
types of viruses because of their rapidity in evolving within an individual, resulting
in increased drug resistance. In this sense, each one is an exception from a statistical
approach. This situation does not imply that we are speaking here of an exception
regarding the frequency of virus abundance but of a specific quality: speed of
52 2 A Small World of Exceptions?

evolution. This particular case serves to warn us, once again, that just as when ana-
lyzing the evolution of traits by natural or sexual selection, it is always best when
analyzing exceptions to specify which trait or group of traits we are referring to. In
the example of HIV, we are dealing with a trait with a particular expression (rapid
evolution) in a context (evolutionary time of only a few days) and space (within the
host). We will return to HIV and examples of disease evolution later in the book
when we analyze the dynamism between rules and exceptions.

2.5 Exceptions: Single-Trait or Multitrait?

When an individual is an exception in a group, is it as a “whole” or regarding a

particular variable? Perhaps we inadvertently tend to speak of an exception based
on a more relevant variable rather than a set of variables, either because of our sen-
sory or conceptual bias or because the latter is critical from a biological point of
view. However, it is worth asking whether we limit ourselves to a typified variable
or variables when we have an individual who falls into the exception category.
Alternatively, we can indirectly generalize it and involve more variables until we
reach the whole individual without analyzing the latter. The implications of consid-
ering this are important. For example, an individual could be an exception within
the population in terms of the variable “body size” (e.g., being tiny or giant), but this
does not imply that other individual variables are associated or correlated, such as
competitive ability or genetic quality. It may or may not, but we should check this
and not generalize from this exception for one variable to the whole possible set of
variables. In other words, we should not label the individual based on a single char-
acteristic. This option limits expressing what a pattern, a rule, and what is not is an
exception.
When, in Chap. 5, we look at the potential value of specific “variants” in a given
trait, we will inevitably limit ourselves to a particular trait. Therefore, it is essential
that, as far as possible, we take into account this limitation in the approach. We have
already mentioned that when talking about selection processes in evolution, it is
best to start by analyzing a particular trait before moving on to a “multitrait” com-
plex. In this sense, it is important to avoid categorizing the decision to consider an
individual solely based on the rarity or exceptionality of a particular characteristic
as either “positive” or “negative” at a reductionist functional level. The same could
be said if what is being analyzed is at a supraindividual level. Examples of this
could be a population, a species, a larger taxonomic group, or even a more extensive
process (e.g., not a trait in the strict sense but a process or mechanism). The concept
of rarity is linked to the frequency of occurrence and abundance at the population or
whole-species level. There are interesting studies on the biology of rarities (almost
synonymizing this term with “infrequency”).
On this subject, it is worth mentioning the book “The Biology of Rarity,” edited
by Kunin & Gaston (1997), which was a synthesis of what had been published up to
that time on rare species, their dynamics in ecosystems, and reproduction systems.
2.5 Exceptions: Single-Trait or Multitrait? 53

It is mainly focused on the presence of rarities as the “opposite” of the abundance

or density of a species. This point is also expressed as species-range size distribu-
tion in terms of geographical level (Gaston, 2014). These authors point out that
these rare species, whether locally rare or geographically restricted, not only differ
from the common ones by this “attribute” linked to their frequency in the number of
individuals but also present other characteristics that differentiate them. These fea-
tures exist, for example, at the reproductive level, such as low genetic incompatibil-
ity when crossing, a tendency to reproduce by chance, low reproductive effort, and
low dispersal ability. They add that several mechanisms may be responsible for such
differences, but in practice, they may be challenging to differentiate. However, the
cataloging of rare-common differences that recur is of great importance, as it may
allow us to partially compensate for the bias of the published literature toward
reports with the most common taxa (Kunin & Gaston, 1993). The implications of
considering rare species in conservation contexts are significant (Rey Benayas et al.,
1999). We highlight the last sentence on the bias, perhaps logical, of having focused
on the most common taxa. This bias has meant losing sight of several opportunities
to learn about exceptions in terms of strategies, mechanisms, reproductive patterns,
life histories, and morpho-physiological patterns, which could be critical to a much
better understanding of “the rule,” the dominant pattern, in these common species.
Are we, in science, to a greater or lesser degree, limited in experimental designs
due to focusing our attention on a handful of variables to label what is and is not an
exception? From the social point of view, we have already mentioned the high cost
for human individuals of “falling” into the category of exception according to
beauty standards or being labeled as “abnormal” in their cognitive or social capa-
bilities. The opposite is also true, as we have already mentioned: cases in which
individuals who are exceptionally good at a particular skill in the art, science, or
sport are expected to be exceptionally “positive” in other cognitive, social, and
human values and skills. Thus, we tend to be biased toward the exceptionally “nega-
tive” or “positive,” attaching the rest of the qualities of that individual in the same
line. This bias brings rejection, prejudice, and discrimination, in the first case, or
excessive admiration, idolatry, and mythologizing in the second. Biology does not
escape this bias, at least in terms of omitting to report exceptions, underestimating
or overestimating them, as the case may be.
As we will see below, we can find a species that is taken as an exception either in
its closest clade (e.g., genus or family) or more distant clade (order, class, phylum).
This criterion may have been based on a particular trait or several traits. In many
publications, this is reflected in the titles, where “a trait” is emphasized to mention
that a species or individual is an exception. However, this unintentional reduction-
ism may occur due to our bias toward the most striking aspects of an organism,
focusing on exceptional traits such as extreme age, size, or weight, as we will
explore later.
The point is that there may well be a very close association between more than
one trait (e.g., between size and weight), and thus, the exception is no longer, strictly
speaking at least, “uni-trait.” Even so, what may still stand out as such is one trait
(i.e., variable) over the associated other(s), even if the latter may also be labeled as
54 2 A Small World of Exceptions?

an exception or at least fall in the minority of the variable distribution. Then, it is

evident that in many cases, there appear before our eyes organisms that can undoubt-
edly be considered valid exceptions at the level of not one but several traits. These
traits may not even be directly associated with each other. In general, the excep-
tional characteristics are presented in atomized form or as watertight behaviors at
the level of “uni-traits.”

2.6 “Invisible” Exceptions: Outliers in a Population

Thus far, we have mentioned two territories of exceptions, on the one hand, those
linked to abnormalities of form or teratology, and on the other hand, exceptions of
taxonomic nature in biological diversity. In the first case, they involve extreme rari-
ties within a species, and in the second, between species (or the clade to which we
refer). Both types will be discussed in more detail in the following chapters. Now,
unlike these two options, some rarities could be more striking. We would say they
are almost “invisible” to an observer, at least in a first approximation. We refer to
extreme cases in the phenotypic expression of a given characteristic or trait. These
cases fall in the extreme quantitative values, either maximum or minimum, well
outside the “average” value within the population. Indeed, as shown in Fig. 2.2a,
under standard conditions, the “norm” of the population (its normal distribution)
shows us that such extreme values exist. However, as scientists, we generally pay
little attention to these cases far from the mean. Thus, we express with means and

a b

Fig. 2.2 Graphical representation of the distribution of individuals of a population with a certain
trait “X”. (a) This example shows how mean values relate to what is known as the pattern or rule
and extreme negative or positive values to what is called the “exception.” Certain selective pres-
sures can generate changes in the distribution. (b) Example applied where the trait of interest is
male coloration, and the selective pressures opposed are sexual and natural selection
2.6 “Invisible” Exceptions: Outliers in a Population 55

their standard deviations what the “majority” of the individuals in the sample do,
which is understandable if we want to characterize a given sample statistically.
Statistics are designed to show this descriptively and comparatively since we can
compare two or more samples according to these parameters. This is based on how
concentrated or dispersed the majority is around a representative value.
This approach is necessary to know the “pattern” of what we are analyzing,
studying, and observing at the intra- or intergroup level. It is not common, of course,
that in a scientific article, the researcher stops in the results to show or analyze
extreme values. For example, suppose the average height of individuals in a popula-
tion is analyzed. In that case, the average value will be apparent in general terms or
expressed according to the association with other variables, such as age, weight, and
origin. However, no one usually stops saying anything about the tallest or shortest
individual in height. According to this or that factor, this sample exhibits signifi-
cantly higher or lower values in height. Nevertheless, this refers to the mean, not the
individual point value.
Figure 2.2b introduces an additional component to consider: selection pressures.
In a classical Gaussian bell, which hypothetically exhibits the typical normality in
the distribution of a variable (e.g., trait “x”), a static scenario is reflected, a “snap-
shot” product of stabilizing selection on that variable. Therefore, we observe the
outcome of the interplay between various selective forces that influence the expres-
sion of a trait to varying degrees. These forces can include abiotic factors such as
temperature, latitude, and altitude, as well as biotic factors such as predation and
feeding. The equilibrium resulting from this interplay is not static but rather fluctuat-
ing and modal. Life is characterized by the existence of these fluctuations, even
though our analysis may often portray the “whole” as a snapshot in the punctual
instant of our analysis, summarized by average values of a given variable. As we will
see in the next chapter, those extremes can be the basis for unbalanced selective pres-
sure changes. This situation can go from one stable state to a different one in a “direc-
tional” way (i.e., toward one extreme of the distribution) or to two different events in
a “disruptive” way (i.e., toward both extremes of the original distribution). Therefore,
it is in these extreme values that new possibilities for change, both at the ontogenetic
and evolutionary levels, can potentially emerge as significant turning points.
However, even without relying on the potential value of evolutionary change to
explain the exceptions, it is important to recognize that the outliers within a popula-
tion provide valuable information about the prevailing “pattern” that is observed in
the majority. We often fail to acknowledge that everything we analyze about the
world around us is from an explicitly or implicitly rationalized comparative per-
spective. In other words, our assessments are far from absolute. When, for example,
we describe an individual as being much taller or shorter than another, we are mak-
ing a comparison. If we say this red color is much stronger than another but fainter
than a third one, we are also engaging in comparison. Therefore, the comparison
implicitly introduces the concept of extreme values.
On the other hand, going back to something previously said, if we have a mean
value, it is interesting to ask what happened to those individuals who exhibit the
expression of the trait in its extreme ranges (e.g., in statistics, those who fall in the
56 2 A Small World of Exceptions?

maximum and minimum interquartile range). How many are there? What are their
particularities? This point connects to the variance in the sample, i.e., how concen-
trated the sample is to the average value. By placing more emphasis on analyzing
and explicitly describing extreme values, we can indirectly gain a deeper under-
standing of why other values that align closely with the mean exist. Neglecting the
analysis of extreme values often leads to an incomplete explanation of the overall
distribution and characteristics of the data. To that end, we cannot deal with abso-
lutes at the variable level, and we will have to consider at least two or more vari-
ables. Thus, taking the example of height, we can add age, origin, or weight and
thus, for example, connect that those who have the highest extreme values in terms
of height are the ones who weigh more, and perhaps this is because they have eaten
better. In contrast, those who measure less are those who may suffer from malnutri-
tion and thus are the ones with the lowest weight. On the other hand, the average is
those who weigh an average, corresponding to a stable, moderate diet—moreover,
the examples in Fig. 2.2a, b are limited to a primary type of statistical data distribu-
tion, the normal distribution. However, we could have distributions that may be
skewed in one direction, for example, toward the maximum or minimum.
Therefore, in our analysis, it would be advisable to keep in mind that by consid-
ering the extreme values, we reinforce the understanding of the statistical mean and,
in addition, the influence of factors that could affect the trait analyzed in the indi-
viduals of the sample. Take, for instance, the case of the former athlete Usain Bolt.
Scientists and doctors have extensively studied his exceptional speed, aiming to
understand the factors that contribute to his extraordinary performance. In essence,
they seek to uncover the underlying causes that allow them to achieve the maximum
speed of human running speed. A combination of anthropometric characteristics,
motor coordination, power generation capabilities, and effective running techniques
would partly explain his performance. In addition, this indirectly sheds light on the
fact that this could explain the lower speed of other competitors or people in general
(e.g., poor development of motor coordination and power generation), added to
anthropometric differences inherent to the athlete (Čoh et al., 2018). Thus, we can
conclude that any extreme value in the distribution of a trait is “resignified” when
contrasted. Otherwise, the extreme value remains an “ornament” and goes unno-
ticed or is considered only a mere curiosity.

2.7 Outliers: Those Underestimated Exceptions

Gladwell’s book “Outliers: The Story of Success” (2008), which attempts to under-
stand the secret of the success of great minds and “exceptional” athletes, was at the
top of the New York Times bestseller list for 11 consecutive weeks. This work
shows us that outliers and attempts to understand them fascinate the general public.
However, the presence of “outliers” in scientific practice is far from being analo-
gous to this example, as they tend to concern scientists. Outliers are defined as “an
outlying observation, or outlier is one characteristic that appears to deviate
2.7 Outliers: Those Underestimated Exceptions 57

markedly from other members of the sample in which it occurs” (Grubbs, 1969).
Alternatively, an outlier is “an observation that lies outside the overall pattern of a
distribution” (Moore & McCabe, 1999). Another typical formal statistical definition
of an outlier is “a point that falls more than 1.5 times beyond the interquartile range,
either above the third or below the first quartiles” (Renze, 2011). Whether consid-
ered for statistical analyses, outliers tend to go unnoticed, except as “nuisance”
points to the researcher (Fig. 2.3a–c), in the vast cloud of data displayed on a plot
such as a scatterplot or a histogram. In many cases, these values are labeled “suspi-
cious,” “ugly,” and “nasty,” or that can “ruin” or “destroy” our inferences
(McClelland, 2000). Therefore, we see how an exceptional value can be considered
from a biased negative valuation in our scientific work.
At the single-trait level, an outlier is a point that deviates from the “majority.”
Although we can quickly visualize several ways of detection in a histogram, the
values are far from the frequent intervals and have low representativeness (Aguinis
et al., 2013) (Fig. 2.3a). In a box plot, they can be seen as points more or less distant
from the interquartile range boundary (Fig. 2.3c). Outliers can also appear when
relating two or more variables or data sets (multitrait approach) (Fig. 2.3b). Points
away from the fit line in scatter plots can be considered outliers. We can have an

a b

Fig. 2.3 Outliers in different statistical graphs. (a) Histogram showing the frequency of occur-
rence of trait “X” in the population, with extremes in positive values that can be considered statisti-
cal “exceptions” or “outliers.” (b) Scatter plot showing relationships between variables “X” and
“Y” with extreme values influencing the relationship patterns found. (c) Boxplot and its compo-
nents, showing cases outside what is considered the pattern or norm (interquartile range)
58 2 A Small World of Exceptions?

outlier arising from the connection, or linkage, of two extreme values of variables
but not necessarily in the same direction. For example, it may arise from the asso-
ciation between the minimum value of one variable and another variable’s maxi-
mum value. Additionally, an outlier may occur between a medium value of one
variable and a high value of another. In other words, the occurrence and character-
istics of outliers and their linkage to the data pool of the respective variables that
give rise to them cannot be predicted at all. However, they appear much more often
than assumed or reported.
Outliers are usually more influential (adding more weight than others in the esti-
mation) than data close to the mean. For example, if from a data set, we remove
these values, our inferences or results may vary greatly; not so if we remove a point
from the region of highest density. How much our results vary by removing these
outliers gives us an idea of the “robustness” of our data set. Hypothesis testing is
highly sensitive to the noncompliance of many model assumptions and the presence
of these outliers. If data do not comply with the assumptions, the ability to detect
true effects decreases (affects the p value, effect size, and estimated confidence
intervals).
The presence of an outlier may also imply a type of problem. For example, a case
that does not fit the model under study or perhaps a measurement error. In the case
of the second option, outliers are good “alerts” of possible errors, so we can detect
them and correct our data collection or discard them because of the impossibility of
repetition. However, when faced with “real” outliers (not measurement errors),
researchers can proceed in different ways or make different decisions. In many
cases, the outlier (or several if more than one) is removed with some statistical tech-
niques such as “least squares fitting to data” (Renze, 2011), or imputation tech-
niques are applied to replace the outlier with one corresponding to the mean (Dang
& Serfling, 2011). However, removing outliers or replacing them is not recom-
mended in scientific practice. This reflects our inability to address the inherent vari-
ability of biological systems or our need to “fit” the data to our hypotheses. These
manipulations (sometimes gross) may alter the inferences from the data since there
is a bias, the sample size may be decreased, and the distribution or variances may be
affected. Cortina (2002) warns, “caution also must be used because, in most cases,
deletion [of outliers] helps us to support our hypotheses (...) choosing a course of
action post hoc that is certain to increase our chances of finding what we want to
find is a dangerous practice.” If this practice is carried out, it is always necessary to
make it clear to the reader that outliers have been removed.
A more Solomonic approach is to perform statistical analyses with and without
the outliers and report and discuss both results (Aguinis et al., 2013). In other
cases, we can perform statistical manipulations in our statistical models to
“deweight” those outlier observations using robust techniques (submit median,
trimmed means, and winsorized mean) so that the estimates better represent the
sample. We can try transforming the data to minimize the distorting effect of the
extreme case (Zimmerman, 1995) (logarithmic or square root transformation) or
use statistical models that have different assumptions (e.g., nonparametric statis-
tics, bootstrapping, and generalized models). There are also specific robust
2.7 Outliers: Those Underestimated Exceptions 59

methods for hypothesis testing samples with outliers, such as Yuen’s robust test
using trimmed means. One of the difficulties of outlier treatments is that there is no
universally accepted theoretical framework for their treatment. In addition, the way
to proceed varies greatly depending on the particular discipline (e.g., economics,
psychology, pharmaceutics, and biology) (Rousseeuw & Leroy, 2003; Aguinis
et al., 2013).
An evolutionary biologist may be interested in these plot points and will attempt
to inspect them in light of other associated characteristics of the individual, includ-
ing interpretations somewhat within the scope of the study. The extreme values of a
particular trait within the natural distribution of the population, whether or not they
are considered outliers, have potential value from an adaptive point of view. Charles
Darwin saw this in his classic studies on the dynamics of variation and selection
(Darwin, 1859, 1868, 1871), and William Bateson in his analysis of variability dur-
ing development (Cock & Forsdyke, 2008; Peterson, 2008). Historically, evolution-
ary biology has shown that some rare expressions of a trait or set of traits can be
influenced by directional selection in some contexts (Westneat & Fox, 2010). Thus,
what used to be the tail end of the distribution may be the “middle” value of a par-
ticular trait now and vice versa. Indeed, this dynamism is at the heart of natural and
sexual selection.

2.7.1 An Outlier Hiding a Spider’s Secrets

The Allocosa senex is a wolf spider inhabiting coastal areas that possesses sex role
reversal, as females compete for males and males exert mate choice (Aisenberg
et al., 2007) (Fig. 2.4a). The male builds a particularly long burrow, compared to the
one inhabited by the female, and remains in it until a receptive female finds it and
enters for copulation. Before mating, the female evaluates the length of the burrow
as an indirect indicator of the male “quality.” Finally, the male withdraws from the
burrow, and the female remains inside until the offspring are born. Interestingly, the
granulometry of the sand on the coasts where this species lives influences the char-
acteristics of the burrows. In this framework, De Simone et al. (2015) found that
adult males and juveniles built longer burrows in coarser substrates, whereas in
substrates with fine sand (to which they were not accustomed), burrows were sig-
nificantly shorter (Fig. 2.4b).
There is an exciting point for our book. An outlier in the box plot corresponds to
juvenile burrows in the fine-grained substrate (Fig. 2.4b). One individual built a bur-
row much longer than the rest, even larger than the burrow built in a coarse sand
substrate. In other words, a “super burrow” is built by a juvenile male. If we were to
analyze, as we said before, only this variable (i.e., “length of the burrow”), it would
remain a simple curiosity. However, if we add other variables to understand this
“atypical” value, for example, specific body characteristics, we can appreciate
something very striking (Fig. 2.4c). This atypical individual in its burrow construc-
tion was the largest and heaviest, so it could be considered a “super individual” from
60 2 A Small World of Exceptions?

b c

Fig. 2.4 Examples of how the analysis of outliers revealed new key information in a scientific
study. (a) Burrow-digging wolf spider Allocosa senex (Image courtesy of Matías Izquierdo). (b)
Comparison of the length of the burrows built in sand with different substrates, highlighting a very
long burrow made by a juvenile in fine sand. (c) Relationship of the size of the burrow with the
weight of the spiders, showing the heavy weight of the juvenile that made the long burrow

the point of view of traditional physical conditions. The “super burrow” was made
precisely by the “super individual,” considering size and body weight. As these
individuals were collected in the field, we cannot discuss their origin or develop-
mental conditions. This individual probably possessed sufficient reserves and
strength to overcome the difficulties in building the burrow in an adverse substrate.
Indeed, burrows in fine sand tend to collapse and require more silk covering by the
building spider. This example shows how not limiting ourselves to a “simple” out-
lier can teach us more about the relationship between variables and possible impli-
cations for the biology of this species. We consider this example as “a grain of
References 61

sand,” metaphorically speaking, in the immense universe of outliers. Any researcher

is confronted with these “annoying” points in the analysis. It would be a matter of
paying much more attention to them and valuing them in our discussions.

2.8 Key Concepts and Ideas in This Chapter

• The definition of exception is strongly linked to the definition of rule. Both are
antonyms and necessary to give entity to what each alludes to.
• In human history, exceptions have been seen as synonymous with success and
what stands out positively from the average, not only in science but also in poli-
tics, art, sports, and other areas. However, they can also have the opposite effect
when they are exceptions in a negative extreme such as deformities, teratologies,
or monstrosities, which in this case produce aversion or rejection.
• In biology, exceptions can become a starting point that generates changes,
whether in morphology, behaviors, different types of organisms, and systems of
evolution.
• To detect exceptions in the scientific world, we must have a detailed look to
avoid obviating, hiding, or considering them less important. This care gives us a
more complete and comprehensive approach to all biological phenomena.
• Individuals who are exceptions within a population could be considered so by
observing a single variable that makes them stand out from the rest or by a set of
variables or traits, which may or may not be associated with each other.
• Extreme cases in the phenotypic expression of a given trait in a population may
be less striking to the observer. However, these quantitative values that are far
from the average value and that fall outside the norm are essential when we talk
about the influence of factors affecting that trait.
• Outliers are essential data for detecting oddities in the natural world. Many
times, they are eliminated or seen as a nuisance to the study. However, outliers
can be an opportunity. After checking the nature of the data, a detailed analysis
can help one to find interesting patterns in our study model.

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Chapter 3
Associations and Dynamics Between Rules
and Exceptions

Everything flows, nothing stands still

—Heraclitus

Contents
3.1 Introduction 66
3.2 C  omplementary Concepts When Focusing on Rules and Exceptions 66
3.2.1 On Terms and Their Synonyms Related to the Normal and the Abnormal 66
3.2.2 Singularity: Each Living Being is Unique 67
3.2.3 Are There Rules for Predicting the Occurrence or Type of Exception? 68
3.3 Three Perspectives on the Dynamics Between Rules and Exceptions 69
3.3.1 The Possibility of Mixed Patterns 69
3.4 Main Directions of the Changes 70
3.4.1 “Conservative” Rules and Exceptions? 71
3.4.2 Movements of Rules “With Continuous Distribution” 71
3.4.2.1 Analysis from Biological Evolution (i.e., From Scenario 1 of Rule
Movement) 72
The Sexual Conflict as an Example of the “Conflict of Interest”
Between R and E 76
3.4.2.2 Analysis from the History of Biological
Sciences (i.e., From Scenario 2) 77
3.5 Key Concepts and Ideas in This Chapter 78
References 79

Abstract There is a complex relationship between rules and exceptions in different

contexts. Rules and exceptions are not always distinct but rather dynamically related
concepts. There are a variety of alternative terms, such as patterns, normalities, rari-
ties, and abnormalities, that can be used interchangeably with rules and exceptions.
This emphasizes the flexibility in the use of these terms. Singularity is often used as a
synonym for exception, as something unique. This uniqueness can be both positive
and negative and contributes to the value of individuality in biology. This feature dem-
onstrates the possibility of mixed patterns and the importance of scale in analyzing

© Springer Nature Switzerland AG 2024 65

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_3
66 3 Associations and Dynamics Between Rules and Exceptions

them. Four scenarios of change and two types of dynamics between rules and excep-
tions can emerge. These scenarios cover situations where rules remain stable, excep-
tions persist, rules become exceptions, and vice versa. These dynamics can occur in a
variety of contexts, including biological evolution. Changes in scientific knowledge
and paradigms can be compared to the dynamics between rules and exceptions.
Overall, this chapter explores the complex and interrelated nature of rules and excep-
tions in different domains, highlighting their dynamic and evolving relationships.

3.1 Introduction

We have referred to rules and exceptions according to their definitions and contexts
to see how they can be linked. Specifically, we will analyze which rules and excep-
tions are not watertight compartments, but, on the contrary, there is a dynamic
between them, both being important. However, before this, we will review alterna-
tive or similar expressions to the concepts of rules and exceptions. Some of them we
have already mentioned, and the reader may wonder whether we can use them as
synonyms.

3.2 Complementary Concepts When Focusing on Rules

and Exceptions

3.2.1 On Terms and Their Synonyms Related to the Normal

and the Abnormal

When we talk about rules, we can refer to them directly throughout the book as pat-
terns or normalities. The same applies to exceptions and associated terms such as
rarities or abnormalities. In this book, we focus mainly on the use of the terms rule
and exception as antonyms, although we also use the meanings of patterns and rari-
ties in some cases, and it is important to emphasize that we should be flexible in the
use of these terms (Boxes 1.1 and 2.1). The concept of rule is more closely linked to
that of law or may allude to establishing and identifying more flexible “mini laws.”
Patterns are also something that the observer identifies from the observation of
nature. From a pattern, a rule may or may not be explicitly stated. We can state that
when we speak of patterns, these are what exists as such, the morph “x,” the func-
tional type “x,” that is, what “is” expressed from the genotype at the phenotypic
level of this or that organism and that is shared, expressed, evidenced by the major-
ity of the individuals of the population, species, clade. Thus, the pattern occurs at
the level of the group in a given time and space. In a way, the rule can be synony-
mous, so we recommend flexibility on the part of the reader when we use rules or
patterns indistinctly (or other options such as norm, standard, etc.).
3.2 Complementary Concepts When Focusing on Rules and Exceptions 67

As for exceptions, its entity will always be relative to something else (time,
group, or space). Rarities correspond as an antonym to patterns (they allude to what
is not common concerning the pattern), and hence this book could be entitled “pat-
terns and rarities” instead of “rules and exceptions.” In any case, the obsession with
definitions should not distract us from what we are analyzing, the common versus
the rare, whether the researchers of the discipline expose it as a rule versus excep-
tion or as pattern versus rarity or, what is hardly less evident, as frequent versus
infrequent occurrence. This situation derives from the fact that nature is not discrete
but rather continuous in many of its transitions. The discrete, deeply analyzed,
finally becomes a continuum in our eyes. Let us always remember that definitions
help, they are necessary, but they must not cage our minds.

3.2.2 Singularity: Each Living Being is Unique

Interestingly, one of the synonyms of exception is “singularity,” which has the syn-
onyms “unique, particular, special, remarkable, outstanding, rare, strange” and the
antonym “common.” Uniqueness, therefore, is the quality that distinguishes some-
thing from other things of its kind. For example, the concept of uniqueness has been
used in mathematics for specific functions that exhibit unexpected behavior when
certain values are assigned to the independent variable(s) (Arnold, 1981). In the
case of “unique,” it is said to be “singular, exclusive, one, pure, scarce, peculiar,
characteristic,” its antonym being “ordinary.” Whether singular or unique, these
terms connect with things that we will see in a broad, holistic view with the value of
each organism in nature.
In humans, a “singular” person stands out (positively or negatively) above the
rest. We have elaborated on this idea in Chap. 2. However, here the question arises,
can we extrapolate this same thing to the rest of the living beings? We do not refer
only to the explicitly striking ones but to some quality or several qualities that make
them an exception in their group or according to a view of time or space. It is a para-
dox that what is the rule, for example, in a species, is the product of the sum of
singularities. This “cryptic singularity” (i.e., not perceived or being underestimated
by the observer) within the pattern is something that, from a holistic point of view,
should call attention to the importance and value of the uniqueness of each living
being in intra and interspecific interrelationships.
In this context, it is helpful to bring up the inspiring book Life Trajectories:
Biology, Freedom, and Determinism by Rose (2001), where the author draws our
attention to scientific reductionism when we only think of the determinism of genes
to mark and define the identity of living organisms. Indeed, since the book’s publi-
cation, this has fortunately been changing toward a view that pays more attention to
the surrounding environment, epigenetics, the evolutionary biology of development,
the social context, and, finally, to each individual in himself/herself. Rose (2001)
shows and highlights the value of individuality by commenting that everyone has
“his or her life trajectory.” It is interesting to note that other authors, such as Fritjof
68 3 Associations and Dynamics Between Rules and Exceptions

Capra, tend to focus more on the “search for the pattern,” even analyzing similar
aspects such as the phenomenon of emergence, patterns in nature, and body geom-
etry. In other words, they aim to find a synthesis of the “whole” in life. Its vision is
as a “network” or “intimately linked system” rather than emphasizing singularity
(Capra, 1996; Capra & Luisi, 2014). It is not that Steven Rose denies these
approaches but emphasizes more individuality, the freedom implicit in each indi-
vidual to have, exhibit, and perhaps change his or her trajectory, as an undervalued
aspect of modern biology. Perhaps because of the obsession to “order” and hierar-
chize the observed and the impressive biological diversity in patterns and rules, we
are missing the richness of the uniqueness of each living being. For example, the
value of the individual has been indirectly highlighted in the advancement of per-
sonality studies in animals, including “lower” groups such as arthropods, anemo-
nes, or even bacteria (Briffa & Weiss, 2010; Briffa & Greenaway, 2011; Carere &
Maestripieri, 2013; Kralj-Fišer & Schuett, 2014; Kaiser & Müller, 2021).
Note that while Capra’s vision is strongly connected with the search for rules,
Rose’s vision links more emphatically with the valuation and rescue of rarities or
exceptions. The “holistic” context is very present in both visions, but they point to
different scales of life organization. In the following, we will examine the dynamics
between these “opposites.” They are focused (unless otherwise stated) on rules and
exceptions and their interchange in different perspectives and contexts.

3.2.3 Are There Rules for Predicting the Occurrence or Type

of Exception?

It is interesting to consider whether it is possible to predict the occurrence of excep-

tions. That is, we can propose predictive rules for the occurrence of different types
of exceptions according, for example, to a certain spatial context (e.g., surrounding
environment, other organisms at the community level) or temporal context (e.g.,
ontogeny, evolutionary time). Therefore, if a particular factor exists, then the prob-
ability of occurrence of a particular rarity increases or decreases.
Theodosius Dobzhansky summarized in his writings on genetics some of the
classic experiments carried out during the first half of the twentieth century on the
effect of mutations to promote predictable changes (Dobzhansky, 1982; Ceccarelli,
2010). Indeed, today, we know that some specific pathologies and syndromes can
appear because of certain carcinogenic factors related to age and nutrition. Therefore,
if there are rare hereditary or environmental pathologies in biomedicine, the ques-
tion arises as to whether we can predict their appearance. If we extrapolate this
beyond biomedicine, we may find that certain teratological exceptions are not
always due to chance but will be determined by spatial and temporal factors.
Unfortunately, it is not easy for us to identify them to make accurate predictions. For
example, the malformations detected in fossils of ammonites and other groups may
have been the consequence of teratologies produced by extreme climatic changes or
gene depletion. We will discuss some examples of this in Chap. 5 of this book.
3.3 Three Perspectives on the Dynamics Between Rules and Exceptions 69

3.3 Three Perspectives on the Dynamics Between Rules

and Exceptions

Thus far, we have presented the main characters, rules and exceptions, their termi-
nological variants, and fundamental theoretical options for their interpretation. We
will now consider them in more detail regarding how they are sustained in time,
space, and group. That is, we will not only limit ourselves to the variable “time,”
whether historical from the point of view of knowledge, or “evolutionary” within
the framework of the evolution of a species. Indeed, these three contexts interact,
and the subject is much more complex than simple linear temporal unidirectionality.
We will address different scenarios and examples throughout the book.

3.3.1 The Possibility of Mixed Patterns

As we see in Fig. 3.1a, we can have situations where the three contexts (taxonomic
group, spatial, and temporal) combine or interact to a greater or lesser extent. For
example, a rule can change in time in general and then according to certain spaces.
Additionally, all this can already be adjusted according to groups. This interaction
can also refer to something evolutionary. For example, how a body structure changed
over time within a clade (e.g., time-group combination) and, in turn, already in par-
ticular environments.

a b

Fig. 3.1 Context and scale of analysis governing the dynamics between rules and exceptions. (a)
Basic combinations in terms of interactions between time, space, and group contexts in the dynam-
ics between rules and exceptions. (b) The scale of the analysis will be larger or smaller according
to the level of the analyzed rule (e.g., type I, II, III, etc.)
70 3 Associations and Dynamics Between Rules and Exceptions

On the other hand, the scale of the analysis may also be different (Fig. 3.1b). That
is, if the study is focused on details of a phenomenon or is much more global. This
is very important because, as we saw in Chap. 1, this will determine whether we are
more or less likely to find exceptions to them. It is not the same to analyze major
patterns, more inclusive of all living beings (e.g., the presence of a genetic code and
how it works), as it is to analyze much more particular patterns (e.g., modifications
in a unique phenotypic trait, such as a particular appendage, be it a fin, a leg, or a
wing). More exceptions might be expected in the more comprehensive rules if they
were “generalized” without discrimination and thus included “subrules” that were
overlooked. However, exceptions would not be expected to occur if they were rules
of type I. It is an apparent paradox that may lead to confusion, but these are two
different situations that refer to the more globally applicable rules.

3.4 Main Directions of the Changes

We can find at least four situations of changes and two of change of dynamics
between rules and exceptions in any of the contexts of time, space, and group (sepa-
rate or mixed, Fig. 3.2). In the course of this book, we discuss and give examples of
these situations in more detail: (A) No change: we can have (1) rules that remain the
same (i.e., nothing or little change), regardless of the context (Chap. 4), and (2)

Fig. 3.2 Dynamics between rules and exceptions. (a) Situations in which both rules and excep-
tions remain stable, without significant modifications over time. (b) Situation in which rules and
exceptions remain unstable. Transitions can be maintained over time or reoccur. Abbreviations: E
exception, R rule
3.4 Main Directions of the Changes 71

exceptions that persist relatively as such (i.e., nothing or little change), regardless of
the context (Chap. 5) (Fig. 3.2a). (B) Dynamic framework: that is, specific to a
changing world. Here, we find (1) exceptions that become rules (Chap. 6), as well
as the opposite: (2) rules that become exceptions (Chap. 7) (Fig. 3.2b). These four
scenarios serve as a guide for the examples we will discuss in the following chap-
ters. Biology offers many examples of these four possibilities of dynamism between
rules and exceptions, whether in time (historical or evolutionary), in place/space, or
in group/clade (Fig. 3.2b).

3.4.1 “Conservative” Rules and Exceptions?

Indeed, whether dealing with a rule or an exception, the system can maintain very
stable temporal, spatial, and group conditions. While minor variations are allowed,
their significance is negligible. The constancy of these rules or exceptions is not a
result of their lack of variation. The ability for rules or exceptions to remain
unchanged depends partly on the scale of analysis, encompassing temporal, spatial,
and group dimensions. Instability is more likely to be found when the scale is signifi-
cantly large. Conversely, with a limited scale, it becomes less probable to detect
changes, resulting in greater stability. This apparent paradox, which links the percep-
tion of change to the scale, can be resolved by recognizing that this “conservatism”
is not universally upheld in the studied system. In other words, we observe a dynamic
relationship between rules and exceptions in these three contexts. Depending on the
specific case, we can observe changes in their importance and applicability.

3.4.2 Movements of Rules “With Continuous Distribution”

The rule (implicitly also the associated exceptions but with emphasis on the rule)
undergoes changes when it “moves” toward ranges previously considered minori-
ties or mere exceptions and may even “dilute” or disappear entirely as an initial rule.
We can apply the look of the analysis of character analogies since the dynamics
between rules and exceptions (either in one direction or the other) is a crucial aspect
of explaining selective pressures (e.g., natural or sexual selection). We could start
from a situation of (dynamic) equilibrium whose distribution is reflected in a way
analogous to a stabilizing selection in evolution. That is, where the rule or norm is
exhibited by an average number of individuals located at the center of the distribu-
tion, while progressively to the left and right, there will be fewer individuals exhibit-
ing the rule at its maximum expression until reaching extreme values at the margins
of the distribution. The latter will be, in a “combined” form, the sum of (1) an
“extreme” expression of the trait, far from typical and, perhaps also (not always),
(2) a very low frequency of occurrence (i.e., few individuals) compared to a high
occurrence (many individuals) concerning that particular trait(s).
72 3 Associations and Dynamics Between Rules and Exceptions

From this initial scenario, a shift may occur within the data distribution, favoring
individuals who exhibit a specific variant of the overall spectrum of expression in
the analyzed pattern. This shift resembles the effects observed under directional
pressure. Therefore, as a result of this movement, the conformations of what will
later become the new majorities and minorities will be modified. It is the same if we
have a situation of disruption, where formerly extreme values become rules, or at
least one becomes the rule. This situation may or may not imply the disappearance
of the original rule.
We could also analyze a situation where the rule becomes ambiguous and unclear.
An example could be the case of a scenario analogous to a dispersion of the expres-
sion of the feature to both sides by similar parts but at the expense of the midpoint.
Therefore, the rule will be “fuzzy.” This situation could occur if there are many
exceptions to the rule that would paradoxically attain the entity of “mini rules,”
either individually or in groups, through potential associations between them. This
scenario could lead to an extreme situation where it would already imply the “disap-
pearance” of the rule as such within the framework of a new flat-type distribution.
Here, there would no longer be any exceptions either. Minorities and majorities
would no longer be distinguishable as such. Everything would be “equal.”
The above leads us to attempt to plot the possible scenarios of “movements” of
the rule. The options may imply, depending on the perspective of analysis, (1)
movement due to biology’s action, for example, due to evolutionary or ecological
change, and (2) movement from the approach of the history of biology as a science,
that is, due to a modification in the vision of man as a researcher of biological phe-
nomena. The analysis of these movements will allow us to conclude that the evolu-
tion of rules follows the same patterns of biological evolution (i.e., evolutionary
processes of traits and phylogenetic patterns of taxa). Furthermore, there are simi-
lar patterns of evolution of rules in forms of change in the distributions of the ele-
ments involved in all contexts of the universe, including abiotic, biotic, and even
manifestations of man in interpreting these—for example, science, ideas, art,
technology.

3.4.2.1 Analysis from Biological Evolution (i.e., From Scenario 1

of Rule Movement)

Not all traits are distributed evenly in a population. In some cases, there is a clear
“zone” where the majority of individuals fall, while others fall outside of this range.
Figure 3.3a shows a state according to a neutral or stabilized situation. Not neces-
sarily toward both sides of the mean distribution, we will find real exceptions (e.g.,
it could well be something already biased toward one side). Within a particular
“zone,” there exists a specific range of trait expressions that is considered the typi-
cal pattern due to its prevalence among the majority of individuals (represented on
the Y-axis as either an absolute number or proportion). For instance, in a species
analyzed from a group context, we would observe a “continuous” rule that pertains
to a character or event displaying continuous attributes, such as a specific color tone
3.4 Main Directions of the Changes 73

or size. Additionally, there would be “minorities” comprising individuals express-

ing a narrower range of the rule. Among these minorities, extreme values can
be found.
The transition from the situation described in Fig. 3.3a to the scenario depicted
in Fig. 3.3b involves a shift driven by directionality. In this new scenario, what was
previously considered an exception (or a group of exceptions or their associations,
to account for multiple possibilities) now becomes the new rule. This phenomenon
can be observed in intraspecific analyses of traits. For instance, rare or extreme
colorations, ornaments, or unusual body sizes may evolve into the new norm if they
are progressively favored through natural or sexual selection over the previously
predominant expressions conforming to the majority.

a b

c d

Fig. 3.3 Dynamics between rules and exceptions illustrated in individuals of a population with a
certain trait “X.” (a) A neutral or stabilized situation, where the majority of individuals fall in the
“norm” or “rule,” while others fall outside of this range (minorities and exceptions). (b) New sce-
nario with a shift driven by directionality, which was previously considered an exception, now
becomes the new rule. (c) The rule zones are maintained but with higher numerical representative-
ness, so we speak of “augmented” patterns, and a narrowed rule. (d) The areas of rules, minorities,
and exceptions are maintained but with lower numerical representativeness, so we speak of
“diluted” patterns. Color references: orange indicates the majority/rule zone; green indicates the
exception zone; gray indicates the minority zone. References: Arrows indicate selective pressures
that change distributions; dotted line, neutral pattern 3.3A
74 3 Associations and Dynamics Between Rules and Exceptions

Another option for change in the rule would be the one shown in Fig. 3.4b, where
the “old” rule is maintained, but another equally important one emerges from some
previously extreme value. For example, if a range of coloration that was the “mean”
persists in one sex but no longer in the other, it would shift to another coloration
value. A minimum of the population previously expressed this value (e.g., now
males are shifting to an intense body color due to advantages in a mate choice con-
text). Alternatively, this disruptive situation could occur in two geographic spaces—
for example, individuals of the same species in two populations isolated from each
other. In one of these populations, the species changed to a more cryptic color for
camouflage to avoid predators. In a phylogenetic case, imagine that an ancestral
species would retain the classic pattern, the “old” rule, while a new species would
present the new rule as a pattern. It is interesting to see how specific extreme values

a b

Fig. 3.4 Dynamics between rules and exceptions illustrated in individuals of a population with a
certain trait “X”. (a) Distribution of “mini rules” in a given distribution, with the appearance of
exceptions and majorities in local regions. (b) The “old” rule is maintained, but another equally
important rule emerges from some previously extreme value. (c) Two nonextreme values in a
minority pool on either side of the mean become two rules, and the old rule does not persist. Color
references: orange indicates the majority/rule zone; green indicates the exception zone; gray indi-
cates the minority zone. References: Arrows indicate selective pressures that change distributions;
dotted line, neutral pattern 3.3A
3.4 Main Directions of the Changes 75

could overlap between the field of the two rules at the beginning and progressively
reach a point where these margins would no longer be shared. We must remember
that this can be analyzed in populations at the level of an intraspecific or interspe-
cific analysis.
An intermediate situation occurs when two nonextreme values in a minority pool
on either side of the mean become two rules (Fig. 3.4c). In this case, the old rule
does not persist (it either no longer exists or is now an exception to one and the other
new rule). A situation could even occur where the new rules on each side arise from
the respective exceptions (i.e., not only from one of the minimum values, as in
Fig. 3.4c). The rule tends to disappear in any of the options. This could occur, for
example, because it could be more costly in the group, spatial, or temporal context
(or a conjunction of all of them).
Another case is when there is polymorphism in the trait and some advantage in
it. For example, populations with different geographic distributions may have dis-
tinct colorations because they are adapted to the specific environments where they
live and to camouflage themselves from predators. The rule (i.e., a stable mean color
to which the majority conformed in Fig. 3.3a) is diluted, and we could already have
what is schematized in Fig. 3.3d.
There it could even be in the range from zero to “x” value of the trait expression
as before or else spread toward new values (hence the “cuts” with two orange lines,
to show that this “plateau” could well be more extensive than what is shown on the
X-axis for reasons of graph space). In addition, we could have before this or at some
time, space or group a situation of several smaller, smaller “mini rules” (Fig. 3.4a),
with extreme cases with fewer individuals for each or in the “flatter” total of
Fig. 3.3d, only two extremes. In either case, the gap will be smaller than that between
the extreme cases and the mean in Fig. 3.3a.
Finally, the latter could directly disappear, as a low proportion of individuals
exhibit any trait value. Here, it is impossible to identify the original rule. This situ-
ation would represent an extreme, almost evolutionary anarchism, at least temporar-
ily. This case is illustrated with the symbol of infinity, not because it is so in reality
but could extend further than is limited in the X-axis.
In short, every example of an evolutionary, ecological, and developmental nature
could be expressed from a viewpoint such as the one mentioned change in the rule
of biology itself. It is certainly not easy to frame options and examples so quickly,
first, because, in many cases, we need to learn all the processes involved. These
examples start from a normal distribution of traits and illustrate what would be
defined as a rule. However, what would happen with other types of distribution?
Could rules behave under these other types of statistical distributions, such as expo-
nential ones? Moreover, as mentioned, we are assuming a “continuity,” that is, con-
tinuous values, when it could be presence–absence or with gaps, intervals, without
being continuous per se.
Of course, these graphs are limited and only schematize the evolution of a single
trait. Changes could occur at a multidimensional level, with multiple variables inter-
vening together. Moreover, graphically, “positive” or “negative” points are quanti-
fied as a function of values of expression of the pattern presented by individuals. It
76 3 Associations and Dynamics Between Rules and Exceptions

is limited to think that it is perhaps as simple as “above” or “below” the rule’s core.
In addition, the graphs aimed to consider the number of individuals as the determin-
ing parameter to establish a rule or an exception. We take the criterion of “how
many” individuals express traits in a specific manner. Indeed, depending on that, we
say whether or not that is a rule. In short, the baseline analysis presented here of
general guidelines and representative examples of the dynamics between rules and
exceptions may inspire mathematicians in biology to organize this potential better,
considering its value and limitations.

The Sexual Conflict as an Example of the “Conflict of Interest”

Between R and E

An interesting example of dynamics between rules and exceptions occurs in areas

of evolutionary biology concerning the interests of the sexes. Specifically, we refer
to sexual conflict and, in particular, to when intralocus type conflict has been ana-
lyzed. We take as an example the work of Cox & Caslbeek (2009), which is useful
as a review with its graphs adapted from other studies on the subject (e.g., Rice &
Chippindale, 2001; Day & Bonduriansky, 2004; Bedhomme & Chippindale, 2007).
First, we would have a theoretical “neutral” situation in which the conflict
between males and females does not exist (or is at its minimum expression). This
situation would coincide smoothly with the distribution in Fig. 3.3a of the relative
fitness optima of each sex. Although this would be the theoretical distribution of an
eventual phenotypic trait encoded by a gene, it could also happen that there are
allelic variants with different optima in each sex. This would then imply that there
is, in fact, an underlying “unresolved” conflict. In other words, as in dotted lines, we
could imagine two bells, such as those in Fig. 3.4c, the presence of a conflict that
underlies but does not yet manifest itself for different reasons.
On the other hand, the conflict could become “partially resolved” if, in one sex,
a particular expression of the trait under analysis occurs and is exhibited to the left
of the mean value of the previous distribution of the same. In contrast, in the other
sex, the expression occurs to the right of that preceding mean. Finally, the conflict
could be “totally resolved” if the “old” rule disappears entirely. Therefore, on both
sides of the distribution, they have extreme values as patterns in relation to the pre-
vious situation and may not even overlap with the average zone of the previous
distribution of the trait. In short, there are at least four possible situations in intersex
conflict: no conflict, unresolved conflict, partially resolved conflict, and fully
resolved conflict. All this is a function of different optima of the trait expression in
each sex, a fact reflected in the distribution of expected and observed values.
From a broader perspective, when considering the theoretical level, this entire
framework and context of sexual conflict prompt us to contemplate whether there
might be “distinct optima” for implicit (or perhaps “evident” but unexpressed) rules
and exceptions. This question could be posed both by action from biology and the
history of science, as we explain below. These optima between a rule and its pool of
exceptions would be quite opposed. However, they would not cease to be like “the
3.4 Main Directions of the Changes 77

two sides of the same coin.” They mutually complement and rely on each other to
establish their individual identities and strengthen their respective characteristics.
Suffice it to recall how the respective definitions overlap and need to give entity to
what is a rule and what is an exception. Seen from a dynamic approach, we find that
they are different, with optima going in opposite directions (i.e., if you are a rule,
you are not an exception and vice versa). Nevertheless, they can transmute to each
other in any change that eventually occurs at the biological evolutionary level or of
scientific knowledge in temporal, spatial, and group contexts.
On the other hand, we could make the situation more complex if we were to add
to this “disruption in optimum” the fact that something can be a rule or an excep-
tion. This criterion will depend on the perspective or scale from which the situation
is analyzed, so the conclusions should be limited to a given perspective and approach
without ever generalizing. An example we will analyze further is the existence of
traits that appear in phylogenetically derived groups within a clade and do not occur
in the rest of the members. Such is the case that we will analyze later the presence
of a true epithelium in a group derived from sponges. In them, the presence of epi-
thelium is a rule. However, this characteristic is a remarkable exception in most of
the phyla.

3.4.2.2 Analysis from the History of Biological Sciences (i.e.,

From Scenario 2)

The previously exposed view on the “movements” of rules in biology could also be
helpful to us when analyzing changes in the historical rules of knowledge in bio-
logical science. We have commented on changes in the rules due to the contribution
of new technologies that modify paradigms and advances in methodologies and
science. In this context, Ruiz & Ayala (1998) highlight the analogy between the
progress of scientific knowledge, characterized by its continual changes, and bio-
logical evolution. They emphasize that science, like species, is in a constant state of
motion and transformation. There are also periods of quiescence without change
and another new stage of upheaval and modification. Thus, science can be examined
and understood in the same way as evolutionary epistemologies have proceeded. In
that case, the objects of knowledge are not living organisms but scientific concepts
and theories. First, the aforementioned epistemological perspectives of Lakatos,
Feyerabend, and, mainly, Kuhn could be well embodied in such graphs.
For example, certain ideas may be the prevailing paradigm with counter ideas
still scattered (Fig. 3.3a), followed by a moment of “chaos” where several options
are possible, and the central paradigm or rule is destabilized (Fig. 3.3b, c). This situ-
ation may result in some new ideas becoming a new paradigm and replacing the old
rule. Lakatos would follow the shift from Fig. 3.3a, b, where at least “all,” 100% of
the scope of the original rule does not fall away. However, the outermost belt of the
idea, the initial paradigm, is modified, but the core (here, as the rule that continues)
is still preserved. The new is not the opposite but complementary and belongs to an
even more superficial level of the belt concerning the altered one. In contrast,
78 3 Associations and Dynamics Between Rules and Exceptions

Feyerabend’s anarchism could be embodied in Fig. 3.3d, where there are almost no
rules, or they are no longer there. In this situation, every exception has a “double
entity” of common and rare; this discrimination would no longer exist and would no
longer make sense.
Second, more on the practical side, such as changes in scientific rules at the his-
torical level on biological concepts, such as monogamy in birds, and molecular
genetics, among other fields, serve this purpose. For example, an early rule postu-
lates that “most birds are monogamous” (Fig. 3.3a), where the mean implies a low
level of polyandry. We will see in more detail in the following chapters that this idea
was modified by advances in molecular techniques that showed that polyandry val-
ues were higher than initially thought (e.g., this would be the change to Fig. 3.3b).
From the “global” view for all birds, this change of interpretation has indeed
occurred beyond a specific clade. Even if we were to analyze the issue of monog-
amy in the animal kingdom, the vague idea of monogamy as something virtually
“ideal” prior to the theory of evolution and influenced by anthropocentrism has
disappeared as such. Today, we know that is one of many options within reproduc-
tive systems and that these are highly context-dependent (which would lead to a
figure of at least Fig. 3.3d if given equally). At least there can be at least two options
in a given clade, such as monogamy or promiscuity, depending on particular taxa
(this would be more toward, Fig. 3.4b or c, in a phylogenetic framework).

3.5 Key Concepts and Ideas in This Chapter

• When we speak of the concept of rule, it can be linked to that of law, although it
does not imply that it is and may be more flexible. The same is true of the concept
of exception when it is different or unique.
• Patterns that can be observed in nature can give rise to the enunciation or not of
a rule, as can its antonym, rarity, related to the uncommon.
• One of the synonyms of rarity could be uniqueness, which distinguishes rare
things from ordinary things. An interesting question is whether these singulari-
ties can be predicted, that is, whether predictive rules about the occurrence of
exceptions can be proposed.
• The dynamics between rules and exceptions, in one direction or another, are key
to their existence. The analysis of these movements will allow us to conclude that
the evolution of rules follows the same patterns as biological evolution.
• There are also cases where the rules are more ambiguous or fuzzy. In such a case,
the spread of the trait expression is to both sides by similar parts. This situation
occurs when there are so many exceptions that they reach the same entity as the
rules and could even make them disappear as such and generate a new flat-type
distribution without rules or exceptions.
• Scientific paradigm shifts in biology can be analyzed in the same way as move-
ments in rules in biological evolution. This view is interesting because it can
References 79

even transcend biology and allow us to see the dynamics of rules and exceptions
from another perspective.

References

Arnold, V. I. (1981). Singularity theory. Selected papers. Cambridge University Press.

Bedhomme, S., & Chippindale, A. K. (2007). Irreconcilable differences: when sexual dimorphism
fails to resolve sexual conflict. In D. J. Fairbairn, W. U. Blanckenhorn, & T. Székely (Eds.), Sex,
size and gender roles: Evolutionary studies of sexual size dimorphism (pp. 185–194). Oxford
University Press.
Briffa, M., & Greenaway, J. (2011). High in situ repeatability of behaviour indicates animal per-
sonality in the beadlet anemone Actinia equina (Cnidaria). PLoS One, 6(7), e21963.
Briffa, M., & Weiss, A. (2010). Animal personality. Current Biology, 20(21), R912–R914.
Capra, F. (1996). The web of life. Anchor Books.
Capra, F., & Luisi, P. L. (2014). The systems view of life: A unifying vision. Cambridge
University Press.
Carere, C., & Maestripieri, D. (Eds.). (2013). Animal personalities: Behavior, physiology, and
evolution. University of Chicago Press.
Ceccarelli, L. (2010). Shaping science with rhetoric: The cases of Dobzhansky, Schrodinger, and
Wilson. University of Chicago Press.
Cox, R. M., & Calsbeek, R. (2009). Sexually antagonistic selection, sexual dimorphism, and the
resolution of intralocus sexual conflict. The American Naturalist, 173(2), 176–187.
Day, T., & Bonduriansky, R. (2004). Intralocus sexual conflict can drive the evolution of genomic
imprinting. Genetics, 167, 1537–1546.
Dobzhansky, T. (1982). Genetics and the origin of species (No. 11). Columbia University Press.
Kaiser, M. I., & Müller, C. (2021). What is an animal personality? Biology & Philosophy, 36(1), 1.
Kralj-Fišer, S., & Schuett, W. (2014). Studying personality variation in invertebrates: Why bother?
Animal Behaviour, 91, 41–52.
Rice, W. R., & Chippindale, A. K. (2001). Intersexual ontogenetic conflict. Journal of Evolutionary
Biology, 14, 685–693.
Rose, S. (2001). Trayectorias de vida: biología, libertad, determinismo. Ediciones Granica SA.
Ruíz, R., & Ayala, F. J. (1998). eEl método en las ciencias. Epistemología y darwinismo. S. L. Fondo
de Cultura Económica de España (Colección Ciencia y Tecnología).
 Part II
Exploring Rules and Exceptions
from Life Sciences
Chapter 4
When THAT Rule Almost Persists
as THAT Rule

One never attains the total truth, nor is one ever totally
far from it
—Aristotle

Contents
4.1 Introduction 84
4.2 F lexibilizing and Enriching Fixed Ideas: A Brief Historical Timeline in Genetics
and Evolution 85
4.3 What Is a Biological Species: Is There a Rule? 89
4.4 Biological Rules: Some Historical Changes and Limitations 93
4.4.1 Analysis of Some Examples 93
4.4.1.1 Bergmann’s Rule 93
4.4.1.2 Emery’s Rule 103
4.4.1.3 More Rules, More Caution 104
4.5 Key Concepts and Ideas in this Chapter 107
References 108

Abstract In biology, theories are constantly enriched and adapted by new exam-
ples and scientific advances. In this chapter, we focus on the debate about the rules
in biology and their persistence over time as rules accepted by the scientific com-
munity. We exemplify this with Darwin’s theory of natural selection, which has
been nourished by new disciplines and technologies during the twentieth and
twenty-first centuries and has undergone transformations, although it undoubtedly
remains the dominant explanation of the evolution of biological systems. Biological
rules are dynamic, although they tend to remain relatively stable over time, and their
response to the appearance of exceptions can be variable, although the integration
of new knowledge into the field is usually gradual until the accumulation of excep-
tions is so significant that the applicability of the rules is questioned (crisis sensu
Kuhnian revolution of scientific knowledge). We illustrate this concept by analyzing

© Springer Nature Switzerland AG 2024 83

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_4
84 4 When THAT Rule Almost Persists as THAT Rule

the historical evolution of biological species concepts, and we draw attention to the
extrapolation of rules originally proposed for certain organisms and applied indis-
criminately to other groups without exhaustive testing (e.g., eco-geographic rules).

4.1 Introduction

Chapter 1 explored the concepts linked to rules and some basic examples. We have
seen that rules can change completely, become an exception, or even disappear.
Something much more subtle is that the rules are gradually modified and adjusted
over time, space, or a group of living beings. With new information in these con-
texts, a rule is modified according to the novelties now included. This situation hap-
pened with many classical rules of biology in fields such as evolution, genetics,
ecology, and biodiversity, among others. This “polishing” of this or that rule is so
common that it often goes unnoticed, either because it was considered obvious or
because we have not stopped examining the point. From a conservative perspective,
the “rule–rule” situation will most likely evolve into dogmatism. However, it also
provides relatively “stable” principles over time, allowing biological facts to be
understood and interpreted. We have already seen that a rule can be general or
restricted. The problem with any rule, especially in biology, is that it must inevitably
be taken as a principle or norm with some degree of flexibility. Otherwise, the first
exception encountered would justify rejecting the rule as inadequate when it should
be restricted relative to its influence to include additional cases. Although biological
rules generally explain the diversity of natural phenomena (e.g., ecology, genetics,
paleontology), many “exceptions to the rule” have been found over time. However,
the critical point is that new information does not necessarily mean that such rules
are wrong. However, some of the original claims must be revised and discussed
more carefully according to specific organisms and regions (Hone et al., 2008; Alho
et al., 2011).
Therefore, when advancing knowledge on a given topic, we have seen how one
reaches a point where the need arises to set basic principles to organize it, some-
thing inherent to the very essence of scientific thinking. One reason is to provide
logical coherence to this vast set of new data, enabling future experimental or com-
parative work on its components within an integrated and unified context, rather
than a confused, diffuse, or chaotic one. This plan can be challenging, especially in
biology, where there are, by nature, patterns and their exceptions. owever, it is good
to list some cases where these rules or principles have been proposed from evolu-
tionary biology, developmental biology, ecology, and other fields. Many of these
aspects will be addressed in the subsequent chapters, particularly those related to
the dynamics between rules and exceptions. Therefore, whether in specific or
broader fields, including biology, the integration of new knowledge necessitates the
organization of clear guidelines and rules, as well as the re-evaluation of existing
concepts and theories. This revitalization process involves incorporating novel
4.2 Flexibilizing and Enriching Fixed Ideas: A Brief Historical Timeline in Genetics… 85

findings to enhance their relevance. It is sometimes a process that takes time.

Sometimes it is slow and, most of all, never-ending. In the following, we will exam-
ine some areas of biology to illustrate this.

4.2 Flexibilizing and Enriching Fixed Ideas: A Brief

Historical Timeline in Genetics and Evolution

In the framework of the dynamics of rules, a body of ideas considered solid at a

given time will only sometimes be overturned entirely or replaced by others in the
future. In any case, what can happen is that new evidence, new information, or alter-
native options are incorporated into the broad umbrella of the initial rule. In this
way, the rule or “super rule” (if it is too broad) will be more flexible and enriched
with new data and perspectives. Indeed, this ultimately happens from the Kuhnian
view of the advancement of scientific knowledge and mainly refers to the theory of
organic evolution. This theory has been taken as a framework analogous to what
occurs at the epistemological level concerning models on conceptual evolution
(e.g., Popper, 1980, 1991; Ruíz & Ayala, 1998).
The occurrence of changes referring to knowledge about organic evolution is
obviously to be expected since it is a scientific theory, which implies something vast
that does not include a single principle or rule. Indeed, a classical definition of a
scientific theory is a “systematic ideational structure of broad scope, conceived by
the human imagination, which encompasses a family of empirical (experiential)
laws regarding regularities existing in objects and events, both observed and pos-
ited.” As we saw, the theory itself will include principles, laws, and rules (as we
said, these terms can and are usually used as synonyms) that attempt to organize the
observable regularities in objects and events.
Thus, it is expected that when new information about sublevels of rules and prin-
ciples is incorporated into evolutionary biology, the theory is eventually renewed,
and a new version emerges. As we observed in the first chapter, the “levels” of rules
are generally varied. It is true, in this sense, that at the “macro” level of the theory
of evolution, we have level I. Let us recall, in this case, what the third law of biology
says: “All living organisms have arisen from an evolutionary process.” While this
principle remains constant, it prompts us to consider whether the accompanying
body of data, hypotheses, ideas, pathways, and mechanisms remain unchanged. The
history of science in evolutionary biology demonstrates, thankfully, that this theory
is inherently flexible due to its subject of study.
Understanding all the details of the mechanisms and processes involved in how
this universal level I law is expressed is not simple and has yet to be completely
deciphered. We are dealing with more than a hundred-year-old theory which has
undergone changes and has not remained unaltered or fixed. This theory has not
been replaced by another but has been enriched, adapted, and modified over the
years based on advances in related disciplines. The theory of natural selection, pre-
sented by Charles Darwin in 1859, marked a profound departure from traditional
86 4 When THAT Rule Almost Persists as THAT Rule

creationist beliefs. Additionally, within the scientific community, there was a pre-
vailing emphasis on Lamarckism, which suggested the inheritance of acquired char-
acteristics. Unlike Alfred Wallace, Darwin did not outright reject this concept (Caso,
2020). However, through the introduction of his new theory, he indirectly chal-
lenged and diminished the significance of the Lamarckian paradigm.
One of Jean-Baptiste Lamarck’s notable contributions lies in that he was the first
to propose an evolutionary theory (Lamarck, 1809) that, while not directly conflict-
ing with religious beliefs, provided a groundbreaking conceptual framework in the
scientific community of his time. Indeed, Lamarck’s ideas were rooted in a solid
scientific, observational, comparative basis, especially considering the early stages
of biological knowledge when the fundamental principles were still being estab-
lished. Lamarck proposed two challenging laws: 1. on modifications of organs dur-
ing ontogeny of the individual by their use or disuse, and 2. on the nature of the
heritability of such modification, as long as it lasted in time and was present in all
progenitors. His second law, the inheritance of acquired characters, was later par-
ticularly questioned and rejected by most evolutionary biologists. However, in the
forthcoming chapter on the transformation of rules into exceptions, we will delve
into the resurgence of Lamarckism in recent decades (neo-Lamarckism). This resur-
gence suggests that the possibility of the second law regarding the inheritance of
acquired traits cannot be entirely dismissed across all groups of living organisms.
The modifications of Darwin’s original theory of natural selection that occurred
during the twentieth and twenty-first centuries have come mainly from technologi-
cal advances and knowledge associated with new disciplines that have helped to
further “polish” the strictly Darwinian vision. In general, it is not a matter of reject-
ing the initial theory but of adding more aspects to it, some of which were very
controversial at the time. Ultimately, they reinforce, to a greater or lesser extent, the
central postulates originally enunciated by Darwin. The dimensions in which evolu-
tion operates are increased, taking into account more types of variations that occur
in the life history of living beings (e.g., the genetic, epigenetic, behavioral, and
symbolic ones analyzed by Jablonka & Lamb (2014) in their excellent book
“Evolution in four dimensions”). Darwin himself relied on nineteenth-century rules
governing growth and reproduction, inheritance, interindividual variability, and
struggle for existence. It was from these rules that he developed his concepts on
natural selection, through which divergence of characters involved in this struggle
would occur, with the most successful form having more survival and success. In
contrast, the least improved form would eventually become extinct. Thus, at that
moment, he enriches and reorganizes the previously existing knowledge about liv-
ing beings.
As we know, the incorporation of Gregor Mendel’s studies on heredity was a key
addition and modification to Darwin’s original postulates. The publication of all his
work (Mendel, 1866) in which he postulates the three laws of heredity (or two in his
alternative vision if the first one is taken as implicit) was a fundamental pillar to give
more sense over time to many of the conjectures and hypotheses that Darwin had
drawn up. As we know, Mendel’s great work was not seriously considered when he
made it known in 1866. Indeed, it was around 1900 that it was rediscovered by
4.2 Flexibilizing and Enriching Fixed Ideas: A Brief Historical Timeline in Genetics… 87

several researchers, including William Bateson, who translated his work into
English (Bateson, 1902), thus forming the new and revolutionary scientific disci-
pline called “Genetics” (Gayon, 2016).
However, the relevance of Mendel’s studies in evolution was questioned and
debated for a long time. The subsequent contributions of W. Bateson, and particu-
larly that of Thomas H. Morgan and his team, regarding the Mendelian basis of
inheritance and the concept of chromosomes, solidified the gene theory (Morgan
et al., 1915; Morgan, 1926) and established genetics as a crucial discipline for the
study of evolution. The unit of variation was no longer the old concept of “gem-
mule” but the genes. However, studies on DNA structure would still be needed to
better define the concept of “gene” at the molecular level, a term that, in turn, would
undergo modifications in its meaning until today (Portin & Wilkins, 2017). From
Morgan’s work onwards, the focus at the hereditary level progressively concen-
trated on the structure of DNA as a unit of variation in evolution. With the contribu-
tions of the biologist and statistician Ronald Fisher (1930) and the geneticists Sewall
G. Wright (1931) and John B. S. Haldane (1932), who would establish more firmly
the knowledge on the genetic basis of evolution, in particular about the foundations
of population genetics.
The discipline of evolutionary biology progressively arrived at a more integrative
theory from Darwin’s original; for this consolidation, the contributions of the genet-
icist Theodosius Dobzhansky (1937), the zoologist Ernst Mayr (1942), the paleon-
tologist George G. Simpson (1944), and the botanist George L. Stebbins (1950),
among other key researchers, were fundamental. This improvement originated the
neo-Darwinism or synthetic theory of evolution (among several matching termino-
logical options). Again, rather than contradicting Darwin’s original ideas, what was
done was to add new information from modern genetics, paleontology, and com-
parative morphology. In the early 1950s, with the knowledge of the chemical struc-
ture of DNA (Franklin & Gosling, 1953; Watson & Crick, 1953; Wilkins et al.,
1953), the molecular basis of evolutionary theory was increasingly deepened. It
involved a refinement in the studies of evolutionary relationships and the concepts
of homologies based initially only on phenotypic characters. This integration led
over the years to revisit and reformulate concepts linked to the phylogenetic rela-
tionships of many groups of organisms. This work involves comparative morphol-
ogy and phylogenetics (Liò & Goldman, 1998; Whelan et al., 2001). Together,
advances in genetics and biochemistry would progressively bring molecular biology
to its apogee.
Advances in epigenetics have demonstrated that heritable changes do not always
involve mutations in the DNA sequence. Changes could also be due to nucleotide
methylation or histone protein acetylation. These events affect gene expression and
RNA micromodifications (Gayon, 2016; Banta & Richards, 2018; Lind &
Spagopoulou, 2018). Epigenetics recovered, in a way, the role of the environment in
shaping phenotypes, relaxing the quasidogmatic idea of unidirectionality from
DNA to phenotype existing up to that time (Jablonka, 2017; Cabej, 2018).
Knowledge about long-standing concepts, such as developmental phenotypic plas-
ticity, was revitalized and enriched, with Mary J. West-Eberhard at the forefront,
88 4 When THAT Rule Almost Persists as THAT Rule

giving it a more important role in evolution (West-Eberhard, 1989, 2003, 2005). The
value traditionally given to random mutations was not discarded at all. However, it
was relativized as the only way to generate variants in a framework of natural and
sexual selection.
These new perspectives from modern molecular genetics, epigenetics, and phe-
notypic plasticity resulted in a more effective and better integration of developmen-
tal biology with evolution, subjects that always seemed curiously associated but not
too influential on each other. It became clear that ontogeny could explain variants in
traits that were not necessarily explained by the classical action of natural selection
on mutations but rather by expressions during the development of the individual and
of a common set of genes. Progressively, a new concept of evolutionary develop-
mental biology, Evo-Devo (Hall, 2003; Carroll, 2008), emerged to summarize this
type of association. The concept of ecological evolutionary developmental biology,
Eco-Evo-Devo (Abouheif et al., 2014), was added to more strongly incorporate the
role of ecology at the level of development and evolution. Eco-Evo-Devo pays
attention to the influence of environmental signals in shaping phenotypes during the
ontogeny of an organism and how this affects the evolutionary process of a species.
Both views, particularly the first as the foundational one, represented a new para-
digm in the vision of evolution, referring to the fact that it consists of changes in
developmental processes. In the field of Evo-Devo, there is a focus on the recovery
of macroevolutionary phenomena, which involves exploring the potential continuity
between these phenomena and genetic-molecular and organismic changes. On the
other hand, in Eco-Evo-Devo, the emphasis is primarily on recovering the charac-
teristics of microevolution (Rendón & Folguera, 2014).
More recently, new innovative visions were raised with advances in neurosci-
ences, knowledge of “networks” at the nervous system level, and extensive analo-
gous concepts of “networks” in molecular biology and ecosystems. The study of
gene (or genetic) regulatory networks (Thompson et al., 2015) is, in fact, an essential
aspect of the Evo-Devo and Eco-Evo-Devo areas. This field is still in full development.
The addition of novel fields that are still in the process of consolidation, such as
epigenetics, phenotypic plasticity, Evo-Devo, Eco-Evo-Devo, gene regulatory net-
works, and neuron-like networks, among others, is what has led many scientific
leaders in these fields and evolution to call for a total and profound “update” of the
theory of evolution (Müller, 2007; Pigliucci, 2007). It is proposed to formalize and
not be limited to the traditional and unidirectional perspective of random mutations
and their subsequent natural selection according to their adaptive functional value.
This classical perspective is not denied, but other possibilities are added, comple-
mentary or alternative, depending on the context, level of analysis, and group. Thus,
instead of weakening Darwinian ideas, the simple, straightforward, and practical
scheme (still the heart of the theory) that was proposed more than 150 years ago is
reinforced. This new “postsynthetic theory” stage is called extended evolutionary
synthesis (Pigliucci & Müller, 2010; Laland et al., 2015). This new name tells us
that there is no contradiction with the preexisting but a significant conceptual
enrichment from the advances in these new areas (Pigliucci & Finkelman, 2014;
Müller, 2017; Fábregas-Tejeda & Vergara-Silva, 2018).
4.3 What Is a Biological Species: Is There a Rule? 89

Therefore, since evolutionary theory is a dynamic body of rules and principles, it

is expected that many more instances of refinement of this key area of biological
knowledge will emerge in the future. New “extensions” of the theory will continue
to take place in line with advances in different fields of biology. The question also
arises: could it be rejected at some point instead of being extended or enriched? This
situation would lead to a crisis no longer only partial, as when it was seen as incom-
plete in the past, but to a level of a Kuhnian revolution of scientific knowledge.
However, scientists have shown in the long run to be flexible and adaptable to per-
fect it and avoid falling into dogmatism, something that Darwin himself would
surely expect. Again, in perspective, we see how evolutionary theory is becoming
more complex. From a broad view at the level of time, it is a great rule that is becom-
ing more flexible and enriched rather than fragmented or replaced in its foundations.
We can conclude that (1) a great initial rule (the evolutionary theory proposed by
Darwin) varied but never ceased to be such; it was never replaced 100% but was
made more flexible, enriched, and therefore improved; (2) the theory was perfected
by the addition of other associated rules of another level, such as those of genetics;
(3) in this process, there were phenomena that initially could have been considered
somewhat circumscribed processes but that gradually became known to be quite
generalized among organisms (e.g., phenotypic plasticity, epigenetics); and (4)
indeed, some of these cases implied conceptual changes from considering an excep-
tion as a rule or vice versa, some of which will be analyzed in the following chapters.

4.3 What Is a Biological Species: Is There a Rule?

If there is a very controversial subject, diverse in approaches and criteria, then in an

endless debate at the core of biology, it is referred to as the “species concept”
(Kimbel & Martin, 1993; Wheeler & Meier, 2000). The “species problem” (as is
known) of what a species is has dominated discussions in the biological sciences
(Clarke & Okasha, 2013). Indeed, the recent detailed review by Zachos (2016)
shows that this issue is still under continuous discussion. There is now a greater
tendency toward a more holistic view, as recent advances in genetics, phenotypic
plasticity, and phylogeny are taken into account, some of which we have exposed
previously when discussing the extended theory of evolution. Indeed, we could
almost be talking about a level I rule regarding the degree of inclusiveness involved
in defining a species. From the strictly human, scientific interest, from our opera-
tional need as researchers we need to discern “without error” what is the “basic
unit” of analysis, which will then be linked at the phylogenetic level in trees, evolu-
tionary patterns, with other organisms. These relationships extend beyond interspe-
cific connections to higher hierarchical levels, encompassing genera, families, and
orders. It means how much we have wondered throughout the history of biology
about how to define an “organism.”
In addition to the challenge to define a species, we must consider both our exter-
nal perspective as observers and the intrinsic nature of the species itself within the
90 4 When THAT Rule Almost Persists as THAT Rule

biological reality of organisms. One thing is our gaze as observers, and another is
what the species represents by its existence in that biological reality. These two
ideas are closely interconnected, yet they entail distinct implications. For example,
when we talk about all organisms arising from an evolutionary process, this is a
natural biological fact. However, this has yet to imply that in the history of biology,
there is a definitive explanation of what evolution is and how it is carried out. Our
view is more changeable than nature itself.
Thus, at least two types of perspectives arise. On the one hand, a transversal
view, when analyzing and evaluating the differences between morphs that are poten-
tially different. An illustrative example can be observed by examining the terminal
branches of a phylogenetic tree, where we currently make transversal comparisons
within a specific clade. This approach, even when dealing with fossils or the com-
plexities of defining a species, has influenced definitions derived from phylogenet-
ics. An alternative framework, focusing on a temporal perspective, adopts a more
longitudinal approach by considering the transformation of a species over time.
This viewpoint acknowledges that a species undergoes changes and ultimately
ceases to be classified as the same species. This transformation has been extensively
discussed (Wheeler & Meier, 2000). As summarized by Zachos (2016), the bound-
aries between both general perspectives, the first more focused on the pattern (“the
picture”), while the second more on the process (“the film”), can be complicated to
establish.
There are so many perspectives to define species that it is difficult to say, at least
from the human methodological point of view, “what a species is.” Indeed, we have
multiple definitions (to explore this diversity of concepts, approaches, and implica-
tions, see Mallet, 2007; Zachos, 2016) (Box 4.1). One of the most widely used is the
one defined at the population level, the so-called “Biological concept of species”,
enunciated by Mayr (1970) “Species are groups of interbreeding natural popula-
tions reproductively isolated from other such groups.” Indeed, multiple variants of
this classic definition are commonly found on science education sites. For example,
“A species is often defined as a group of individuals that actually or potentially
interbreed in nature” (University of California, Berkeley, 2023), or “A biological
species is a group of organisms that can reproduce with one another in nature and
produce fertile offspring” (Nature Education, 2014). However, both sites clarify that
these definitions have limitations since they do not contemplate, for example, organ-
isms with asexual reproduction, something familiar in many invertebrates and plants.
Other species concepts are based on essential taxonomic criteria, particularly
comparative morphological criteria, and more recently, evolutionary genetics has
been added. Thus, there are typological definitions of species (including several,
even ancient ones), evolutionary definitions of species (a more linear view of the
status in evolutionary time as mentioned above), and phylogenetic and cladistic
definitions (a more transversal view, a specific current branch) (Mallet, 2007) (Box
4.1). Alternatively, or as a complementary approach (depending on the researcher),
there are two additional concepts to consider: the concept of recognition and the
ecological concept of species. To decide in our book on these options is not the
intention and would be superficial. What we find helpful in this controversial topic
4.3 What Is a Biological Species: Is There a Rule? 91

is how a rule can mutate over time. Additionally, how many definitions and criteria
are presented in opposition to each other? The consideration of these options is not
intended to imply a unidirectional choice between them. Instead, it can be viewed
as a multilinear approach, with varying degrees of emphasis depending on the
researcher’s specific area of expertise. For instance, an ecologist, taxonomist, or
geneticist may lean more toward one concept over the other. Suppose the focus is
more on gene flow and interbreeding. In that case, the researcher will prefer a defini-
tion associated with an “inbreeding concept” (i.e., biological, recognition, isolation
concepts) over others such as cohesion or monophyletic species concepts (Lee, 2003).
Therefore, in the face of so many options of definitions, it emerges that (1) we
cannot say that there is “a single rule or law” for what is considered a species and
(2) the understanding of species has undergone changes throughout history, influ-
enced by advancements in knowledge regarding crucial aspects of organisms,
including their evolution, genetics, ecology, and behavior. (3) Even today, there is
still a diversity of definitions and concepts due to the perspective of each discipline
and its biases (e.g., in evolution, ecology, taxonomy, behavior, genetics); (4) the
definition of what is considered to be a species will always be relative and biased,
depending on the approach of study. Thus, while some definitions will prevail over
others (e.g., biological or evolutionary over many others), it will not imply the elim-
ination of other concept options as “wrong.”
Of particular interest in this issue are two definitions that, in some way, have tried
to find a unifying concept of species. One of them is that coined by Templeton
(1989, 1998). His definition is a summation of all or almost all the components
implied in the other definitions: “A taxon characterized by cohesion mechanisms,
including reproductive isolation, recognition mechanisms, ecological niche, as well
as by genealogical distinctness.” Indeed, this definition is known as the cohesion
concept (Box 4.1). On the other hand, the concise general lineage concept proposed
by de Queiroz (1998, 2005): “Species are independent lineages.” In this case, rather
than adding several elements to the definition, the author highlights what will always
exist, what will characterize any taxonomic entity that is to be called a “species,” an
element common to all of them. In essence, the only necessary property will be to
have the general concept of species as separately evolving metapopulation lineages
(de Queiroz, 2007). All the other properties considered by other concepts are not
necessary but will depend on whether or not the species in question has adopted
them throughout its existence. Indeed, the author emphasizes that lineages do not
have to be “phenetically distinguishable, diagnosable, monophyletic, intrinsically
reproductively isolated, ecologically divergent, or anything else to be considered
species. They only must evolve separately from other lineages” (de Queiroz, 2007).
From the framework of our book, we see that the species problem is an excellent
example (Box 4.1) of how a rule (the concrete answer to what is a species?) will
depend on two-time contexts. On the one hand, we refer to historical time in the
biological sciences as regard changes in concepts, as well as to evolutionary time as
regard changes in the entity called species. On the other hand, the species concept
will depend on the context of the group, i.e., the taxon being analyzed. For example,
for an asexual taxon, a concept different from the classical biological definition
92 4 When THAT Rule Almost Persists as THAT Rule

would be easier to adopt. In turn, species concepts will depend on the spatial com-
ponent. For example, the ecological definition of species focuses on the specific
niche occupied by the organism within an ecosystem. In short, it is only possible to
choose one rule if there are many partialized, interrelated, context-dependent rules.

Box 4.1 Alternative contemporary species concepts

Modified from de Queiroz, 2007.

The truth is that everything is linked in biology. Although discussions about defi-
nitions concerning the species problem can be endless and fruitless (like most
debates about “definitions”), its implications would not be minor. For example,
there is an extreme definition of species based on the degree of extinction danger,
which considers any isolated population a species (Waples, 1991). Therefore, we
have that a species concept will impact fields that, in principle, may not be directly
associated in theory, such as endangered species by human action (“Endangered
Species Act”—George & Mayden, 2005). Here, the question arises: could the num-
ber of species in our biological lists and catalogs be reduced or increased depending
on the concept adopted to define a species? Eventually, this would impact species
management and conservation strategies, perhaps not only at the scientific level but
also at the political level, for the preservation of natural areas where endangered
species live (George & Mayden, 2005).
4.4 Biological Rules: Some Historical Changes and Limitations 93

4.4 Biological Rules: Some Historical Changes

and Limitations

If there is a field of biological sciences where we can appreciate in a didactic way

the implications of the scope and limitations of some postulates, then it is the one
concerning the so-called biological rules, which in many cases date back to the
times of Aristotle. By biological rules, we refer to a set of type II level rules, which
focus on ecological, eco-geographical, embryological, and genetic, among other
areas. We make this clarification since, in Chap. 1, we mentioned the levels of rules
and said that there was a level I that encompassed all biological organisms. From
this level, we move on to more specific areas where other levels appear that are more
restricted to certain organisms or ecological and/or geographical situations.

4.4.1 Analysis of Some Examples

Biology students come across many rules and laws during their careers. For instance,
Table 4.1 lists examples of biological rules, their scope, and some references to their
application. Many of them refer initially to a particular animal group. The problem,
and not a minor one, is that some of these rules were later extrapolated to other
groups of organisms, even quite distant phylogenetically from those originally stud-
ied. This led us to think that these rules had been poorly formulated from the begin-
ning or that they arose from considering extremely restricted cases. In reality, the
problem often lies in the extrapolation of the rule without taking into account the
factors mentioned above or even “forcing” its extension to other organisms. Below,
we highlight two illustrative cases of the problem, Bergmann’s and Emery’s rules.

4.4.1.1 Bergmann’s Rule

A classic example of a biological rule of the eco-geographic type is Bergmann’s

rule. This rule states that within a widely distributed taxonomic clade, larger popu-
lations and species are found in colder environments, while smaller species are
found in warmer regions (Bergmann, 1847). As depicted in Fig. 4.1, this particular
rule has received extensive analysis and has been the subject of considerable contro-
versy for over 150 years. There has been a significant amount of extrapolation from
the original postulates, which were formulated for specific mammalian taxa, to phy-
logenetically distant groups such as insects (Shelomi, 2012). Furthermore, it is not
a minor fact that the original paper was written in German; therefore, the English
translations could have added some confusion to the topic.
Table 4.1 Rules in biology. Examples of biological rules (principles, laws, theories), year of postulation, biological field, and range of application
94

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
Dogmas/axioms
1958 Central dogma Physiology DNA makes RNA, and RNA makes proteins. Once “information” has passed into F. Crick Broad Crick (1958)
of molecular protein it cannot get out again. The transfer of information from nucleic acid to
biology nucleic acid, or from nucleic acid to protein may be possible, but transfer from
protein to protein, or from protein to nucleic acid is impossible
1977 Woese’s dogma Evolution The evolution of ribosomal RNA was a necessary precursor to the evolution of C. Woese Broad Woese & Fox
modern life forms (1977)
Rules
1833 Gloger’s rule Ecology Within a species, more heavily pigmented forms tend to be found in more humid C. W. L. Gloger Restricted Gloger (1833)
environments (e.g., near the equator) (Endotherms,
plants see
Lev-Yadun,
2016)
1847 Bergmann’s Ecology Within a broadly distributed taxonomic clade, populations and species of larger size C. Bergmann Restricted Bergmann
rule are found in colder environments, and species of smaller size are found in warmer Endotherms, (1847)
regions ectotherms see
Mousseau, 1997;
Vinarskiĭ (2014)
1877 Allen’s rule Ecology Body shapes and proportions vary by climatic temperature by either minimizing J. A. Allen Intermediate Allen (1877)
exposed surface area to minimize heat loss in cold climates or maximizing exposed Endotherms,
surface area to maximize heat loss in hot climates. Animals from colder climates ectotherms see
have shorter appendages than animals from warmer climates Alho et al. (2011)
1884 Hertwig’s rule, Cell Biology A cell divides along its long axis. Predicts cell division orientation, which is O. Hertwig Broad Hertwig (1884)
long axis rule important for tissue architecture, cell fate, and morphogenesis
1892 Jordan’s rule Ecology There is an inverse relationship between water temperature and meristic D.S. Jordan Very restricted Jordan (1892)
characteristics (e.g., number of fin rays, vertebrae, or scale numbers) which are seen (Fishes)
to increase with decreasing temperature
1894 Bateson’s rule Morphology The long axes of the normal appendage and the two extra appendages lie in a single W. Bateson Broad Bateson (1971)
plane. One of the extra appendages is closer to the axis of the normal appendage, and
the other is farther away. The closer extra appendage is structured and positioned as
a mirror image of the normal appendage in a plane mirror placed between the normal
4 When THAT Rule Almost Persists as THAT Rule

appendage and the closer one. The farther appendage is the mirror image of the
closer one in a plane mirror similarly positioned between the two extra appendages
 4.4

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
1880 Deep-sea Ecology Deep-sea animals are larger than their shallow-water counterparts H. Nottidge Very restricted Moseley (1880)
gigantism Moseley (Deep-sea
animals)
1887, Cope-Depéret Evolution Animal population lineages tend to increase in body size over evolutionary time E. D. Cope, C. J. Broad Depéret (1907),
1907 rule J, Depéret Cope (1887)
1909 Emery’s rule Ecology Insect social parasites are often closely related to their hosts, such as being in the C. Emery Very restricted Emery (1909)
same genus (Host-parasites)
1915 Harrison’s rule Ecology Parasite body sizes covary with those of their hosts L. Harrison Very restricted Harrison (1915)
(Host-parasites)
1922 Haldane’s rule Genetics If in a species hybrid only one sex is inviable or sterile, that sex is more likely to be J. B. Sanderson Very restricted Haldane (1922)
the heterogametic sex Haldane (Hybrid species)
1942 Eichler’s rule Evolution Parasites tend to be highly specific to their hosts, and thus it seems reasonable to W. Eichler Very restricted Eichler (1942)
expect a positive covariation between the taxonomic richness of hosts and that of (Host-parasites)
their parasites
1950 Rensch’s rule Ecology Across species within a lineage, sexual size dimorphism increases with body size B. Rensch Broad (Animals, Rensch (1950)
when the male is the larger sex, and decreases as body size increases when the plants see
female is the larger sex Kavanagh et al.,
2011)
1959 Baker’s rule Population Colonization by self-compatible organisms is more likely to be successful than H.G. Baker Very restricted Baker (1959)
colonization by self-incompatible organisms because of the ability for self- (Self-compatible
Biological Rules: Some Historical Changes and Limitations

compatible organisms to produce offspring without pollination agents organisms)

1963 The Ecology Beyond a certain density of sowing, the number of surviving plants is not related to K. Yoda and Broad (Plants) Yoda et al.
self-thinning the initial seed density; instead, a constant relationship (W) is evident between the colleagues (1963)
rule, -3/2 power density of survivors and their total biomass.
rule, Yoda's
power law
(continued)
95
Table 4.1 (continued)
96

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
1964 Foster’s rule, Ecology Members of a species tend to be smaller or bigger depending upon the resource J. B. Foster Broad (Animals, Foster (1964)
the island rule, availability in the environment. Insular dwarfism explains the shrinking of animals plants see
or the island with the course of time due to limited food supply and more competition among the Biddick et al.,
effect species. Insular gigantism is seen in animals that migrate to the islands from the 2019)
mainlands. This is mainly because of reduced predation and lesser competition
1964 Hamilton’s rule Genetics Selection will favor altruistic behavior if the benefits to the recipient, multiplied by W. D. Hamilton Restricted Hamilton (1964)
the relatedness between actor and recipient, outweigh the costs to the actor. This is a (Altruistic
prediction from the Theory of kin selection species)
1966 Hennig’s Evolution As clades diversify, plesiomorphic traits dominate at centers of origin. The “most W. Hennig Broad Hennig (1966)
progression rule displaced” member of the clade will have the most apomorphic traits
1966 Deviation rule Evolution When two sister species split one deviates more strongly than the other from the W. Hennig Broad Hennig (1950)
common stem species
1967 Janzen’s rule Ecology Tropical habitats with reduced thermal seasonality would select for species with D. H. Janzen Restricted Janzen (1967)
narrow thermal tolerance, thereby limiting dispersal among sites of different (Tropical insects)
elevations showing little overlap in temperature
1967 Species–area Ecology The number of species found in a given area increases with the size of the area R. MacArthur & Broad MacArthur &
relationship sampled E.O. Wilson Wilson (1967)
1971 Thorson’s rule Ecology At low latitudes, animals tend to produce large numbers of eggs developing to S. A. Very restricted Mileikovsky
pelagic and widely dispersing larvae, whereas at high latitudes such organisms tend Mileikovsky (Benthic marine (1971)
to produce fewer and larger lecithotrophic (yolk-feeding) eggs and larger offspring, invertebrates)
often by viviparity or ovoviviparity, which are often brooded
1975 Community Ecology Competition, not random immigration, was the main force structuring the species J. Diamond Very restricted Cody &
assembly rules composition of islands. Reduced niche overlap, species occurring together on islands (Island species) Diamond (1975)
should have less niche overlap than random assemblages because they have
undergone specialization
1989 Rapoport’s rule Ecology Latitudinal ranges of plants and animals are generally smaller at lower latitudes than G.C. Stevens Broad Stevens (1989)
at higher latitudes
1996 Temperature– Ecology Organisms exhibiting a plastic response are capable of allowing their body size to D. Atkinson Broad Atkinson (1994)
size rule fluctuate with environmental temperature
1995 Phylogenetic Ecology Closely related species tend to occupy similar ecological niches P.H. Harvey & Broad Harvey & Pagel
niche M.D. Pagel (1991)
4 When THAT Rule Almost Persists as THAT Rule

conservatism
 4.4

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
2019 Read’s rule Ecology Trees that associate with arbuscular mycorrhizal fungi would dominate in warmer B. S. Steidinger Very restricted Steidinger et al.
forests (such as in the tropics, where tree growth is limited by phosphorous) and and colleagues (Mycorrhizal (2019)
ectomycorrhizal fungi in colder forests (where decomposition is slow and leaf litter fungi)
is abundant)
Principles
1865 Krogh’s Epistemology For such a large number of problems, there will be some animal of choice, or a few C. Bernard Broad Bernard (1865)
principle such animals, on which it can be most conveniently studied
1908 Hardy– Genetics Allele and genotype frequencies in a population will remain constant from G. Hardy & Broad Hardy (1908)
Weinberg generation to generation in the absence of other evolutionary influences W. Weinberg
principle
1948 Bateman’s Evolution Males typically experience more variance in reproductive success than females, due A. J. Bateman Broad (Sexual Bateman (1948)
principle to their ability to mate with multiple partners species)
1954 Lack’s principle Ecology The clutch size has been adapted by natural selection to correspond with the largest D. Lack Restricted (Birds) Lack (1954)
number of young for which the parents can, on average, provide enough food
1975 Handicap Evolution Costly signals must be reliable signals, costing the signaler something that could not A. Zahavi Broad (Sexual Zahavi (1975)
principle be afforded by an individual with less of a particular trait. It will be selectively species)
advantageous for a female to choose as a mate a male with some conspicuous
characteristic which is also a handicap as far as survival is concerned
1934 Dale’s Physiology A neuron performs the same chemical action at all of its synaptic connections to H.H. Dale Broad Dale (1935)
principle, other cells, regardless of the identity of the target cell
Biological Rules: Some Historical Changes and Limitations

Dale’s law
Laws
1816 Smith’s law or Paleontology Sedimentary strata contain different fossils (fauna and flora) that succeed each other W. Smith Restricted Smith (1816)
principle of vertically in a specific and predictable order that can be identified over a wide (Fossils)
Faunal horizontal distance
succession
1824–1826 Meckel-Serres Embriology A higher animal in its embryological development recapitulates the adult structures J. Meckel & Broad Serres (1827)
law of of animals below it on the linear “scale of being.” Conversely, lower animals E. Serres
parallelism represent permanent larval structures of the more advanced forms
(continued)
97
Table 4.1 (continued)
98

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
1828 Von Baer's laws Embriology Embryos start from a common form and develop into increasingly specialized forms K.E. von Baer Broad Von Baer (1828)
or laws of so that the diversification of embryonic form mirrors the taxonomic and phylogenetic
development tree. Therefore, all animals in a phylum share a similar early embryo; animals in
smaller taxa (classes, orders, families, genera, species) share later and later
embryonic stages
1835 Law of specific Physiology The nature of perception is defined by the pathway over which the sensory J. P. Müller Broad Müller (1838)
nerve energies information is carried. Hence, the origin of the sensation is not important. Therefore,
the difference in perception of seeing, hearing, and touch is not caused by
differences in the stimuli themselves but by the different nervous structures that
these stimuli excite
1838 Surface law Evolution The heat production of different-sized species should be related to their surface area P. Sarrus & Restricted Sarrus &
rather than their body masses if they were to maintain the same body temperature. J.F. Rameaux (Endotherms) Rameaux (1839)
Small animals should have greater mass-specific rates of metabolism than larger
animals, just as relative surface area increases with decreased size of similar-shaped
objects
1840 Liebig’s law of Ecology Growth is dictated not by total resources available, but by the scarcest resource J. Von Liebig Broad Liebig (1840)
the minimum (limiting factor)
1865–1866 Laws of Genetics A set of rules on the transmission by genetic inheritance of characteristics from G. Mendel Broad Mendel (1866)
inheritance or parent organisms to their offspring. It includes the law of Independent Assortment:
Mendel’s laws inheritance of one gene does not affect the inheritance of another gene unless the
of inheritance genes are linked on the same chromosome. Law of Dominance: one allele (the
dominant allele) can mask the expression of another allele (the recessive allele). Law
of Segregation: when two traits come together in one hybrid pair, the two characters
do not mix with each other and are independent of each other. Each gamete receives
one of the two alleles during meiosis of the chromosome
1904, 1934 Gause’s law, Ecology Two species competing for the same resource cannot coexist at constant population J. Grinnell, Broad Grinnell (1904);
competitive values. The competition leads either to the extinction of the weaker competitor or to G. Gause Gause (1934)
exclusion an evolutionary or behavioral shift toward a different ecological niche
principle
1889 Galton’s Genetics The two parents contribute between them on average one-half of the total heritage of F. Galton Broad Galton (1889)
ancestral law the offspring, the four grandparents one-quarter, and so on
1893 Dollo’s law of Evolution Once an organism has evolved in a certain way, it will not return exactly to its L. Dollo Broad Dollo (1893)
4 When THAT Rule Almost Persists as THAT Rule

irreversibility previous form

 4.4

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
1905 Law of limiting Ecology Growth is limited by the factor that is in the shortest supply. When a process is F. Blackman Broad (Plants) Blackman
factors conditioned as to its rapidity by several separate factors, the rate of the process is (1905)
limited by the pace of the “slowest” factor
1911 Shelford’s law Ecology An organism’s success is based on a complex set of conditions and each organism V. E. Shelford Broad Shelford (1911)
of tolerance has a certain minimum, maximum, and optimum environmental factor or
combination of factors that determine success
1914 Williston’s law Evolution Multipart structures in organisms tend to reduce the number of elements during W. Williston Broad (Animals) Williston (1914)
evolution but, at the same time, provide a mechanism to increase diversity and
functional specialization
1922 Jordan’s law Ecology Given any species in any region, the nearest related species is unlikely to be found in D. Jordan Broad Jordan (1922)
the same region nor in a remote region, but in a neighboring district separated from
the first by a barrier of some sort
1928 Lewis’ law Cell Biology The average apical area of a cell with n neighbors (divided by the average apical area F. T. Lewis Very restricted Lewis (1928)
of all cells) is proportional to its shape (epithelial cells)
1932 Kleiber’s law, Evolution The metabolic rate of an animal is proportional to its body mass raised to the 3/4 M. Kleiber Restricted Kleiber (1932)
3/4 rule power (Endotherms)
1936 Allometric Evolution A biological variable Y is related to the mass M of the organism by a power Law, J. Huxley & Broad Huxley &
scaling law Y=Y0M(exp=b), where b is the so-called allometric exponent G. Tessier Tessier (1936)
1942 Lindeman’s law Ecology During the transfer of organic food energy from one trophic level to the next higher R.L. Lindeman Broad Lindeman
of trophic level, only about ten percent of the transferred energy is stored as flesh. The (1942)
Biological Rules: Some Historical Changes and Limitations

efficiency, ten remaining is lost during transfer, broken down in respiration, or lost to incomplete
percent law digestion by higher trophic levels
1967 Ohno’s law Genetics The gene content of the mammalian species has been conserved over species not S. Ohno Restricted Ohno (1967)
only in the DNA content but also in the genes themselves. That is, nearly all (Mammals)
mammalian species have conserved the X chromosome from their primordial X
chromosome of a common ancestor
1973 Van Valen’s Evolution The probability of extinction for species and larger evolutionary groups bears no L. Van Valen Broad Van Valen Leigh
law, law of relation to how long it may have already existed (Red Queen hypothesis). Species (1973)
constant must constantly adapt, evolve, and proliferate to survive while pitted against
extinction ever-evolving opposing species
2000 Schmalhausen’s Ecology A population at the extreme limit of its tolerance in any one aspect is more R. Lewontin & Broad Lewontin &
99

law vulnerable to small differences in any other aspect R. Levins Levins (2000)
(continued)
Table 4.1 (continued)
100

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
Theories
1762 Germ theory of Medicine Microorganisms known as pathogens or “germs” can invade humans, other animals, M. von Plenciz, Broad von Plenciz
disease and other living hosts. Their growth and reproduction within their hosts can cause etc. (1705–1786)
disease
1830s Cell theory Cell Biology All living organisms are composed of one or more cells. The cell is the most basic M. Schleiden & Broad Schleiden
unit of life T. Schwann (1838)
1858–1859 Theory of Evolution Natural selection is the differential survival and reproduction of individuals due to C. Darwin & Broad Darwin (1859)
evolution by differences in phenotype. It is a key mechanism of evolution, the change in the A. R. Wallace
natural heritable traits characteristic of a population over generations
selection
1868 Ernst Haeckel’s Embriology Development (size and shape changes during ontogeny) of an individual organism E. Haeckel Broad Haeckel (1868)
revised literally and faithfully recapitulates the evolutionary history of its species
recapitulation (phylogeny). The development of advanced species passes through stages
theory, represented by adult organisms of the more primitive species and, thus, is classified
biogenetic law as a “strong recapitulation” theory
1932 Shifting Evolution Adaptive evolution may proceed most quickly when a population divides into S. Wright Broad Wright (1932)
balance theory subpopulations with restricted gene flow. In fitness landscapes (evolutionary
landscapes) the populations may move across an adaptive valley to a higher adaptive
peak
1944 Quantum Evolution To explain the rapid emergence of higher taxonomic groups in the fossil record. G. G. Simpson Broad Simpson (1944)
evolution Evolutionary rates differ from group to group and even among closely related
theory lineages. These different rates of evolutionary change can be bradytelic (slow
tempo), horotelic (medium tempo), and tachytelic (rapid tempo). The word
“quantum” therefore refers to an “all-or-none reaction,” where transitional forms are
particularly unstable, and thereby perish rapidly and completely
1949 Hebbian theory, Physiology An increase in synaptic efficacy arises from a presynaptic cell’s repeated and D. Hebb Broad Hebb (1949)
Hebb’s rule, persistent stimulation of a postsynaptic cell. It is an attempt to explain synaptic
and cell plasticity, the adaptation of brain neurons during the learning process
assembly
theory
4 When THAT Rule Almost Persists as THAT Rule
 4.4

Biological rule, Biological

Year law or principle field Statement Author Application range Citation
1966, 1976 Selfish gene Evolution Gene-centered view of evolution (the more two individuals are genetically related, it R. Dawkins, Broad Dawkins (1976)
theory makes for them to behave cooperatively with each other). A lineage is expected to G. C. Williams
evolve to maximize its inclusive fitness. As a result, populations will tend toward an
evolutionarily stable strategy
1967 Island Ecology The number of species on an island is determined by a balance between immigration E.O. Wilson & Broad MacArthur &
biogeography of new species to the island and extinction of existing species on the island R.H. MacArthur Wilson (1967)
theory
1967 r/K selection Ecology Selection of combinations of traits in an organism that trade-off between quantity E.O. Wilson & Broad MacArthur &
theory and quality of offspring. The focus on either an increased quantity of offspring at the R.H. MacArthur Wilson (1967)
expense of individual parental investment of r-strategists, or on a reduced quantity of
offspring with a corresponding increased parental investment of K-strategists, varies
widely, seemingly to promote success in particular environments
1967 Serial Cell Biology, States that eukaryotic cells evolved from a symbiotic relationship between different L. Margulis Broad Sagan (1967)
endosymbiotic Evolution types of prokaryotic cells
theory
1970s Gaia theory, Epistemology Living organisms interact with their inorganic surroundings on the Earth to form a J. Lovelock & Broad Lovelock (1972)
Gaia paradigm, synergistic and self-regulating, complex system that helps to maintain and perpetuate L. Margulis
and Gaia the conditions for life on the planet
principle
1972 Punctuated Evolution Once a species appears in the fossil record, the population will become stable, N. Eldredge & Broad Eldredge &
Biological Rules: Some Historical Changes and Limitations

equilibrium showing little evolutionary change for most of its geological history (stasis). When S.J. Gould Gould (1972)
theory significant evolutionary change occurs, the theory proposes that it is generally
restricted to rare and geologically rapid events of branching speciation called
cladogenesis
1973 Evolutionary Evolution Application of game theory to evolving populations in biology. It defines a J. Maynard Broad Maynard-
game theory framework of contests, strategies, and analytics into which Darwinian competition Smith & G. R. Smith & Price
can be modeled Price (1973)
1989 Contingency Evolution After hundreds of different phyla evolved during the Cambrian period, many of them S. J. Gould Broad Gould (1990)
theory, subsequently became extinct, leaving the relatively few phyla that exist today
wonderful life
theory
(continued)
101
102 4 When THAT Rule Almost Persists as THAT Rule

aa

bb

Fig. 4.1 Bergmann’s rule. (a) Different levels of applicability of Bergmann’s pattern in organisms
(Modified from de Mungee et al., 2021). (b) Example of Bergmann’s rule in penguin species
(Credits: Mike Weston, Hannes Grobe/AWI).
Credits: (a) Galapagos penguin. License: CC BY 2.0 https://creativecommons.org/licenses/
by/2.0, via Wikimedia Commons.https://commons.wikimedia.org/wiki/File:Gal%C3%A1pagos_
Penguin_(Spheniscus_mendiculus)_-­standing_on_rock.jpg. Emperor penguin. License: CC BY
3.0 https://creativecommons.org/licenses/by/3.0, via Wikimedia Commons. https://commons.
wikimedia.org/wiki/File:Emperor-­left_hg.jpg

In this situation, it is not surprising then that numerous exceptions began to

appear, leading to the discussion about whether the rule truly worked, whether it
was initially wrongly stated, or whether its reliable degree of scope was quite lim-
ited (Geist, 1987; Ashton et al., 2000; Olalla-Tárraga, 2011; Clauss et al., 2013). As
some authors have pointed out, to accurately assess the link between predictions and
empirical evidence for Bergmann’s rule, it is key to revisit its original postulates
(e.g., Pincheira-Donoso, 2010; Salewski & Watt, 2017). That is, to focus on its use-
fulness for predicting eco-geographics patterns specifically in certain homeotherm
vertebrates. Adopting this conservative position, therefore, implies being cautious
in extrapolating such a rule to, for example, ectothermic animals (Vinarskiĭ, 2014),
something that would be discouraged (Salewski & Watt, 2017).
4.4 Biological Rules: Some Historical Changes and Limitations 103

It has also been investigated whether Bergmann’s rule could be applied to plants
(Moles et al., 2009). This has been analyzed in Cactaceae, with articles that do not
support the rule (Drezner, 2003) and others in which observations would indicate a
concordant trend (Donati et al., 2016). However, this intention to examine the extent
to which a rule originated for certain animals applies or not to another kingdom
reflects extremely the “obsession” to make extrapolations that help to simplify the
comprehension of the immense diversity of phenotypic patterns in biology. This is
very understandable, although risky. A concrete attempt to “extend” Bergmann’s
rule was made by Hesse et al. (1937) through the “heart-weight rule.” This holds
that species inhabiting colder climates have a larger heart relative to body weight
than close phylogenetic-related species inhabiting warmer climates. This rule can
be an extension of the principles contemplated in Bergmann’s rule for a specific
organ of the body, the heart. As stated initially by Bergmann, this so-called Hessian
rule also emphasizes the existence of a close phylogenetic relationship between the
species being compared. This is an important point that, as we will exemplify later,
if not taken into account, will inevitably bring much confusion to the assessment
and scope of the rule.
The attempt to extend the scope of a rule or principle to other groups and/or situ-
ations is valid and inherent to the sciences. However, it can lead to a certain reduc-
tionism if we do not take the necessary precautions. It is well known that even today,
there are still old debates about the degree of precision and relevance of this or that
rule. Indeed, it is not uncommon to see titles heading articles such as “Rule A does
not apply to situation X” or “Evidence rejecting rule B for group Y,” etc. This is the
first point to consider regarding what we will see in the next chapter, focusing on the
exceptions. Here, an important question may arise: To what extent is the finding of
an “exception” of the rule reliable, or is it simply an artifice of our bias in trying to
forcefully apply a rule to something (e.g., taxon, context, etc.) not initially covered
by the rule? To answer this question, it is essential to know whether we are dealing
with a situation of “mixing” of statements. That is, to be clear about the original
author’s predictions of the rule and which statements were later added as extensions
or extrapolations carried out by other researchers. Therefore, the groups that do not
fit a specific rule, rather than being a real exception, may represent observations that
were never contemplated initially. This difference is essential to not “waste” the
word “exception” on something that does not apply.

4.4.1.2 Emery’s Rule

Although not reaching the same level of study and controversy as Bergmann’s rule,
another example of a biological rule that highlights the debates regarding the group
for which it was originally proposed is the Emery Rule. In 1909, the entomologist
Carlo Emery of the University of Naples observed that social parasites (i.e., klepto-
parasites) among insects tended to exert such parasitism on species or genera to
which they were phylogenetically close (Emery, 1909). Their specialization to klep-
toparasitism arises within a well-defined clade of Hymenoptera, among close
groups, and not in taxonomically distant groups. It is important to note that the
104 4 When THAT Rule Almost Persists as THAT Rule

postulation of this rule arose from studies that Emery conducted specifically on
distinct groups of ants that were closely related to each other. However, it was sub-
sequently explored by meta-analysis whether this rule was valid for other ant groups
where social parasitism was also present (Huang & Dornhaus, 2008). The original
rule did not apply to all analyzed types of social parasitism in ants.
In a recent study by Lopez-Osorio et al. (2015), it was found that phylogenetic
tests refute the applicability of this rule in explaining the evolution of social parasit-
ism in certain hymenopterans, including yellowjackets and hornets. The point is that
it was not Emery who generalized this rule. Emery explained social parasitism in a
specific group of ants without even speaking of a rule. As is often the case, it was
extrapolated and applied to other Hymenoptera and even within other completely
distant organisms, such as fungi. Thus, if we adhere exclusively to Emery’s original
idea and his precise observations, this rule should never have been enunciated, or at
least it should have been enunciated with appropriate caution and limitations.

4.4.1.3 More Rules, More Caution

Like these two preceding cases of biological rules, other rules have also been sub-
ject to criticisms related to the scope of their postulates. For example, in the field of
eco-geographical rules, J. A. Allen described in 1877 that endothermic animals
from colder places usually have shorter body appendages (limbs) compared to those
endotherms living in warmer climates. However, Allen’s rule has been criticized for
its application in some groups of endotherms and/or in some areas of the world
(Serrat et al., 2008; Alho et al., 2011). Something similar has occurred with Cope’s
rule. The rule is named after the paleontologist E. D. Cope, who contributed to evo-
lutionary theory, including the “law of the unspecialized,” which we will see in
Chap. 6 (Raia & Fortelius, 2013). Cope’s rule holds that population lineages increase
in body size over evolutionary time (Rensch, 1948). Again, this principle is invalid
for some taxonomic groups (Hone & Benton, 2005).
Many of these rules were actually described by the author after whom they were
named (e.g., Bergmann’s, Allen’s). However, others were named in honor of the
author who had provided the seminal observations, which were the foundation for
the future rule (e.g., Cope’s, Rapoport’s). Sooner or later, papers appear that falsify
the generalizations made of specific rules, circumscribing and better delimiting the
rule’s scope. Indeed, there is a growing interest in refining these rules, taking into
account factors not considered in detail. Such is the case with Hamilton’s rule
(Dillard & Westneat, 2016). This rule states that genes should increase in frequency
when the relatedness of a receptor to an actor, multiplied by the benefit to the recep-
tor, exceeds the reproductive cost to the actor (this is a prediction of the theory of
family selection formulated by W. D. Hamilton—Queller & Strassman, 2002).
These conditions are fundamental to understanding this rule. It is interesting that,
among other factors to take into account, Queller & Strassman (2002) analyze social
and genetic monogamy, and even in the former, they see this link with cooperation,
for example, in communities.
4.4 Biological Rules: Some Historical Changes and Limitations 105

On the other hand, some works have also suggested the importance of consider-
ing more than one rule in an investigation, mainly when they could be linked to each
other (Sargis et al., 2018). Such is the case of Island’s rule and the aforementioned
Bergmann’s rule. The Island rule (or “Island effect” or “Foster’s rule”—Foster,
1964) is an eco-geographical rule in evolutionary biology that states that members
of a species decrease or increase depending on the resources available in the envi-
ronment. In its statement, we see that there are common points with Bergmann’s
rule. Thus, it is necessary to evaluate multiple variables simultaneously in studies of
eco-geographical norms. Sargis et al. (2018) studied these rules simultaneously in
the common treeshrew (Tupaia glis), a group of small mammals. They observed a
strong negative effect of latitude on body size, indicating the opposite of what is
expected by Bergmann’s rule. They also observed no difference in body size
between the island and mainland populations. They found that among island popu-
lations, there was an effect of island area and maximum sea depth on body size.
While there was a strong latitudinal effect on body size, the authors note that neither
Bergmann’s rule nor the Island rule would apply, at least clearly, for this group of
small mammals.
This last example is very useful since it shows the importance of evaluating more
than one rule in combination, especially if they could be linked, and then it leads us
to the original statements of these rules. Indeed, the Island rule was extended in the
framework of the so-called Island Biogeography Theory (Case, 1978). In addition,
it was analyzed whether or not plants follow the statements of that rule (Biddick
et al., 2019). As we said previously, the latter is challenging and scientifically valu-
able. However, it involves risks at the level of interpretation since it is indirectly
“forcing” the applicability of a principle originally conceived for animals. In other
words, it is not a universal type I rule but rather a type II rule, which implies that
from its conception, it was circumscribed to specific taxa. In this context, it is neces-
sary that in publications demonstrating “nullity,” rejection, or nonapplicability of a
rule, it should be stated whether or not the taxon and/or conditions are the same
under which the rule was initially described. Making this point clear in scientific
publications and discussions is essential to avoid confusion about the scope, clarity,
and flexibility of biological rules. Otherwise, biologists themselves are “justifying”
a certain discredit that is erroneously given to specific fields of biological sciences
(mainly in diversity, ecology, and evolution) for the lack of laws, principles, and
rules of reliable application.
The proposal of modifications to enhance the understanding, clarity, and applica-
bility of these rules presents a valuable challenge for biologists. Again, it is key to
keep in mind what the original author postulated and, vitally, what researchers ulti-
mately “understand” by such a rule. In this context, Delhey’s (2019) recent review
of the Gloger rule provides an excellent example of the analysis that would be
needed for most biological rules. First, Gloger (1833) pointed out that the birds'
overall pigmentation and coloration patterns would be more intense at lower lati-
tudes, which coincides with warmer regions. The effect of humidity was also high-
lighted since desert birds are paler even if they inhabit warmer areas. That is, the
temperature–humidity combination would work together. Rensch (1929) expanded
106 4 When THAT Rule Almost Persists as THAT Rule

the scope of these ideas and framed them in what he defined as “Gloger’s rule.” He
even expressed a “simple” version of the rule, not different from that already men-
tioned by Gloger himself, and a “complex” version of it. In this complex version,
more details are given on the effect of temperature and humidity on certain types of
pigments. Precisely, the deposition of phaeo-melanins should decrease with tem-
perature, whereas only extreme cold will reduce the deposition of eu-melanin. In
addition, the eu-melanin deposition should decrease with lower humidity, whereas
phaeo-melanin deposition will increase.
Dehley’s analysis of the literature on the subject (Delhey, 2019) concludes that
Gloger’s rule in its “complex” version has unfortunately not been analyzed in detail
thus far. For the “simple version,” the rule would not be satisfied for the temperature
factor, being only consistent with the humidity factor. Therefore, he stresses the
need to reformulate the rule, focusing only on humidity. However, he points out that
more studies are needed and that to avoid biases in the work, it should always be
clear which definition is being used and cite the appropriate references. He mainly
suggests Rensch (1929) and not Gloger (1833) since the latter was not who actually
coined the rule. In addition, he points out that because the original papers were writ-
ten in German, later translations into English may have contributed to some confu-
sion surrounding the rule. He concludes that a complete re-evaluation of Gloger’s
rule should identify and test mechanistic links between coloration and climate. For
example, the likely mechanisms that would lead to greater melanin deposition in
more humid-leafier-regions would be camouflage and protection against parasites
and pathogens. This case exemplifies the changes and misinterpretations of a rule
according to its original postulates and the importance of clarifying these changes
and citing them correctly.
Finally, another relevant aspect is the theoretical basis underlying the formula-
tion of biological rules. The formulation of rules explicitly—or even implicitly—
has been based mainly on empirical methods, i.e., on the observation of facts and
experimentation. Such is the case of the accumulation of information from com-
parative observational studies for eco-geographical rules, as well as experimental
studies in others, such as those linked to genetics (e.g., Hamilton’s rule). However,
the theoretical bases may not have been strong in all cases. A pending is, therefore,
to advance theoretical modeling to see the extent to which this or that rule is
explained and supported. In particular, this is important when adding factors such as
taxonomic group, region, age, and kinship index according to the type of rule being
analyzed. In this context, we can highlight the study of Jørgensen (2002), who ana-
lyzes cases in ecology that demonstrate that it is possible to give theoretical expla-
nations from the ecosystem: (1) the lower the mortality of mammals, the later the
offspring are weaned; (2) lower mortality implies later first parturition with lower
risk; and (3) exploitation competition can be explained by a slight advantage in the
growth rate relative to mortality rate; (4) It is a good strategy for ectoparasites to
have relatively high mortality in early stages. In addition, the optimal founder den-
sity is higher for relatively high mortality at an early stage. All these “rules,” as
stated by the author, would thus be supported by ecosystem theory, not only by
empirical data.
4.5 Key Concepts and Ideas in this Chapter 107

On the other hand, as part of the “search for rules,” there is still debate about how
many species can coexist in a community. When the number of species reaches a
certain threshold, the community may saturate. It is critical to be clear whether this
occurs in all communities since, in the current times, with the influence and chal-
lenges of global climate change, biodiversity conservation studies and policies
should be based on precise predictions. Recent studies indicate that many communi-
ties could be “unsaturated,” i.e., not having a maximum of coexisting species. In this
regard, Mateo et al. (2017) reconsider the problem to clarify the “rules” on this
issue. They emphasize that perhaps a partial view prevails regarding the saturation
of communities. They propose that biodiversity models could adequately address
this problem by considering an existing “duality”: it would be better to consider
communities as unsaturated, but where species composition is influenced and con-
ditioned by different drivers and scale-dependent biodiversity factors.
In conclusion, if we consider all the examples mentioned above of biological
rules (whether consolidated, questioned, or in development), it will be good to con-
tinue advancing in comprehensive approaches that combine the empirical approach
and theoretical modeling in their respective disciplines. Otherwise, as mentioned
above, we biologists are proposing rules with imprecision or refuting them by a
mere accumulation of observations without giving attention to the original state-
ments of the rules. The challenge will be to contribute to the knowledge of the
principles without neglecting biological diversity, which, ironically, may cause
some confusion when the principles of the rules are extrapolated and generalized to
nonrelated organisms and only from empirical data.

4.5 Key Concepts and Ideas in this Chapter

• In evolutionary biology, it is common for theories to be eventually renewed,

enriched, and adapted by incorporating new information from advances in related
disciplines, and thus, new versions of the original theory emerge.
• Darwin’s theory of natural selection has undergone modifications during the
twentieth and twenty-first centuries from new disciplines, which have helped to
refine Darwin’s strict vision and reinforce the central postulates initially
enunciated.
• Molecular genetics, epigenetics, and phenotypic plasticity generated new per-
spectives to improve the integration of developmental biology with evolution.
• Progressively, the concepts of evolutionary developmental biology (Evo-Devo)
and ecological evolutionary developmental biology (Eco-Evo-Devo) emerged,
constituting a new paradigm in terms of the vision of evolution.
• A controversial topic refers to the concept of species because there is a diversity
of definitions, approaches, and perspectives to define it. This means that there is
no single rule in this case, and each discipline will relativize it according to the
scope of the study.
108 4 When THAT Rule Almost Persists as THAT Rule

• Many times, some rules have been extrapolated to other groups of organisms for
which they were not initially conceived by their authors. This has led people to
think that they have been poorly thought out; when in fact, the problem arises
when this extrapolation forces their application.
• The rules should be based not only on data obtained from experiments but also
on theoretical contributions from different disciplines.

References

Abouheif, E., Favé, M. J., Ibarrarán-Viniegra, A. S., Lesoway, M. P., Rafiqi, A. M., & Rajakumar,
R. (2014). Eco-Evo-Devo: The time has come. In C. Landry & N. Aubin-Horth (Eds.),
Ecological genomics. Advances in experimental medicine and biology. Springer. pp. 781.
Alho, J. S., Herczeg, G., Laugen, A. T., Räsänen, K., Laurila, A., & Merilä, J. (2011). Allen’s rule
revisited: Quantitative genetics of extremity length in the common frog along a latitudinal
gradient. Journal of Evolutionary Biology, 24, 59–70.
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Chapter 5
When THAT Exception Persists Almost
as THAT Exception

Rarely do we realize that we are surrounded by the

extraordinary
—Paulo Coelho

Contents
5.1 Introduction    117
5.2 T eratologies: Aberrations Revalorized    120
5.2.1 Defining Teratologies, Subjectivities, and the Relationship Between
Concepts    120
5.2.2 Utility of Teratologies in Evolution    121
5.2.3 Factors That Can Generate Teratological Traits    123
5.2.4 Invertebrate Teratologies    125
5.2.4.1 Reflections from the Discovery of Teratological Scorpions    128
5.2.5 Some Examples of Teratologies in Plants    129
5.2.5.1 Desired Malformations in Plants    129
5.2.5.2 Harmful Teratologies Could Bring Ecological Benefits    131
5.2.5.3 Teratologies That Inspired Theories of Plant Physiology    132
5.3 Treasure Your Exceptions    132
5.3.1 Temptation to Generalize When Encountering an Interesting Exception    133
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies    134
5.4.1 Exceptional Animal and Plant Groups    135
5.4.1.1 A Protozoan That Does Not Appear to Be One    135
5.4.1.2 Tardigrades: The Most Resilient Organisms?    136
5.4.1.3 Sponges Breaking Several Rules    139
5.4.1.4 Some “Worms” as Models of Exceptions    142
Using Foreign Weaponry: Flatworms and Nematocysts    143
“Photosynthetic” Worms    144
Atypical Parasites: Separate Sexes in a Hermaphroditic World    145
5.4.1.5 Contributions from a Rare Crustacean    147
5.4.1.6 Cephalopods: The Most Intelligent Invertebrates?    148
5.4.1.7 Exceptional Fungi    149
Challenges When Classifying Fungi    149
Amoeboid Fungi    150
Glowing Fungi    153
An Unusual Distribution    154
The Oregon Monster    154

© Springer Nature Switzerland AG 2024 115

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_5
116 5 When THAT Exception Persists Almost as THAT Exception

5.4.1.8
 arnivore Plants: Exceptions in the Group Show Us
C
the Carnivore Rule    155
Murderous Plants Strange as Fiction    156
A Molecular Recipe Behind the Evolution of Carnivory    156
Vegetarian Carnivorous Plants    158
5.4.2 Extraordinary Phenomena    159
5.4.2.1 Exceptions from the World of Deception    159
Beetles That Mimic Ants    159
Cephalopods as Masters of Camouflage    167
Mushrooms That Look Like Berries    167
Defensive Masquerade in Plants    167
5.4.2.2 Strange Forms of Pollination    168
Pollinators Not as Ridiculous as Previously Assumed    169
Underwater Pollination    169
Intermediary Pollinators of “Armed” Plants    170
5.4.2.3 Reproductive Biology: Source of Valuable “Exceptions” at
the Evolutionary Level    172
Minorities That Remain: Alternative and Conditional Sexual
Strategies    172
Animal Homosexuality    175
On Female Andromorph Dragonflies    177
Fluid Sex in Fish    178
Speculating Behavior from Morphological Observations    179
5.4.3 Evolutionary and Ecological Exceptions    180
5.4.3.1 Evolutionary Simplification    180
How To Be a Good Parasite?    180
On De-evolution and When the Simple Deceives Us    181
5.4.3.2 Exceptions at First Sight    183
“Nonanimal” Eyes    183
Cave Dwellers: Blind Fish    183
The Whites of Your Eyes Are More Unique Than You Think    185
5.4.3.3 Value of “Rare” Species in Ecosystems    186
Ecosystem Services of Rare Species    188
Rare Species Loss Affects Functional Assemblages in Tropics    189
The Rare Biosphere    190
5.5 Key Concepts and Ideas in This Chapter    191
References    192

Abstract We present the counterpart to Chap. 4 in Chap. 5, where we focus on the

role of “permanent” exceptions and their importance in scientific knowledge and
biology. These exceptions can be analyzed at any scale and are often not appreciated
beyond anecdotal mentions. They can be aberrant or teratological groups, taxo-
nomic groups unique for some features of their biology, “intermediate exceptions”
with minorities of species or clades with certain characteristics compared to the
majority, or organisms with exceptional distributions in space or time. In this chap-
ter, we reviewed groups that have been difficult to classify because of their rarity,
rarities that can be used for human benefit, exceptional groups that make us rethink
phylogenetic relationships, rare and incredible biological phenomena, and evolu-
tionary and ecological aspects of rare species. Our goal is to vindicate rarities and
minorities, to highlight their importance for the understanding of evolution, and to
begin to make these cases visible and treasured in the teaching of biology.
5.1 Introduction 117

5.1 Introduction

As we saw in Chap. 2, when thinking about situations or organisms characterized as

“permanent” exceptions (i.e., they have always been exceptions and are expected to
remain as such), we probably first think immediately of outstanding individuals
with extreme “positive” traits from an adaptive perspective. However, there are also
“negative” extremes, and we find the norm or the majority between these positive
and negative extremes. Indeed, there is a trend in biological sciences to use the so-­
called morphological “aberrations” to illustrate the extreme concept of exceptions.
Occasionally, certain groups accumulate multiple “rarities” or exceptional features,
and we said there are exceptional or “aberrant” among their group. The word “aber-
rant” may be more common than we think in the scientific literature or scientific
communication. Our emotional perception may influence us to use the word “aber-
rant” subjectively. This word refers to something “deviating from the normal or
usual type, someone behaving in an abnormal or untypical way, or something devi-
ating from truth, morality, etc.” (Collins English Dictionary, 2003). Thus, although
it is used more for human acts, the definition is connected to that of “exception,”
since it deviates from the regular pattern. If it is aberrant, it is because it presents a
particular trait or “aberration.” In biology, this word is the “deviation from the nor-
mal type of a morphological or physiological character.” Complementarily, in biol-
ogy, we refer to something aberrant to an organism that presents one or more
differences concerning those presented by the species to which it belongs.
We can also find aberrant organisms that show a mixture of several characters or
a maximum reduction of the ancestral form. This includes groups that are usually
rare in number, living fossils, or parasitic species (Wisnivesky, 2003). Viruses, for
example, were considered “aberrant” forms of bacteria at the time M. W. Beijerinck
began to study them (Jenkins, 2003), considering that there could be no smaller
organisms. The term “aberrant” is also commonly used among paleontologists to
highlight discoveries of strange fossils. For example, the case of the aquatic reptile
Sclerocormus supported the idea of a rapid evolutionary divergence that occurred in
many groups after the great Permian extinction (Jiang et al., 2016).
Charles Darwin (1859) refers to aberrant species when he mentions that “as a
small number of the old and intermediate forms have transmitted to the present day
very little modified offspring, these constitute the so-called aberrant or osculating
species.” He adds that this perception of aberration is intensified as more related
species become extinct. This makes them even more striking, unique, true excep-
tions among the larger clades that encompass them. He also says, “...they are almost
always represented by very few species, and these generally differ greatly from each
other: which also implies extinctions” and “...leaving a small number of representa-
tives which are still preserved under extraordinarily favorable conditions.” He gives
examples of aberrant species such as the platypus (Ornithorhynchus anatinus) and
the South American lungfish (Lepidosiren paradoxa). He points out that even if spe-
cies more closely related to them were still alive, they would still be aberrant. The
reference to the small number of representatives is added to the rarity of the mor-
phology, making a “cocktail” that attracted his attention.
118 5 When THAT Exception Persists Almost as THAT Exception

These Darwinian concepts have not become obsolete in the lexicon of many
authors in biology. One example is the phylum Gnathostomulida, mentioned as a
small group of “aberrant” organisms in some invertebrate zoology textbooks
(Marshall & Williams, 1985). These animals are tiny, vermiform-bodied, and live
among particles on the seafloor, particularly in anaerobic environments, where they
feed on fungi and microorganisms. Their evolutionary and systematic history is still
not entirely clear, and they present a mix of features that a priori resemble groups of
now obsolete categories, such as the “acoelomates,” but at the same time present
features of “pseudocoelomates” (Ruppert et al., 2003). Indeed, they were initially
considered an “aberrant” group of turbellarians within the flatworms, and only in
1969 were they considered a separate phylum (Sterrer et al., 1985). Currently, they
are included in the clade Gnathifera, grouping them together with rotifers, among
others (Marlétaz et al., 2019; Giribet & Edgecombe, 2020).
Similar is the case with the so-called “sea spiders” of the class Pycnogonida.
Pycnogonids are often said to possess “aberrant” characteristics compared to other
representatives of the Subphylum Chelicerata (Ruppert & Barnes, 1994), a group
they share with the horseshoe crabs (class Merostomata), and the arachnids (class
Arachnida). These unique features include an articulated “thorax” instead of the
typical prosoma and opisthosoma found in other chelicerates, well-developed ovig-
erous (egg-carrying) legs, particularly in males, and various additional traits that
justify the use of the term “aberrant.” Similar situations of use of this term are often
repeated in any animal group. For example, in birds, certain anomalies in color,
design, and development of flight feathers, rectrices, and remiges are considered
“aberrant” (Sáez-Royuela et al., 1975). Additionally, some fish, such as abyssal fish,
with large teeth and lures, even soles with both eyes on the same side of the body,
can be labeled “aberrant.”
Interestingly, the perception of aberration may be greater as we move up the
zoological scale, and we are further impacted by this “departure from the common.”
Table 5.1 shows examples of various taxa in terms of so-called “aberrant” groups,
highlighting the traits that make these groups extraordinary. We must acknowledge
and consider emotional subjectivity and anthropocentric prejudices, which are gen-
erally unintentional in using the term “aberration.” Here, we prefer the use of excep-
tion or rarity in many of these cases, but we do not deny the term “aberration” for
some cases, as it is something we can still find in biological descriptions. What is
clear is that exceptions or aberrations can occur in different taxonomic groups in
different spatial and temporal contexts, ranging from morphological curiosities at
phenotypic extremes to unique teratological cases.
5.1 Introduction 119

Table 5.1 Examples of species considered aberrant in biology highlighting the aberrant traits
Species Trait that makes it aberrant Reference
Vertebrate animals
Axolotl Ambystoma Able to regenerate limbs and Monaghan et al. (2007);
mexicanum internal organs Satoh et al. (2008);
Voss et al. (2009)
Platypus Ornithorhynchus Mammal that lays eggs, Whittington et al.
anatinus venomous, with a duck-billed (2008)
snout and a beaver tail
Common Desmodus Bats that feed on the blood of Greenhall (1972)
vampire bat rotundus other animals
Naked Heterocephalus Hairless rodent Tucker (1981); Daly &
mole-rat glaber Buffenstein (1998)
Northern Channa argus Fish can breathe air and move Ishimatsu &
snakehead on land to reach other bodies of Itazawa (1981, 1983)
water
Four-eyed Anableps sp. Fish with eyes divided into two Borwein & Hollenberg
fishes sections, allowing them to see (1973); Sivak (1976);
above and below the water Zahl & Gomprecht
(1977)
Invertebrate animals
Vinegar fly Drosophila Flies in mating groups of males Niida & Koshikawa
guttifera beat each other with their wings (2021)
until some of them become
unconscious
Green ormer Haliotis Mollusk that can regenerate the Fleury et al. (2008)
tuberculata shell
Immortal Turritopsis Jellyfish can reverse their life Lisenkova et al. (2017);
jellyfish dohrnii cycle and return to their juvenile Martell et al. (2016)
stage
Ground beetle Brachinus sp. Beetle that produces a chemical Lai (2010); McManus
reaction to defend itself from et al. (2018); Attygalle
predators et al. (2020)
Plants
Corpse flower Rafflesia arnoldii It produces the largest flower in Nikolov & Davis (2017)
the world but without leaves or
roots, it obtains nutrients by
parasitizing other plants
Venus flytrap Dionaea Carnivorous plants that feed on Poppinga & Joyeux
muscipula insects and other small animals (2011); Pavlovič et al.
(2017)
Bacteria
Extremophile Deinococcus Resists high radiation doses Daly (2009); Krisko &
Bacteria radiodurans Radman (2013)
120 5 When THAT Exception Persists Almost as THAT Exception

5.2 Teratologies: Aberrations Revalorized

5.2.1 Defining Teratologies, Subjectivities,

and the Relationship Between Concepts

Teratology is a scientific discipline that studies abnormal morpho-physiological

developments in various taxa, employing terms such as “individuals of a species that
do not respond to the common pattern” (Dicke, 1989). Other definitions of teratol-
ogy are more emphatic, such as “the scientific study of congenital abnormalities and
abnormal formations” (Oxford English Dictionary, 2017). Etymologically, it is
derived from the French word tératologie, and this term in turn comes from the
Greek τέρας, -ατος (téras, -atos), which is the genitive form of “téras,” which refers
to something extraordinary, monstrous, or prodigious, often denoting something that
surpasses the boundaries of the natural. On the other hand, λογία “logos” signifies
study, treatise, reason, or discourse. Consequently, cf. gr. τερατολογία “teratology”
can be translated literally as the study or treatise of congenital malformations, defor-
mities, or dysfunctions in living beings (Treviño-Rodriguez, 2023). Additionally,
etymologically, the word teratological implies a dichotomy between something
monstrous and prodigious, referring to a phenomenon that can cause fascination
and/or terror. Another definition for teratology is “a collection of tales about mythi-
cal or fantastic creatures and monsters” (Collins English Dictionary, 2003). The
term “monster” is undoubtedly striking and begs the question, what is a monstros-
ity? Definitions range from “something very ugly and usually large” (Cambridge
Advanced Learner’s Dictionary, 2023) to “a person or animal that is markedly
unusual or deformed” (The American Heritage Roget's Thesaurus). As the reader
will see, again, the emphasis is on something, someone, which departs from what is
considered “regular,” i.e., the pattern, the norm. The first definition is interesting
because it includes a physical characteristic such as size and an attribution linked to
our human perception of what is considered “ugly” as opposed to what is “beautiful”
to our senses. This is linked to artistic representations and the valuation of beauty
across different temporal and sociocultural contexts, which we will see in Chap. 8.
If we return to the meaning of teratology, we see that the intrinsic components
that give it entity (e.g., monstrosity) or its antonyms (beauty versus ugliness) are
based mainly on human perception. Something that pleases or does not please our
senses, a sensory and emotional experience, similar to when we analyze the term
“aberration.” This suggestive bias does not detract from the value of this discipline,
and it is important to bear in mind that it arose to highlight in some way biological
abnormalities or aberrations that would otherwise be ignored, hidden, or denied.
Nevertheless, it is crucial to acknowledge that science, or certain scientific fields,
can be influenced by subjective human perspectives and biases. Ultimately, nothing
we describe nature is without a human bias, given our sensory universe and its
limitations.
One of the complementary meanings of teratology is the “relation of prodigies.”
This is interesting as the term “prodigy” (from the Latin prodigium) has an intrinsic
5.2 Teratologies: Aberrations Revalorized 121

duality, which ultimately confers a certain neutrality to the term, highlighting an

oddity regardless of whether it is categorized as positive or negative. A prodigy
could be considered “an amazing or unusual thing, especially one out of the ordi-
nary course of nature” (Oxford English Dictionary, 2017). The complementary
definitions of prodigy, such as “an outstanding example of a particular quality” or
“a young person with exceptional qualities or abilities” (Oxford English Dictionary,
2017), are more subjective. In these cases, it is evident that the term prodigy is
framed in positive attributions from a human perspective to refer to something or
someone exceptional. Finally, a prodigy can be defined as a “miracle, an event of
divine origin,” which, in addition to being at the opposite pole to “monstrosity,”
appeals to a supernatural sense.

5.2.2 Utility of Teratologies in Evolution

“Monsters” or teratological forms have classically been viewed as nonfunctional

entities, evolutionary dead ends not worthy of study. However, the recognition of
“monsters” in studies such as Evo-Devo arises from the research for “logics” or
“rules” to explain morphological development (Alberch, 1989; Reiss et al., 2008).
Back in the 1700s, and after the contributions of some scientists based on studies
with teratological humans (like the studies of two French anatomists, Jean Méry and
Alexis Littré), the French Academy of Sciences proclaimed: “Monsters are usually
regarded as games of nature. But the philosophers are very much convinced that
nature does not play, that she always follows the same rules and that all her works
are, so to speak, equally serious. There can be extraordinary things but not irregu-
larities. Furthermore, it happens very often that these very extraordinary things pro-
vide the path to discover the general rules in which they all are included” (Histoire
et Memoires de l’Academie Royale Des. Sciences, 1703 [1720]: 28.; Moscoso,
1998). This strategy of using teratologies to understand development goes back a
long way (Paré, 1573; Aldrovandi, 1642), and since then, contributions to the field
have been somewhat irregular, as the perspectives on which studies have focused.
Modern versions include these “monsters” in fields such as evolutionary teratology
or evolutionary developmental pathology (Evo-Devo-Path) (Moscoso, 1998;
Blumberg, 2009; Nestawal, 2014; Guinard, 2015; Diogo et al., 2017; Diogo, 2020).
Why do some monster forms, despite being nonadaptive, appear repeatedly?
Perhaps internal variations and rules of form–function relationships in develop-
ment could answer this question. Teratologies can be generated in an organized
or nonchaotic way, with certain forms being more likely than others (Alberch,
1980). This characteristic makes the description and classification of these mor-
phological variants possible (Saint-Hilaire, 1836; Alberch, 1989). For example,
two-headed monsters are relatively common in many vertebrate groups (Stockard,
1921; Saint-Hilaire, 1836), while three-headed monsters are extremely rare in
nature. In turn, certain teratologies are more common in certain species than oth-
ers (Stockard, 1921; Bulmer, 1970; Stephens & Shepard, 1983). In contrast, the
122 5 When THAT Exception Persists Almost as THAT Exception

recurrence of teratologies in different species suggests that the ontogenetic path-

ways that produce these morphologies may be maintained throughout the phylog-
eny (Alberch, 1989).
Indeed, Blumberg (2009), in his book “Freaks of nature,” highlights multiple
examples of the connections between teratology, developmental biology, and evolu-
tion. For example, from a biomedical perspective, it can be very useful to explain
patterns of teratology by failures in physiological or developmental processes. This
allows us, through the presence of specific malformations, to better understand cer-
tain physiological processes that fail (whether due to genetic and/or environmental
factors) and to understand more clearly how these physiological processes function
under normal conditions (e.g., in a healthy individual). Interestingly, both Alberch
and Blumberg emphasize the role of “internal machinery” in determining form as a
counterbalance to a pure adaptationist view with natural selection as an omnipotent
external force. Stephen Jay Gould and Richard Lewontin had called for an apprecia-
tion of “organisms as integrated wholes, fundamentally not decomposable into
independent and separately optimized parts,” also criticizing extreme adaptation-
ism (Gould, 1977; Gould & Lewontin, 1979).
Different interpretations of morphological variability from diverse disciplines
can be mixed, and the tools and explanations provided by each discipline are equally
rich and valid. By conceptualizing potential morphological variations as a morpho-
space, we can identify unoccupied or sparsely represented regions as spaces associ-
ated with morphologies that may indicate lower fitness (Olson, 2012). This could be
explained by the elimination of these morphologies by natural selection or by con-
straints inherent to development (“constraints,” “scaling laws”) (West & Brown,
2005). Olson (2012) suggests thinking about teratology in a framework of the pos-
sible and the impossible; they may be abnormal but possible morphologies and
forms that are imaginable but unobserved. This means that to study whether specific
data support biological “laws” or rules, the study of teratologies is fundamental.
Uncommon variants give evolutionary biologists valuable information about what
can and cannot develop ontogenetically (Reiss et al., 2008; Blumberg, 2009; Olson,
2012) and what certain morphological features would look like if they were evolu-
tionarily selected. The empty spaces represent a wide range of morphological pos-
sibilities (Blumberg, 2009). The variations that occur naturally in species are the
necessary substratum where selection acts. The “normal” to the “aberrant” are part
of this continuum, and knowing this gradient is key to understanding evolutionary
morphological trajectories.
Different approaches can study and explain empty spaces, but a developmental
approach is necessary to understand the adaptive landscape of these morphological
variants (Klingenberg, 2010; Olson, 2012). An embryological approach studies spe-
cies’ possible and not possible developmental pathways and their evolutionary
implications (Alberch, 1989; Reiss et al., 2008; Blumberg, 2009). However, experi-
mental manipulations can be performed to reach these empty spaces in morpho-
space (Sinervo & Litch, 1991; Conner et al., 2011). Finally, comparative studies
allow the morphospace to be “filled” by characters from different species to analyze
discontinuities and differences in their occupancy (Alberch, 1989; Polly, 2008;
5.2 Teratologies: Aberrations Revalorized 123

aa b

Fig. 5.1 Explanations for the empty space found in morphospaces. (a) Diagram illustrating an
empirical pattern of a scaling relationship, on the upper diagonal, empty space would be ontoge-
netically impossible following a developmental constraint explanation. On the lower diagonal, the
morphospace would be ontogenetically possible, though constrained by selection (gray dots), fol-
lowing an adaptationist explanation so the empirical pattern would represent the highest possible
fitness. (b) Study of bone size scaling patterns in terrestrial mammals from a comparative (com-
parison with bats and cetaceans) and embryological–teratological approach by examining bone
teratologies (Modified from Olson, 2012; Swartz & Middleton, 2007)

Minelli, 2009). An example is the study of limb bone proportions of terrestrial

mammals, where the authors tested whether morphological relationships outside the
allometric scaling line in the empty space of the morphospace were ontogenetically
impossible or the result of selective processes (Swartz & Middleton, 2007)
(Fig 5.1a). By comparison with nonterrestrial mammals, relationships outside the
allometric scaling line were found to be ontogenetically accessible, and by an
embryological-teratological study, bone disorders in bone size ratios and size–den-
sity relationships were found to occupy other empty spaces of the morphospace
(Fig. 5.1b). Thus, by combining different approaches, it was possible to conclude
that these relationships were not ontogenetic “constraints” but adaptive outcomes to
life on land in mammals (Swartz & Middleton, 2007; Olson, 2012).

5.2.3 Factors That Can Generate Teratological Traits

As discussed earlier, teratologies can be categorized to identify a “teratological pat-

tern,” which involves investigating the underlying causes of specific teratological
traits. This pursuit has been ongoing since the era of T. H. Morgan’s classical genet-
ics and subsequent studies exploring the physicochemical factors capable of induc-
ing abnormalities, both genetic and phenotypic, in animal models such as Drosophila
(Bianchini et al., 2018; Li & Bi, 2018; Mishra & Barik, 2018) and amphibians
(Pownall & Saha, 2018). Over time, an increasing number of teratogenic elements
124 5 When THAT Exception Persists Almost as THAT Exception

have been identified. Teratogenic elements are defined as chemical compounds that
can lead to developmental abnormalities in offspring if consumed during prenatal
stages (Barik & Mishra, 2019). This field is becoming increasingly important
because it can be extrapolated to possible effects on humans. For example, Barik &
Mishra (2019) have recently reviewed the potential as teratogens of nanoparticles
(thus in vogue promoting their use in cutting-edge biomedicine), as they have been
found to cause defects at the behavioral, developmental, phenotypic, and genetic
levels in Drosophila.
As we observed in animals, teratologies in plants and fungi can also be indicators
of specific environmental variables such as lack of illumination (Michael et al., 1983)
or the presence of harmful compounds that function as teratogens and produce indi-
viduals who deviate from the “normal” in diverse ways (Masters, 1869; Goebel,
1896; Bos, 1957). Studies on abnormal fungal fruiting bodies that develop in response
to infection by other fungi or exposure to toxins have been very useful in analyzing
the processes responsible for the appearance of the symmetrical form in fungi and for
understanding their extreme sensitivity to environmental stress. An example is a phe-
nomenon known as “rosecomb,” which occurs in cultured fungi due to exposure to
diesel vapor, kerosene, creosote, Lysol, and other petroleum-­ derived chemicals
(Phillips, 1881; Lambert, 1930). Some of these exogenous chemical agents are asso-
ciated with genetic instability, producing malformations and distortions in fruiting
bodies (Umar & Van Griensven, 1999; Kearney & Kearney, 2009, 2011). The
response of fungi is progressive depending on the severity and duration of exposure
to teratogenic compounds (Flegg, 1983), and morphogenic changes begin to occur in
the middle of fruiting structure development (Kearney & Kearney, 2009).
The study of teratogenic factors can also help examine the possible effect of
some pollutants and climatic disturbances on the evolutionary history of organisms.
For example, Munnecke et al. (2012) examined the occurrence of teratologies in a
group of organisms, the acritarchs. These organisms are a collection of organic-­
walled microfossils characterized by their diverse shapes and sizes. They are con-
sidered an informal and polyphyletic group, meaning they consist of organisms
from multiple evolutionary lineages with unknown biological affiliations (Servais
et al., 2004). Munnecke and collaborators studied this group on a particular evolu-
tionary time subject to major environmental perturbations: the late Ordovician–
Silurian interval. This period was characterized by pronounced negative isotope
excursions (of carbon δ13C and oxygen δ18O) measured in marine and terrestrial
substrates that indicate large-scale changes in the global carbon cycle and mass
extinction events (Calner, 2008). The preceding stages of some of these excursions
are marked by the high abundance of malformed acritarchs in various parts of the
world (Delabroye et al., 2012). Although the mechanisms directly involved in the
occurrence of teratologies in these organisms are still unknown, isotope excursions,
as well as contamination by heavy metals, changes in temperature, salinity, and sea
level may have been key factors involved in the teratogenesis of acritarchs
(Munnecke et al., 2012).
A similar example occurs in the fossil palynological record that can provide
clues to past climatic disturbances (Visscher et al., 2004; Foster & Afonin, 2005;
5.2 Teratologies: Aberrations Revalorized 125

van de Schootbrugge & Wignall, 2016; Lindström et al., 2019; Gravendyck et al.,
2020; Marshall et al., 2020). The process of pollen production is known as micro-
sporogenesis and is one of the most vulnerable processes to environmental stress in
the life cycle of seed plants (De Storme & Geelen, 2014). Deviations in microspo-
rogenesis can influence the shape and size of pollen and spores (collectively termed
palynomorphs), and due to the resistance of palynomorph walls to decomposition,
these teratologies could appear in the fossil record. Therefore, morphological tera-
tologies of palynomorphs are unique indicators of paleoenvironmental stress for
terrestrial ecosystems (Benca et al., 2022). Aberrant spores and pollen grains were
found in the fossil record from the Permian–Triassic and Triassic–Jurassic boundar-
ies. Possible drivers of the malformations may have been geographic and temporal
proximity to volcanic eruptions (Broadley et al., 2018; Lindström et al., 2019; Chu
et al., 2021), ozone depletion, or elevated UV-B exposure (Visscher et al., 2004;
Benca et al., 2022). The study of these fossil teratologies provides new insights into
the different responses of the plant kingdom to ecological crises (Gravendyck
et al., 2020).

5.2.4 Invertebrate Teratologies

There are reports of teratologies and deformities in vertebrates (Hendrickx & Binkerd,
1990; Kalter, 2003; Garcês et al., 2020), a notorious case being Janus, the longest-
lived (25 years) two-headed turtle in the Geneva Natural History Museum. This turtle
also has two hearts, two lungs, and a digestive tract, with the right head controlling
the right legs and the left head the legs on the corresponding side. His keepers claim
that Janus has two personalities and tastes and that they occasionally conflict with
each other, for example, when walking (Farge & Mantovani, 2022). Beyond this
lovely case, many reports of teratologies have occurred in invertebrates collected in
the wild (Spanó et al., 2003; Asiain & Márquez, 2009; Eeva & Penttinen, 2009;
Lesniewska et al., 2009; Ferrer et al., 2014; Chitimia-Dobler et al., 2017; Mitchell
et al., 2020). In this group, mutants were crucial in discovering the role of homeotic
genes in shaping the anteroposterior axis and conferring segments and appendages
their specific identities (Rosenberg et al., 2009; Wanninger, 2015). In general, the
systematics are good at detecting these morphological “aberrations” when analyzing
characters for taxonomic descriptions. For example, in Coleoptera, multiple reports
of abnormalities were reported, recurrently, some titled “A remarkable teratological
specimen of....” Such is the case of a chrysomelid Coleoptera that, instead of a palpus,
has an antenna (Clark & Belo Neto, 2010), a scarabaeid with an unusual malforma-
tion of the eyes (Gasca-Álvarez et al., 2018), and another of the same family with a
deformation of the right elytra (Barria et al., 2020). These are typical examples of
reports in which the teratological case is presented along with a brief analysis but is
not intended to connect to causes, processes, or evolutionary implications.
In annelids, the bifurcation of the anteroposterior axis is common, i.e., worms
with two or more heads and/or tails (Andrews, 1892; Dualan & Williams, 2011).
126 5 When THAT Exception Persists Almost as THAT Exception

These bifurcations can be classified into different types according to anatomy (lat-
eral, dorsoventral) or developmental origin (embryonic, postembryonic).
Postembryonic bifurcations may occur during growth, regeneration, and reproduc-
tion. Lateral bifurcation can result in well-integrated phenotypes in adults, whereas
dorsoventral bifurcation does not since it requires discontinuity of at least some
internal organs (Andrews, 1894; Ponz-Segrelles et al., 2022). This phenomenon is
especially notable in the Syllidae family (Polychaeta), specifically within the
“Ribbon Clade.” These organisms reproduce through stolon formation, which can
exhibit abnormal patterns such as collateral stolon emergence (where new stolons
cluster tightly together in a ventral to posterior arrangement) and successive gem-
mation (involving a dorsoventral bifurcation where each segment gives rise to only
one stolon, following a posterior to anterior developmental gradient) (Johnson,
1902; Okada, 1937; Nogueira & Fukuda, 2008; Alvarez-Campos et al., 2013).
Developmental anomalies in annelids emerge as a model that should be incorpo-
rated into the growing field of Evo-Devo and examined with modern techniques and
perspectives (Ponz-Segrelles et al., 2022).
When delving into the underlying causes of these teratologies, it becomes evi-
dent that various factors, particularly during embryogenesis, can contribute to their
development. Numerous studies with an experimental approach in arachnids have
successfully identified the causative factors behind these morphological disorders
(Buczek, 2000; Napiórkowska & Templin, 2017; Buczek et al., 2019). Among these
factors, thermal shocks during embryogenesis have been found to play a significant
role in generating different types of teratology, including oligomely (absence of one
or more appendages), schistomely (bifurcation of appendages), heterosymely
(fusion of adjacent appendages), symely (fusion of appendages from the same pair),
and bicephaly (Jacunski et al. 2002; Jacunski & Templin, 1992, 2003; Napiórkowska
& Templin, 2013, 2017, 2018) (Fig. 5.2a). The giant house spider Eratigena atrica
is a great model used for experimental teratogenesis studies. In this species, defor-
mities also include changes in the central nervous system, such as ganglion fusion
(Jacunski et al., 2005; Napiórkowska & Templin 2017). Studying these teratological
cases is extremely important, as they could teach us how certain environmental
conditions affect arthropod development (Balazuc, 1948; Burke et al., 2018). This
may also allow us to predict morphological changes and phenotypic consequences
of the use of certain chemicals or temperature increases (e.g., linked to climate
change) in the embryology of certain animal groups.
It is interesting, for example, that in spiders, there are body portions more prone
to suffer teratologies, such as walking legs and ocular structures (Jiménez & Llinas,
2002; Napiórkowska et al., 2007; Gonzalez-Moliné, 2008; Mitchell et al., 2020). In
contrast, in other structures, such as chelicerae, pedipalps, and genital structures, it
is less common to find deformations (although see Muma, 1943; Kaston, 1962,
1963; Izquierdo, 2021; Nadolny et al., 2022) (Fig. 5.2b). Aberrant copulatory organs
are usually more closely linked to cytogenetic (aberrant karyotypes) and genetic
5.2 Teratologies: Aberrations Revalorized 127

b c

Fig. 5.2 Teratologies in spiders. (a) Ventral view of Eratigena atrica juveniles showing therato-
genic changes after thermal shocks during embryogenesis (from Napiórkowska et al., 2017. (b)
Ventral view of the opisthosoma of Almafuerte peripampasica (Image courtesy of Matías
Izquierdo). (c) Teratological chelicerae of Tetragnatha versicolor (Image courtesy of Darko
Cotoras). Black arroSws indicate teratological traits
(a) Eratigena atrica juveniles. License: Public Domain. (b) Almafuerte peripampasica teratology.
License: Author permission. (c) Tetragnatha versicolor teratology. License: Author permission.

(aberrant patterns of gene expression in the subadult instar) disorders. This may
result in “abnormal” gynandromorphic individuals or intersex cases (Roberts &
Parker, 1973).
A noteworthy case was recently reported, where teratology was described in the
long-jawed orb weaver Tetragnatha versicolor that possessed a duplicated left che-
licera on its proximal–distal axis, with a terminal secondary schistomely on the fang
(Cotoras et al., 2021) (Fig. 5.2c). This teratology could have occurred from an injury
to the area where the duplication occurs, similar to what has been observed in the
sea spider Pycnogonum litorale (Scholtz & Brenneis, 2016). The mechanism behind
this could be the “boundary model” (Meinhardt, 1986), where an appendage devel-
ops from the boundaries between two cell populations (anterior and posterior), and
a mechanical injury can cause the displacement of a third cell group, causing juxta-
position of morphogens that confer anterior, posterior, and ventral fates during
128 5 When THAT Exception Persists Almost as THAT Exception

regeneration. Knowing the possibility of the existence of this phenomenon behind

the teratology of the proximal–distal axis of the chelicerae allows the study of the
mechanistic basis of the induction of the proximal–distal axis of the chelicerae in
chelicerates, which could be a key to corroborate the homology with other head
appendages in Panarthropoda (primary antennae—mandibulates, chelicerae—euc-
helicerates, and chelifores—sea spiders) (Budd, 2002; Brenneis et al., 2008). The
study of this teratology and its comparative approach (Olson, 2012) leads to eluci-
dating shared patterns in the formation of chelicerae, opening the door to future
functional and experimental studies of appendage development in different
study models.

5.2.4.1 Reflections from the Discovery of Teratological Scorpions

Certainly, in each field, scientists come across rarities that fall into the teratological
domain, which may not have evolutionary potential, but inform us a lot about what
may be happening, for instance, at the physiological level. An example, derived
from personal observations in the field of scorpion reproductive biology, highlights
both the teratological occurrence and the subsequent resistance encountered within
a segment of the scientific community in regard to acknowledging and reporting
teratology. The fact referred to report the case of a male in a species of Bothriurus
bonariensis scorpion that presented an excessively long courtship, with the male
not being able to deposit the spermatophore. The courtship took almost 24 hours,
when it usually occurs after no more than one hour (Peretti, 1992). At some point
in this unusually long courtship, the couple was separated, and the male had a part
of his spermatophore outside the genital opening. The male died within a few days,
and the specimen was dissected. Surprisingly, it was found that this individual had
only half of the reproductive system, so it can be considered an “aberrant”
individual.
It was remarkable that despite lacking complete reproductive organs, this male
scorpion engaged in courtship behavior and initiated the expulsion of a partial sper-
matophore through his genital opening, which did not fully exit. Reporting this
curiosity as a scientific note in a local entomological journal (Peretti, 2000) was a
difficult task. On the one hand, a strange case was exposed, and on the other hand,
the implications of the lack of part of the reproductive apparatus were discussed.
This involved more than three years of reviews and a journal referee labeling the
report as of minor importance, as it was “merely teratological.” That is what it was,
something teratological, but apparently, this expression was taken as a synonym for
something that was not worth being reported at a scientific level. This simple but
intense experience made me reflect on the extent to which we researchers omit
reporting rare situations regarding the morphology, physiology, or behavior of the
animal group studied. It could simply be “self-censorship,” considering that teratol-
ogy is not worth reporting or that it is worth reporting, but we are too busy with
more important things.
5.2 Teratologies: Aberrations Revalorized 129

5.2.5 Some Examples of Teratologies in Plants

References to teratologies are more commonly found in relation to animals, includ-

ing humans. The inclusion of teratology in other kingdoms, such as plants, algae, or
fungi, is relatively rare and not as explicitly explored. This observation points to a
certain bias among human scientists. However, it is important to recognize that
abnormalities and aberrations also occur in these “nonanimal” groups. While the
study of teratology in the plant and fungal kingdoms is not as advanced as in ani-
mals, there are multiple examples of such phenomena documented in these organ-
isms (Phillips, 1881; Goebel, 1896; Bos, 1957; Meyerowitz et al., 1989).

5.2.5.1 Desired Malformations in Plants

“Malformations” in plants have attracted the attention of botanists for ages. Plants
can exhibit mutations that result in various types of deformations. One notable
example is fasciation, a phenomenon characterized by abnormalities in the growth
of the apical meristem. These abnormalities lead to the formation of flattened,
ribbon-­like, crested, or sinuous shapes in the stems, roots, fruits, or flowers, deviat-
ing from their typical appearance (White, 1948; Iliev & Kitin, 2011) (Fig. 5.3b).
This phenomenon is produced by mutations that may result from bacterial infection,
insect or parasite attacks, or chemical or mechanical damage (Iliev & Kitin, 2011).
Although these morphological alterations are not lethal, they can be inherited and
are more common in families such as Amaranthaceae and Cactaceae (Piringer &
Borthwick, 1961; Maliarenko & Mudrak, 2013).
Another teratology in plants appears as variegation and virescence, also due to
genetic alterations that produce abnormal pigmentations in various portions of plants
(Darwin, 1844; Kirk & Tilney-Bassett, 1978; Marcotrigiano, 1997) (Fig. 5.3a). A
common cause of variegation is the masking of the green pigment by others, such as
anthocyanins. This often extends to the entire leaf, turning it reddish or purple.
Variegation is considered unstable and can be easily lost in plants that turn green
again, but in some species, it is stable and does not change during the plant’s life (Yu
et al., 2007). Variegation mutants have played a prominent role in the history of
genetics (Tilney-Bassett, 1975; Kirk & Tilney-Bassett, 1978). For example, it was
observed that the mechanism of variegation transmission did not obey Mendel’s laws
(Baur, 1909; Correns & Correns, 1924), which opened the way for the discovery of
non-Mendelian (maternal) inheritance (Granick, 1955; Rheinberger, 2013). We will
also see later that some types of variegation can serve for mimicry in some plants.
Some cactus species that exhibit fasciation are highly valued by collectors of
these species (Fig. 5.3c). This illustrates some of the ideas previously discussed
regarding valuation and subjectivity when considering teratological individuals.
Depending on the organisms in which the malformation occurs and the morphologi-
cal outcome of the malformation, our subjectivity may appreciate these anomalies
and intentionally seek them out. For example, some varieties are attractive and orna-
mental, and gardeners and plant cultivators tend to preserve and even replicate these
130 5 When THAT Exception Persists Almost as THAT Exception

a b

c d

Fig. 5.3 Teratologies in plants. (a) Variegated leaves of Calathea roseopicta (Credits: Forest &
Kim Starr) (b) Normal (on top) and fasciated (below) white-rayed mule’s ear (Wyethia helianthoi-
des) (Credits: Perduejn) (c) Fasciation of saguaro cactus (Carnegiea gigantea) showing a “crested”
type (Credits: James G. Howes). (d) Witches’ broom on birch caused by the fungus Taphrina betu-
lina (Credits: Morten DD Hansen)
(a) Calathea medallion. License: CC BY 3.0 https://creativecommons.org/licenses/by/3.0, via
Wikimedia Commons. https://commons.wikimedia.org/wiki/File:Starr_070906-­8758_Calathea_
roseopicta.jpg. (b) White-Rayed Mule’s Ears (Wyethia helianthoides). License: CC BY 3.0,
https://creativecommons.org/licenses/by/3.0 via Wikimedia Commons. https://commons.wiki-
media.org/wiki/File:MulesEarFasciated_107393.jpg. (c) Crested saguaro cactus. License: Public
Domain. https://upload.wikimedia.org/wikipedia/commons/4/43/Crested_Saguaro_cactus.jpg. (d)
Taphrina betulina. License: No restrictions (CC0), via Wikimedia Commons. https://commons.
wikimedia.org/wiki/File:Taphrina_betulina_31161103.jpg
5.2 Teratologies: Aberrations Revalorized 131

cases (Datta, 2009). In this case, a certain “teratological degree” is accepted and
sought after because that malformation is considered striking, beautiful, exotic, and
extraordinary in a positive sense. Botanists even generate variegated plants through
inoculation with certain viruses (Marcotrigiano, 1997). Such is the attraction for
plants with these characteristics that there is in the United Kingdom the “Special
Interest Group on Variegated Plants of the Hardy Plant Society” that, since 1980,
shares and promotes the love for variegation.

5.2.5.2 Harmful Teratologies Could Bring Ecological Benefits

Another interesting example of teratology is the case of “witch broom,” an unusual

multiplication of branches on the upper part of the woody plant that resembles a
broom or bird’s nest (Hawksworth, 1961; Mathiasen, 1996) (Fig. 5.3d). This forma-
tion is caused by diseases produced by phytoplasmas, fungi, mites, aphids, and
nematodes, causing what is known as “Witch Broom Disease.” This disease can
cause economic damage in plants such as cocoa (Evans, 2002, 2007) and cherry
(Fujii et al., 1968), as well as in trees from which wood is extracted, such as pine,
oak, and walnut (Gomez et al., 1996; Yun et al., 2001; Spicer, 2016). Forests with
infestations of witch broom are more prone to forest fires (Harrington & Hawksworth,
1990). In the case of cocoa in Brazil, its production has been in decline for several
years since a large outbreak of “witches’ broom” in the late 1980s (Pereira et al.,
1990; Evans, 2002; Griffith et al., 2003), which meant that thousands of hectares of
cocoa farms were abandoned in Brazil and elsewhere in Latin America (Evans &
Prior, 1987; Pereira et al., 1996; Griffith et al., 2003; Hebbar, 2007). Multiple lines
of research are currently being developed to “combat” this teratology and mitigate
its economic consequences (Purdy & Schmidt, 1996; Lopes et al., 2003; Medeiros
et al., 2010; Tirado-Gallego et al., 2016). Here, we are at a negative extreme of tera-
tology, which from the name already carries a bias associated with something
“unpleasant” or “ugly” (since witches have had this reputation since ancient times).
Paradoxically, “witches’ brooms” are ecologically important because they create
and enhance the structural diversity of the forest canopy (Mathiasen, 1996; Tinnin &
Forbes, 1999). Many wildlife species visit witches’ brooms for nesting, foraging,
latrines, hiding, or resting (Hawksworth & Wiens, 1996; Mathiasen, 1996; Shaw
et al., 2004). For example, many threatened or endangered raptors use brooms in the
western United States as nesting sites (Fletcher, 1990; Martin et al., 1992; Seamans
& Gutiérrez, 1995; Forsman et al., 2015). Some mammals also nest on brooms, such
as red squirrels at various sites in North America (Parks et al., 1999; Tinnin & Forbes,
1999; Hedwall & Mathiasen, 2006) and northern flying squirrels that form aggrega-
tions within brooms during cold winter periods, utilizing brooms twice as much as
other nest sites (Mowrey & Zasada, 1984; Cotton & Parker, 2000). Maintaining
conifers with “witches’ brooms” in their habitat has been proposed to protect these
animals (Mowrey & Zasada, 1984; Cotton & Parker, 2000; Garnett et al., 2006). This
raises the complexity of categorizing teratology on certain occasions and reflects the
subjectivity we may encounter when assessing these phenomena.
132 5 When THAT Exception Persists Almost as THAT Exception

5.2.5.3 Teratologies That Inspired Theories of Plant Physiology

Especially interesting is how observations of certain plant teratologies inspired the-

ories and generalizations that were fundamental in plant physiology. In this case, a
unique or exceptional trait can lead to establishing a general rule. We have previ-
ously highlighted the case of variegation and the subsequent development of non-
Mendelian laws, although we would like to highlight the case of “phyllody” in
plants. The German poet and philosopher Johann Wolfgang von Goethe observed at
the end of the eighteenth century some roses in which the floral organs were substi-
tuted by structures similar to leaves or stems, in his words he expressed: “From our
acquaintance with this abnormal metamorphosis, we are enabled to unveil the
secrets that normal metamorphosis conceals from us, and to see distinctly what,
from the regular course of development, we can only infer.” These teratological
roses led him to suggest the “leaf theory”, where it was postulated that all parts of
the flower are highly specialized leaves. When specific interferences occur in the
early stages of growth (e.g., caused by phytoplasma or virus infections) (Mor &
Zieslin, 1992; Sim et al., 2004; Hogenhout & Segura, 2009), these organs may
develop, departing from the basic “construction plan” from the general pattern.
This type of anomaly is known as “phyllody” (Masters, 1869), i.e., the abnormal
development of floral parts into leaf structures, and implies sterility of the plant
(Mor & Zieslin, 1992). Goethe called this “metamorphosis” the main subject of his
homonymous essay (von Goethe, 1790). Just as teratologies and exceptions were
ignored or denied for a long time, the same has happened with certain theories or
observations based on these anomalies, such as what happened with Goethe’s pro-
posal. However, this theory was fundamental for explaining homeotic genes, homol-
ogy in comparative anatomy, the so-called ABC model of plants, and its implication
in the field of Evo-Devo in plants (Coen & Meyerowitz, 1991; Weigel & Meyerowitz,
1994; Causier et al., 2010).

5.3 Treasure Your Exceptions

William Bateson was one of the first geneticists to emphasize the significant role
that phenotypic rarities and exceptions play in both developmental and adaptive
processes. One of his famous quotes was highlighted in Cock and Forsdyke’s (2008)
inspiring biography of the scientist: “if I may throw out a word of counsel to begin-
ners, it is: Treasure your exceptions! When there are none, the work gets so dull that
no one cares to carry it further. Keep them always uncovered and in sight. Exceptions
are like the rough brickwork of a growing building, which tells that there is more to
come and shows where the next construction is to be”—W. Bateson (1908). This
highlights the importance of appreciating rare cases, minorities, and exceptions,
including the value of novel traits within an evolutionary framework (e.g., West-­
Eberhard, 2003, 2005). We will comment on these works later in the chapter focused
on changes from exceptions to rules.
5.3 Treasure Your Exceptions 133

In many groups of organisms, the “classic” definitions and descriptions in biol-

ogy configure in part what we can understand as generalities, rules, or what the
“majority” of species share, and this will be what identifies the group. However, as
we go deeper into the details of these descriptions, rare cases appear occasionally,
usually mentioned as friendly curiosities of natural history rather than as something
of evolutionary interest. When there are “exceptions” that make up certain minori-
ties, we are dealing with what we can call “intermediate exceptions,” i.e., species
that deviate from the general pattern in a not-so-drastic way and that include char-
acters measured as continuous variables (e.g., number of groups, body size, inten-
sity of coloration). In the descriptions, we can implicitly find these minorities, and
it is important to keep in mind that these “intermediate” exceptions also have bio-
logical values.
Thousands of examples could be mentioned regarding these “intermediate”
exceptions, implicit in the definitions, which tend to indirectly state the rule or pat-
tern for a given trait under analysis. However, the deepening and valorization of
these exceptions are not common. To learn about them, it is often necessary to go to
specific scientific articles where we can go deeper into these exceptions and some-
times (not often) to discussions or explanations about their existence. Moving
beyond the mere observation of patterns or “what” occurs, delving into the “why”
enables a better understanding of the underlying causality behind the analyzed
traits. This includes exploring “intermediate” exceptions that may arise at the group,
temporal, spatial, or combined levels. Without intending to be deterministic, expla-
nations of a functional-adaptive and/or evolutionary nature can be found for the
existence of these “intermediate” exceptions.
A taxonomic curiosity or exception can be invaluable from a comparative point
of view since, from a phylogenetic perspective, it provides valuable information on
potential phylogenetic and evolutionary hypotheses. As we saw in Chap. 2, the basis
of the beginning of an evolutionary process can be characterized by an exception,
from the point of view of how common this pattern or trait is in the group under
study, either from a global or a more specific perspective within a clade. Therefore,
it is crucial to approach each definition cautiously to avoid falling into the reduc-
tionism of generalizations. We must understand that “intermediate” (i.e., not
extreme but more subtle) exceptions are often prevalent in biological diversity, and
therefore, we must recognize the importance of exploring these exceptions in bio-
logical research and education.

5.3.1 Temptation to Generalize When Encountering

an Interesting Exception

The exceptional is in itself something neutral, neither useful nor useless, since
everything will ultimately depend on the interpretation and contextualization of this
morphological variant. It is as negative to quickly discard or omit them in the study
of a species, as it is to fall into an incorrect generalization and interpretation of what
134 5 When THAT Exception Persists Almost as THAT Exception

the exception represents or its potential evolutionary consequences. Something very

important in studying patterns is the detailed preliminary study with sufficient sam-
ple size to corroborate that specific observations are indeed norms or patterns or that
they are exceptions. Failures or oversights in this initial determination can lead to
misinterpretation of what a few data show with great repercussions for particular
theoretical fields or paradigms.
A classic example, in the field of sexual selection, in particular the mechanisms
of sperm competition, was that of the “killer” sperm also known as the “kamikaze”
sperm hypothesis. This was postulated in a brief review by Baker & Bellis (1988),
who argued that in mammals, males transfer part of their sperm agglutinated to slow
down the sperm of rivals. Thus, in addition to its primary role in fertilization, sper-
matozoa would serve a secondary function of obstructing the success of competing
males by destroying their immediate rival’s spermatozoa. Later, it became evident
that these speculative postulates were based on infrequent occurrences of sperm
agglutination within the female reproductive tract. This so-called “reproductive tac-
tic” was not a deliberate strategy in itself (Moore et al., 1999). Instead, sperm agglu-
tination was recognized as a rare or anomalous event. The mistake here was
attributing adaptive significance to an uncommon observation without thorough
prior analysis and experimentation.

5.4 Unfolded Life Diversity: Some Rare Taxa

and Amazing Strategies

As we are seeing, a whole book could be written on exceptions in different taxo-

nomic groups alone. Here, the intention is to highlight some biological examples
that would otherwise be omitted or ignored. Undoubtedly, in the present book, how-
ever, we give exceptions an important entity since it is an aspect of biology that is
highly underestimated, often even underappreciated. If we are talking about excep-
tions, we can mention “group exceptions” or taxonomic exceptions in more precise
terms. Here, we do not refer to exceptions within a species or a population but to the
species, genus, or family as a “whole,” a unit of taxonomic rarity. In several cases,
we address evolutionarily derived groups within the clade under study, which
exhibit many autapomorphies. We can also focus on phenotypic extremes within a
species. That is, to consider cases that are part of the natural variability within the
normal range of a particular phenotypic trait.
From a biodiversity standpoint, we can assess the degree to which supraspecific
species or groups have been genuine rarities and taxonomic exceptions. In other
words, they were or have been exceptions compared to other members of phyloge-
netically related taxa. Those taxa that are rare not only in having, for example, fewer
species or individuals (this would be purely a numerical variable) but also in terms
of body structure, physiology, ecology, etc., are true exceptions within the pattern or
rule that, explicitly or not, characterizes that group of organisms. In other cases, we
can highlight exceptions at the “spatial” level in terms of unique distributions or
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 135

completely different from what is expected for that taxonomic group. In the follow-
ing sections, we will try to include some examples in the context of rarities and
exceptions that show that we can find amazing cases in all groups.

5.4.1 Exceptional Animal and Plant Groups

5.4.1.1 A Protozoan That Does Not Appear to Be One

A few years ago, a notable species within the protozoa was reported, Spiculosiphon
oceana (Foraminifera) (Maldonado et al., 2013). This species combines several
exceptions to the Order in terms of its size, appearance (and way of reaching it), and
feeding strategy. Spiculosiphon oceana reaches a size of 4–5 centimeters in length
(Maldonado et al., 2013), so it was initially considered a multicellular animal, more
precisely, a sponge. Most foraminifera are only a few millimeters long and can form
shells that they use for shelter (Ruppert et al., 2003). While these shells, in general,
are formed by external mineral particles or calcium carbonate (Kaminski, 2004), the
shell of S. oceana is composed of silica spicules of dead sponge cemented and
bonded with a spongin-like organic substance (Maldonado et al., 2013). Thus, the
peduncle is covered by regularly arranged spicules, while the globular region is
irregularly arranged in an arborescent manner, allowing the extrusion of pseudo-
pods through the cavities between the spicules. Spiculosiphon oceana collect and
arrange spicules with high selectivity. This high selectivity also appears to be an
exception within the genus (Christiansen, 1964). These organisms show chemose-
lectivity and can precisely discriminate siliceous materials from other common
materials for the construction of shells. In addition, they can discriminate between
silica materials of different nature and even between spicules of different shapes and
sizes to locate them in different body portions (Maldonado et al., 2013).
Foraminifera are heterotrophic organisms that capture prey through their pseudo-
pods, usually small organisms such as diatoms or bacteria. However, S. oceana has
a peculiar feeding strategy related to its morphology and resemblance to carnivo-
rous sponges. As we will explain below, some sponges have exceptional adapta-
tions, such as a carnivorous feeding strategy (Demospongiae, Cladorhizidae)
(Vacelet & Boury-Esnault, 1995; Vacelet & Custódio, 2007; Lee et al., 2012). For
example, S. oceana exhibits remarkably similar size and morphology to sponges of
the genus Asbestopluma. Both these sponges and S. oceana are carnivorous preda-
tors, feeding on other smaller calcareous foraminifera and planktonic organisms.
This curious case could be considered a morphological and functional convergence
between exceptions from different taxonomic groups. In these sessile organisms,
prey is digested intracellularly since there is no digestive cavity per se. As previ-
ously discussed, these convergent exceptions would reflect adaptation to similar
environmental conditions and pressures. Strikingly, some species of Spiculosiphon
have been found in the same geographic location as cladorrhizid sponges (Vacelet
et al., 1994; Vacelet & Boury-Esnault, 1995; Maldonado et al., 2013).
136 5 When THAT Exception Persists Almost as THAT Exception

5.4.1.2 Tardigrades: The Most Resilient Organisms?

If we talk about exceptions, we must mention the tardigrades, a taxonomic group

with unique characteristics in the animal world. These microscopic invertebrates
(0.5–1 mm) were first described in 1773, and their discoverer was surprised by their
bear-like morphology: “Strange is this little animal, because of its exceptional and
strange morphology and because it closely resembles a bear in miniature. That is
the reason why I decided to call it little water bear. “—J.A.E. Goeze (1773).
With more than a thousand species worldwide, these organisms are present in
virtually every habitat on Earth (Guidetti & Bertolani, 2005): mountain peaks,
underwater volcanoes, tropical rainforests, and even polar environments. However,
tardigrades are exceptional because they are hyperresilient and extremophilic, i.e.,
they are resistant to extreme conditions. They can tolerate temperatures from -200 °C
to 151 °C (Wright et al., 1992; Hengherr et al., 2008; Horikawa et al., 2012), high
saline concentrations, the absence of oxygen, highly toxic chemicals (Baumann,
1922; Ramløv & Westh, 2001), and extremely high pressures (Seki & Toyoshima,
1998; Ono et al., 2008). Tardigrades tolerate extreme desiccation conditions through
a reversible physiological process called “anhydrobiosis” (Alpert, 2006; Jönsson
et al., 2008; Wełnicz et al., 2011). Through this process, they reduce their size and
body water (going from 85% to 3% body water) and metabolism by entering a state
of suspended animation (Crowe, 1975; Wright, 1989; Jönsson & Bertolani, 2001).
The time they can spend in this state can be several years (Jönsson & Bertolani,
2001; Rebecchi et al., 2006; Guidetti & Jönsson, 2002), surviving up to three
decades (Tsujimoto et al., 2016).
One of the most striking characteristics of tardigrades is their tolerance to high
doses of ionizing radiation (May & Guimard, 1964; Jönsson et al., 2005; Horikawa
et al., 2006). Both during anhydrobiosis and in the normal state, these organisms
possess high radiation resistance (Jönsson et al., 2005; Horikawa et al., 2006),
which could indicate that tolerance is not restricted to biomechanical protection of
cells during anhydrobiosis. However, it is not all daisies and sunshine for irradiated
tardigrades since, although they can survive, molt, and lay eggs, these eggs are not
viable, so radiation produces sterility in these organisms (Jönsson et al., 2005;
Horikawa et al., 2006). Recently, it was found that the protection of tardigrade cells
from X-rays is due to a specific protein (Dsup = Damage suppression protein) that
can be added to human cell cultures, providing them with partial protection from
this type of radiation (Hashimoto et al., 2016; Chavez et al., 2019). Unraveling the
mechanisms underlying anhydrobiosis and radiotolerance could contribute consid-
erably to developing new technologies in radioprotection, cryopreservation, and
preservation of biological material and in developing new technologies that protect
humans from these types of stressors (Table 5.2).
Recently, along with the description of a new species of the genus Paramacrobiotus,
their amazing ability to resist ultraviolet radiation was discovered. They possess a
“fluorescence shield” (Suma et al., 2020). Although fluorescence has been described
in many animals, very few studies have proven its functional significance (Lagorio
et al., 2015; Jeng, 2019). In this case, it could be experimentally demonstrated that
the presence of fluorescent pigments conferred protection from ultraviolet radiation
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 137

Table 5.2 Some examples of living organisms that represent exceptions or rarities within their
clades in terms of specific functions that, from a human perspective, could serve to minimize,
combat, or optimize industrial, agricultural, environmental, or medical production processes
Quality as an
exception within Potential
Organism a group Function in nature application References
Wax moth Larvae can The butterfly and Biorecycling/ Bombelli et al.
Galleria degrade its larva inhabit degradation (2017)
mellonella polyethylene colony enclosures
with beehives.
The larva feeds on
beeswax
Bacterium Degradation of Use polyethylene Recycling and Yoshida et al.
Ideonella hydrocarbon- terephthalate reuse of PET (2016),
sakaiensis derived (PET) as the Bornscheuer
compounds primary carbon (2016)
source
Amazon Polyurethane Use polyurethane Bioremediation Russell et al.
mushroom digestion under as the only carbon (2011)
Pestalotiopsis aerobic and source
microspora anaerobic
conditions
Coelacanth “Living fossil” It retains primitive Its notochord is Amemiya et al.
Latimeria traits due to its sold on the illegal (2013)
chalumnae slow evolution market as a
fountain of youth.
Many
environmental
associations point
to well-known
cosmetic companies
that include
coelacanth
notochord in their
formulas
Rare Important role in Keystone species These microbes Rubin (2008),
microbes biogeochemical regulating the have diverse Jousset et al.
cycles functioning of enzymes, some key (2017)
host-associated, in industrial
terrestrial, and processes, such as
aquatic thermophilic
environments cellulases for
biofuel applications
Tardigrades Anhydrobiosis, “Superpredators” Development of Jönsson (2007),
resilience, UV on flesh-eating new technologies Ono et al. (2008),
resistance, bacteria and that protect humans Guidetti et al.
resistance to nematodes, from (2012),
ionization and regulating the radioprotection, Hashimoto et al.
radiation food chain cryopreservation, (2016), Weronika
and preservation of & Łukasz (2017),
biological material Chavez et al.
(2019), Suma
et al. (2020)
(continued)
138 5 When THAT Exception Persists Almost as THAT Exception

Table 5.2 (continued)

Quality as an
exception within Potential
Organism a group Function in nature application References
Smith’s Vivid colors, a Predators, Potential models Patek et al.
mantis shrimp high-range vision regulators of the for studies of (2013), Chiao
Gonodactylus of the spectrum, reef food chain shooting et al. (2000)
smithii powerful frontal mechanics,
appendages hydraulics, hunting
apparatus, or the
neuroscience of
memory and
learning
Dictyostelium Cell movement, Decomposers in Useful in human Kay et al. (1978),
discoideum chemical soils rich in cancer research, Solomon et al.
signaling. Cell organic materials model for studying (2000), Hägele
differentiation. cell differentiation et al. (2000),
Chemotaxis. Williams et al.
Sociality (2006), Annesley
& Fisher (2009),
Jia et al. (2009),
Clarke (2010),
Sillo et al. (2011),
Bozzaro &
Eichinger (2011),
Steinert (2011),
Müller-
Taubenberger
et al. (2013),
Hashimura et al.
(2019), Pal et al.
(2019), Schaf
et al. (2019),
Pears & Gross
(2021)
Panellus Bioluminescence Wood Bioindicator of Stevani et al.
stipticus decomposers environmental (2013), Prasher
pollution et al. (2014),
Ventura et al.
(2021)

to these animals. Furthermore, Suma et al. (2020) were able to extract these pig-
ments and transfer the protection to other UV-sensitive organisms, doubling their
survival, so this ability of tardigrades could be universal and eventually have prom-
ising applications in industry or other applied fields (Table 5.2).
Anhydrobiosis not only allows tardigrades to survive in extreme terrestrial con-
ditions but also allows these animals to survive unnatural conditions such as space
vacuum (which imposes extreme dehydration) and solar/galactic cosmic radiation
(Jönsson et al., 2008). Different species of tardigrades were sent to outer space
twice (FOTON-M3 Mission—2007—Jönsson et al., 2008; Rebecchi et al., 2009,
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 139

2011a; Persson et al., 2011; Shuttle Mission STS-134 Endeavour—2011—Rebecchi

et al., 2011b; Vukich et al., 2012), returning to Earth safe and sound and even being
able to reproduce upon arrival. In space conditions, solar radiation imposes damage
and changes in DNA structure by specific photoproducts. It is speculated that tardi-
grades may have special configurations of DNA or other cellular components that
prevent cell damage and superefficient DNA repair systems (Jönsson, 2007;
Rebecchi et al., 2011b; Vukich et al., 2012). Thus, tardigrades are promising models
for Astrobiology, offering the unique opportunity to study the effects of space expo-
sure on metazoans. Then, the strategies used by these incredible animals can be
extrapolated to protect other organisms exposed to these environments, including
humans (Jönsson, 2007; Ono et al., 2008; Guidetti et al., 2012; Weronika & Łukasz,
2017). Recently, using mathematical models, the exceptional resilience of tardi-
grades has been calculated, and it has been suggested that they would survive astro-
physical catastrophes (such as ocean temperatures rising to boil), representing the
most resilient life form in the animal world (Sloan et al., 2017).

5.4.1.3 Sponges Breaking Several Rules

Sponges are found within the phylum Porifera, which currently has more than 9000
species. This group of organisms has specific characteristics that make it unique:
they are sessile, with an internal skeleton formed by calcareaous spicules or silica
spicules, with or without spongin (collagen-like threads). Their body is perforated,
forming an aquifer system through which water enters and exits through a larger
perforation, the osculum. This water current is used for feeding, waste elimination,
gamete release, and gas exchange. No less important is the fact that they lack true
differentiated tissues. These characteristics are listed at the beginning of their
description in any book on invertebrate zoology and phylogeny (e.g., Ruppert et al.,
2003; Brusca et al., 2016; Giribet & Edgecombe, 2020).
In sponges, we can find multiple “intermediate” type exceptions. For example, it
is common to think of a sponge as an immobile, medium-sized, brownish-colored
animal. However, “brownish color is the exception rather than the rule in Porifera“
(Ruppert & Barnes, 1994). Brownish sponges predominate in the class Calcarea but
not in the others, where most species have bright colors, which are thought to serve
as protection against solar radiation, as well as aposematic colors. Another example
involves exceptions linked to the size of the organisms. Also within the class
Calcarea, there is a very simple type of body structure called “asconoid,” present,
for example, in the genus Leucosolenia, where each individual of the colony (united
at their bases by a stolon) has a size of 2.5 cm or even less. In this genus, it has been
established that “only rarely [each individual] is more than 10 cm tall” (Ruppert
et al., 2003). This would imply that such “rare occasions” do exist and lead us to
ask: what are these exceptional cases? Do they occur in particular places or types of
water currents? Indeed, the “rule” obviously is that the asconoid type is always
small, but the exceptions of larger sponges should invite us to think about what lies
behind them. In this case, the exception of the “implicit rule” for body size in
140 5 When THAT Exception Persists Almost as THAT Exception

Leucosolenia is L. somesii, in which each member of the colony can exceed 10

centimeters, reaching 12 cm (Van Soest et al., 2007).
The absence of true tissues is so important that sponges have traditionally been
grouped into a particular subkingdom known as Parazoa. This differs from the
Eumetazoa subkingdom, where the rest of the animal groups are found, where we
can already find true tissues (i.e., solid junctions between the cells of a given stra-
tum). In parazoans, it was known that the cells of the outermost layer, the pinaco-
derm, laterally lacked cell–cell junctions between each other (e.g., the desmosomes
of higher animals) and a basal lamina for seating (formed by a collagen layer in other
animals). Therefore, although they form strata “analogous” to eumetazoans (e.g.,
pinacoderm equivalent to a “proto-epidermis”), they cannot be termed true tissues
but as an ordered, but not cohesively united, aggregation of cells. This was the clas-
sical concept and rule for Porifera, and it is still the one that is referred to when
defining them in their generalities. However, such a rule, almost of a level I for the
group, presents surprising exceptions discovered and analyzed in depth not long ago.
Within the family Oscarellidae (class Homoscleromorpha), there is an exception
that represents a very valuable evolutionary link between Porifera and the animals
of the subkingdom Eumetazoa. We refer to what happens in the genera Oscarella
and Pseudocorticium (Fig. 5.4b) (Van Soest et al., 2012). In them, we find some-
thing that departs from what is reported as a rule for the phylum Porifera, as many
lack a skeleton and mainly possess a true epithelium. Ereskovsky et al. (2009) ana-
lyzed the ultrastructure of the pinacoderm layer of these sponges and found that at
the base of this layer, there is a basal lamina formed by type IV collagen, as occurs
in eumetazoans. Therefore, this pinacoderm can be considered an intimately associ-
ated cellular layer, i.e., a true tissue (Fig. 5.4c). Therefore, using the term epidermis
instead of pinacoderm is correct. These discoveries were very important, to the
point of suggesting that Homoscleromorpha would form a kind of “link” between
the subkingdoms Parazoa (rest of Porifera) and Eumetazoa.
Now, what explanation could we have for the appearance of this “taxonomic
exception” that Oscarella represents? The authors mentioned above have tried to
provide one explanation that is quite logical: these sponges inhabit very shallow
waters on the Mediterranean coasts, where they may be embedded in rocks or their
interstices, that are continuously whipped by water waves. These conditions favor
the absence of a skeleton. However, the lack of a skeleton also means having a
firmer pinacoderm to resist the beating of the waves against the body of the sponge
and prevent it from being destroyed. The presence of basal lamina would contribute
to this, forming a proper epithelium. As we can see, two specific modifications (lack
of skeleton and appearance of an epithelium) would be intimately linked to environ-
mental characteristics. However, the latter alone would not explain why changes
“should” be directed toward these morphological patterns; we are not appealing to
determinism but rather to the selection of specific random mutations that, primarily,
would have occurred in the ancestors of these sponges while they were trying to
colonize the more coastal and agitated habitats of the Mediterranean. Thus, we see
that the exceptions have their explanation, which may result from adaptive pro-
cesses to the surrounding environment.
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 141

b c

Fig. 5.4 Homoscleromorphae, a group full of exceptions among sea sponges. (a) Curious deep-
sea carnivorous sponges (Credits: National Oceanic and Atmospheric Administration | Office of
Exploration and Research, NOAA Photo Library). (b) Oscarellidae with its strange morphology
(Credits: Géry PARENT.). (c) Histology of Oscarella lobularis showing the basal membrane (from
Ereskovsky et al., 2015)
(a) Chondrocladia lyra. License: CC BY 2.0. https://creativecommons.org/licenses/by/2.0.
https://www.flickr.com/photos/noaaphotolib/39695069932/. (b) Oscarella lobularis. License:
Public domain. https://commons.wikimedia.org/wiki/File:Oscarella_lobularis_(Schmidt,_1862).
jpg. (c) Oscarella lobularis. License: Public domain. https://doi.org/10.1371/journal.pone.0134566
142 5 When THAT Exception Persists Almost as THAT Exception

Continuing with other examples of this wonderful group of invertebrates, we can

contemplate another rarity. This time, it represents an extreme within a class, with so
many autapomorphies that make it a well-derived group. We refer to a particular spe-
cies of the so-called “carnivorous” sponges. Lee et al. (2012) described the fascinating
Chondrocladia lyra (Cladorhizidae) (Fig. 5.4a), which has a particular body arrange-
ment consisting of stems with spicules that become two rows of intersecting columns.
Small animals such as crustaceans are entrapped within them and subsequently
phagocytosed by the pinacoderm. This represents a distinct departure from the feed-
ing mechanism commonly observed in other Porifera. In those species, nutrients are
acquired through water currents via orifices and the capture of microparticles by cho-
anocytes, specialized cells found in ducts or aquifer chambers. Without the meticu-
lous examination of spicules and histology, it would be very challenging to categorize
the sponges belonging to the Cladorhizidae family as part of the demosponges.
In these sponges, we also found globular apical zones in each column containing
spermatophores. This contrasts with the male gamete-producing zones of the other
Porifera, which are derived from choanocytes. Here one may ask “why” or “what
for” these sponges exhibit these traits that confer an exceptional character to this
species. Chondrocladia lyra lives at great depths (approximately 3,500 meters),
with low food availability and less water flow, and in conditions of low illumination,
resulting in less phytoplankton available to filter. Under these conditions, the “hunt-
ing” net-like body arrangement would prove more efficient than an in-stream sys-
tem for feeding (Lee et al., 2012). Thus, this “body shape” would have developed
due to the environmental characteristics of this particular environment that favor a
shift in body morphological pattern from a microscopic water-filtering in-stream
feeding system to one adapted for capture with a larger available food web (Lee
et al., 2012). Additionally, the sperm production zone is moved to the apical zone of
each capture column, optimizing the entire lateral surface of each column. That is,
almost the entire body is now used exclusively as a capture net, while at the same
time, the dispersal of gametes occurs from the top of the individual’s body.
Again, we can, as in the case of sponges with epithelium, find plausible explana-
tions for these exceptions on a comparative level with other members of their clade
in terms of morphology, physiology, and ecology. These two examples from marine
sponges illustrate how taxonomic exceptions highlight the remarkable extent to
which evolution can manifest adaptive processes in surprising phenotypic patterns
that are well suited to the environment.

5.4.1.4 Some “Worms” as Models of Exceptions

When we speak of exceptions, particularly at the taxonomic-relative level, animal

models can be particularly useful. Examples are those known as “worms.” This
terminology encompasses several phyla, such as flatworms, nematodes, annelids,
and xenacelomorphs, among other animals. Within them, some cases fall into the
category of exceptions. In the following sections, we will take some of these cases
as examples, detailing the features that make them taxonomic exceptions.
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 143

Using Foreign Weaponry: Flatworms and Nematocysts

Turbellaria, a class of flatworms of the phylum Platyhelminthes, is characterized as

a basal group and is primarily free-living, generally predator and scavenger, although
there are some commensal and ectoparasitic species (Ruppert et al., 2003). Within
this diversity, there are many particular feeding strategies. Predators, for example,
have hooks, secrete mucus, or use secretions from the epidermis to obtain food. The
secretions of the epithelium and mucus help prey adhere and protect the worm from
attack, as it can move easily, thanks to this lubrication. In this context, one tactic in
the face of potential danger is the expulsion of “rhabdites,” protein capsules, or acid
mucopolysaccharides from glandular cells of the epidermis. In turn, the rhabdites
protect against water stress and allow the cilia on the ventral side to move over a
mucous base, facilitating locomotion.
However, although we find variants of these types of secreted products, an excep-
tional example is when foreign “weaponry” is used (i.e., that has been initially pro-
duced by another organism). We have as a maximum exponent of this rare species
of the genus Microstomum that sometimes feeds on hydras, a typical freshwater
cnidarian. The point is that they will use certain defense elements of these prey for
self-protection. Among the species in which this phenomenon has been analyzed
are M. caudatum and M. lineare, with long-standing studies on the subject (Kepner,
1911; Kepner & Nuttycombe, 1929).
To understand this, let us review that these cnidarians possess specialized struc-
tures called “nematocysts” in their tentacles as a protective mechanism (i.e., small
coiled threads produced and stored inside cnidocytes). The nematocysts are dis-
charged by the hydra to defend themselves and, at the same time, immobilize prey.
They can be of different types, such as enveloping, sticky, and toxic (toxicists). This
last variant is characterized by having a basal part that forms a vesicle charged with
venom with a neurotoxic effect. It is precisely this type of nematocyst that
Microstomum recycles. When ingesting the captured hydra, Microstomum does not
digest the toxicists but makes them migrate from its digestive tract to the epidermis,
where they will remain housed inside the cells of the simple epithelium (Kepner &
Nuttycombe, 1929; Kepner, 1951; Krohne, 2018, 2020). In this way, Microstomum
may use them for its defense or prey capture, similar to freshwater hydra.
Interestingly, Microstomum tends to eat hydras until he fills that “nematocyst bat-
tery,” after which it ceases to feed on them. This behavior suggests that its ingestion
is primarily driven by the need to acquire defensive armaments. Once Microstomum
has used them, it will return to feed on hydras and repeat this cycle of supplying
itself with defensive nematocysts. Even after asexual reproduction, when the worm
divides transversely, the nematocyst endowment will be passed on to the offspring,
thus becoming an epigenetic type of inheritance in a more literal sense.
In the context of this book, there is no doubt that we are in the presence of true
group exceptions. Microstomum represents an absolute rarity among the approxi-
mately 20,000 species of flatworms and 3500 turbellarian species. There are discus-
sions about how this worm came to develop this strategy and its implications from
an Evo-Devo point of view. What is certain is that by the 1950s, this example came
144 5 When THAT Exception Persists Almost as THAT Exception

to be widely used as evidence of acquired traits with a clear adaptive value. This was
mainly seen as support for the twentieth-century “Neo-Lamarckian” school, with
criticisms of Darwinism on unconventional forms of adaptations from a viewpoint
prior to the development of epigenetics (Grassé, 1977).
On the other hand, it is interesting to know if this strategy is unique or if it also
appears in some other groups. In other words, are more animals exhibiting this
“armament-stealing” behavior? Gooheart & Bely (2016) note that while chemical
sequestration is widespread among animals (e.g., subsequently using prey toxins to
prey or for self-defense), the ability to seize entire structures is not common. While
nematocyst sequestration remains rare, “Kleptocnidae” behavior (Krohne, 2018,
2020) also occurs exceptionally at the “intragroup” level in other organisms. In
addition to Platyhelminthes, it appears in representatives of Ctenophora,
Acoelomorpha, and Mollusca (Gooheart & Bely, 2016). Nematocyst sequestration
is estimated to have evolved at least 9–17 times in these phyla. This ability is not
restricted to Microstomum but is shared, analogously and with their respective par-
ticularities, among several species of different phyla. Thus, we see that an exception
is not something that exists as an absolute but that even though it is a rarity, it can
be characteristic of a pool of organisms, which within their respective clades are
unique for this trait.

“Photosynthetic” Worms

Within the xenacelomorphs, we can find other exceptional cases. One of them is
related to the “rule” that suggests that, apart from corals and other sedentary organ-
isms, triblastic metazoans (i.e., which already possess mesoderm in addition to
ectoderm and endoderm) have to ingest food to acquire nutrients. This is the oppo-
site of what can occur with autotrophic organisms such as algae and plants. However,
cases of symbiosis between animals and plants exist, although they are strange com-
pared to the predominant pattern in the Animal Kingdom. In this framework, we
find the worm Symsagittifera roscoffensis, which presents green algae symbionts
(called Zoochlorella because it is inside an animal). This alga, Tetraselmis convolu-
tae, photosynthesizes, and the worm feeds on the product of photosynthesis
(Muscatine et al., 1974). This represents a clear example of photosymbiosis, in this
case, between a metazoan and an alga. In effect, the alga is introduced into the early
larval stages of the worm, which still feeds heterotrophically. When it reaches adult-
hood, it becomes totally dependent on the algae, to such an extent that its absence is
lethal for the worm, so that the two organisms can be said to form a “photosymbiotic
unit” (Bailly et al., 2014). It no longer presents a translucent color but is green due
to the content of these green Zoochlorella. The worm is gregarious and even behaves
by clustering toward light areas to facilitate photosynthesis. The adult of this worm
is considered a true “solar-powered mature stage” due to this type of behavior
(Bailly et al., 2014).
Several studies have been carried out on S. roscoffensis, as a model Acoela spe-
cies for studies on this symbiotic relationship, at the level of respiration and
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 145

photosynthetic physiology. Other more recent studies have focused on its photo-
taxis behavior concerning facilitating the photosynthesis of its symbiont (Nissen
et al., 2015). In addition, it is an interesting organism for studying brain regenera-
tion capacity (Sprecher et al., 2015). Definitely, this exceptional species has
become a model for research on photosymbiotic relationships in marine animals
due to this particular type of linkage with algae. In fact, the knowledge of
S. roscoffensis. also allows extrapolation to other photosymbiotic animals, such as
corals, which are vulnerable to climate change (e.g., water warming and acidifica-
tion) (Bailly et al., 2014). Another species of the same class, convoluta partially
prescinds from this symbiosis with an alga of the genus Licmophora, as it can
obtain its food heterotrophically by consuming juvenile mussels, copepods, and
other microorganisms (Byrnes & Witman, 2003), similar to other free-living
worms. In a way, linked to these examples, we will later discuss the concept of
symbiogenesis postulated by Lynn Margulis, among others, as an alternative—or
at least as a complement yet to be synthesized as a whole—to the Synthetic or
Neo-Darwinian Theory.

Atypical Parasites: Separate Sexes in a Hermaphroditic World

Among the invertebrate parasites, we found trematode flatworms of the digenean

group, characterized by parasites that mainly have vertebrates as definitive hosts.
The intermediate host, where the larval stages develop, is usually a gastropod mol-
lusk. A typical characteristic of the digeneans is hermaphroditism. In fact, this
particularity is reflected in a neophorous reproductive system, with great develop-
ment and division of functions of the female part of the reproductive apparatus (an
ovary and specialized vitelline glands) in such a way as to produce ectolecithal
eggs or eggs that take up yolk from the vitelline glands (Adell & Riutort, 2021). In
contrast, there is an Arcophore reproductive system where the gonad does not
exhibit division of functions and produces endolecithal eggs (common in some
Turbellaria). Thus, digeneans are very effective at producing thousands of eggs,
which is crucial in the life cycle of a parasite due to the high mortality when mov-
ing from one host to another (Ruppert & Barnes, 1996). Among the digeneans, the
family Schistosomatidae stands out for exhibiting particular characteristics. This
family has approximately 100 species among the approximately 6000 species of
the subclass Digenea (Loker & Brant, 2006). These organisms are parasites hosted
in the portal-hepatic venous system of the definitive host (generally two) and have
the “furcocercaria” as the vertebrate infecting larval stage, which is mobile and
infests the definitive host. The best-known species of the group where sexual
dimorphism is highly accentuated is Schistosoma mansoni, which causes schisto-
somiasis that affects Southeast Asia and part of the tropical and subtropical regions
of the world.
What makes schizosomatids particularly unique is that they are dioecious. This
synapomorphy, presenting separate sexes, is a rarity in the class Trematoda. Indeed,
dioecious parasitic flatworms are rare but occur among the Digenea, Monogenea,
146 5 When THAT Exception Persists Almost as THAT Exception

and Eucestoda that inhabit the gills, intestines, and circulatory systems (Platt &
Brooks, 1997). Interestingly, dioecy would not have occurred during specialization
on homeothermic definitive hosts but would have been present when infecting ecto-
thermic archosaurs (Brant & Loker, 2005). Today, there is a family of schizosoma-
tids specialized in homeothermic hosts and two other families in ectotherms. From
an evolutionary point of view within the class, what we call the “rule of hermaphro-
ditism” was replaced in these groups by the “rule of dioecy” beyond the type of
definitive host.
Why should these organisms abandon the successful hermaphroditic system?
Platt & Brooks (1997) mention as one of the possibilities the adaptation to a blood
medium, mainly venous, coupled with the need for females to oviposit in thin mes-
enteric veins associated with the intestinal wall. The combination of these factors
could have favored the replacement of a depressed and extensive body by a filiform
and elongated body. This change, however, represented a constraint to the further
optimized development of a hermaphroditic reproductive apparatus. As a solution,
this change was accompanied first by androdiocidity and progressively by marked
sexual dimorphism. This resulted in flat, more muscular males that house the female
within a “gynecophore” channel formed by the folding of the male at the time of
fertilization. This relationship between the sexes allows the transport of females to
oviposition sites. Females, on the other hand, specialized to be slimmer and longer
to enter the subepidermal venous capillaries of the gut in which they oviposited
(Platt & Brooks, 1997; Brant & Loker, 2005). It has been postulated that genetic
changes, such as chromosomal inversion or translocation, mediate the appearance
of dioecy (Platt & Brooks, 1997).
Interestingly, we can find different degrees of sexual dimorphism according to
each host’s characteristics of the arterial and mesenteric systems. As we named it,
S. mansoni has a marked sexual dimorphism, while other species, such as
Dendritobilharzia pulverulenta, have less sexual dimorphism, inhabiting the arte-
rial system of ducks. In this species, the females remain in the large vessels of the
heart and do not migrate to areas of thin subintestinal veins as the blood pressure is
very high, ensuring the transport of eggs in the larger blood vessels. Consequently,
these worms are poorly filiform, and while they remain dioecious, sexual dimor-
phism is slight (Loker & Brant, 2006).
An exciting concept can be illustrated with this example: “a chain, associated
concatenation, of exceptions to the rule that harbor other exceptions and so on.” In
other words, schistosomatids are exceptions because they are dioecious among the
Trematodes. In turn, this leads to great sexual dimorphism, which precisely charac-
terizes “most” schistosomatids and becomes a rule pattern for the family. However,
as the last example shows, there are exceptions to that family rule, according to the
particularities of the punctual habitat within the circulatory system. This concept or
“paradox” of a chain of exceptions and rules serves as a reminder that the classifica-
tion of something as a rule or exception is relative and dependent on the context of
comparison and the level of analysis. As we suggested before, rules and exceptions
are not closed compartments but are intrinsic dynamic, depending on the compara-
tive, evolutionary, spatial, and group-level perspective (or their combination) being
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 147

considered. These mere examples serve to reinforce the need to always holistically
and dynamically analyze the patterns and rarities at the evolutionary and phyloge-
netic levels.

5.4.1.5 Contributions from a Rare Crustacean

Smith’s mantis shrimp, Gonodactylus smithii, is a Malacostracan crustacean inhab-

iting the Great Barrier Reef of Australia. This species represents an exception not
only in its group but also among predatory organisms in general due to its “leverage
and pressure” apparatus used for prey capture (Cox et al., 2014). This consists of a
series of modified parts of its exoskeleton in the style of ossicles that articulate,
resulting in movements of such speed and force that they produce something equiv-
alent to the shot of a bullet on the shell of a clam, to the extent that it is said that this
shot is like that of “a 22 revolver.”
In connection with the aforementioned, and equally remarkable albeit exten-
sively publicized, these organisms stand out due to their exceptional visual capabili-
ties. They are considered one of the best and complete visions among animals
(Marshall et al., 1991). They are endowed with two pedunculated eyes that can
move independently and even in different directions from each other. Their vision is
chromatic, so they are specialized for detecting colored signals from their conspe-
cifics and even fish or other animals (Chiao et al., 2000). It has 16 photoreceptors,
much more than the only 3 present in humans. In addition, it has infrared and ultra-
violet vision and four linear and two circular polarization types (Kleinlogel &
White, 2008). This allows it to better map objects to distinguish them properly.
Gonodactylus smithii, as well as the peacock mantis shrimp, Odontodactylus scyl-
larus, represent the first cases of animals with dynamically polarized vision, where
polarization information is maximized through rotational movement of the eyes
(Daly et al., 2016). Their eyes are of the compound type, as in insects and some
crustaceans, but are optically divided into three separate zones that produce overlap-
ping fields of vision (Cronin et al., 2017). The ommatidia have different sizes in the
central girdle relative to those that make up the rest of the eye, representing a more
conventional compound eye. These central girdle ommatidia are usually larger and
are believed to be used for color perception and polarization at different wave-
lengths as well as ultraviolet light. Finally, the presence of “pupils,” up to three per
eye, means that each eye zone can see the same point simultaneously from several
viewing directions (Land et al., 1990). This feature could achieve stereoscopic
vision from one eye (Exner, 1891).
More recently, the finding of another trait has added a reputation of true rarity
to these species. These animals have neural memory and learning centers in their
brain (Wolff et al., 2017), something not previously known to exist among crusta-
ceans but in insects, identified as mushroom bodies. In fact, these appear in social
insects such as bees, as they are complex centers associated with memory capacity
and learning linked to having, for example, excellent spatial orientation at feeding
time. In these shrimps, it could be linked to their ability to visit certain areas
148 5 When THAT Exception Persists Almost as THAT Exception

several times, remembering paths and places. The finding of these centers opens
the debate as to whether these mushroom bodies were in the common ancestor of
crustaceans and insects and were lost later in evolution in most of the former (with
the exception of these shrimps) or whether it is an evolutionary convergence
observed in G. smithii. Future studies at the transcriptomic level will then be able
to see and compare the naturalness of specific proteins and thus answer this
question.
Thus, as a whole, we have here a species that at least shows multiple striking
characteristics that are rare in its group and even in comparison to other distant
ones, making it a “multitrait” exception. The value of these exceptions as potential
models for studies of shooting mechanics, hydraulics, hunting apparatus, or the
neuroscience of memory and learning is invaluable (Table 5.2).

5.4.1.6 Cephalopods: The Most Intelligent Invertebrates?

Cephalopods have approximately 800 current species and are a remarkable class
among invertebrates, as they possess many characteristics that undoubtedly position
them as an exception to the group. First, these organisms are among the largest
invertebrates, with the squid genera Architeuthis and Mesonychoteuthis being able
to reach approximately 18 meters and weigh up to 1 ton (Clarke, 1966; Roeleveld &
Lipinski, 1991; Ellis, 2006). These organisms inhabit the abyssal depths, and it is
thought that this large size could be because they inhabit polar environments with
high latitudes so that they would follow ecological rules, some of which we saw
previously (e.g., temperature-size rule, Bergmann rule, oxygen availability coupled
with low metabolic rates hypothesis) (Atkinson, 1994; Chapelle & Peck, 1999,
2004; Vermeij, 2016).
The eyes of these squids are the largest in the animal kingdom and have evolved
to detect large predators rather than prey, although they are considered voracious
predators themselves (Rosa et al., 2017), being key in marine food webs (Xavier
et al., 2002, 2011; Cherel et al., 2004; Cherel & Hobson, 2007). It is believed that
the rarity and extraordinary size of these creatures inspired legends from
Scandinavian mythology, giving rise to the “kraken” or “leviathan” (probably from
the genus Architeuthis), which may have originated from sightings of squid 33–45 m
long (Philip, 2004). These creatures inspired Jules Verne in his work Twenty
Thousand Leagues Under the Seas (Verne, 1870) and have appeared in popular
films such as Pirates of the Caribbean: Dead Man’s Chest (Verbinski, 2006) and
several video games (Salvador & Tomotani, 2014). This highlights the human fasci-
nation with these extremes, ranging from mythological terror to literary inspiration
(Ellis, 2006).
At the morphological level, cephalopods have other characteristics that distin-
guish them from other invertebrates: they have the foot next to the head diversified
from 8 (Octopus) to 90 tentacles (Nautilus), they have appendages that are modified
into reproductive structures to introduce spermatophores into the female paleal cav-
ity, they have strong jaws that they use to tear prey, their circulatory system is closed
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 149

with a network of capillaries, a systemic heart for the blood and two gill hearts that
provide pressure to the circulation and the entrance of blood to the gills (Ruppert &
Barnes, 1996).
However, the most exceptional feature of this group is certainly its complex ner-
vous system that resembles that of vertebrates in relative size (Packard, 1972) and
complexity (Young, 1991; Hochner et al., 2006; Shigeno et al., 2018). It consists of
ganglia around the esophagus, forming a brain surrounded by a cartilaginous mass.
This feature explains the existence of extremely fast behaviors, as they possess giant
motor nerve fibers that control the contractions of the mantle muscles, allowing the
outflow of pressurized water. In addition, they possess first- and second-order giant
neurons connected to stellate ganglia and third-order giant neurons that innervate
mantle muscle fibers. Due to the characteristics of their nervous system, cephalo-
pods are considered the most “intelligent” invertebrates because they are able to
open closed containers, find exits to mazes and learn specific behaviors, have long-­
term memory, and can rapidly change color (Darmaillacq et al., 2014; Mather &
Dickel, 2017; Hanlon & Messenger, 2018). These exceptional traits have success-
fully allowed cephalopods to occupy multiple ecological niches by presenting com-
plex inter and intraspecific interactions.
The intelligence of cephalopods and vertebrates with large brains appears to have
evolved through different pathways at different pressures and in association with
different life histories, despite sharing great sophistication (Amodio et al., 2019).
Cephalopods’ great flexibility, mate competition, and potential cooperative hunting
with other species (Bayley & Rose, 2020) make it clear that their interactions with
other individuals would not be as simple as previously thought (Boal, 1996; Hanlon
& Messenger, 2018). In addition, octopuses may use coconut shells as a defensive
tool and even bivalve shells and stones as shields against shark attacks (Jeffs &
Brownlow, 2017), which could be related to planning abilities and the expression of
behavioral innovation (Finn et al., 2009). Cephalopod research has great potential
for understanding the evolution of intelligence in different animal groups (Amodio
et al., 2019).

5.4.1.7 Exceptional Fungi

Challenges When Classifying Fungi

Fungi are extraordinary organisms and represent one of the cases where their mul-
tiple “outside the rules” characteristics have troubled naturalists and scientists
throughout history, which has been reflected in the uncertainty in their taxonomic
classification over time (Dube, 2015). This ambiguity is also reflected in the ety-
mological root of “fungus” from the ancient Greek σφογγος (sponge), which refers
to the macroscopic structures of molds and mushrooms. From this, the German
terms “Schwamm” (sponge), “Schimmel” (mold), and the French “Champignon”
have been derived. At first, fungi were considered closer to plants within the sub-
kingdom Talobionta (the thallophytes, or thallus plants) (Scagel et al., 1977) and
150 5 When THAT Exception Persists Almost as THAT Exception

were believed to be descended from red algae (Rhodophyta) (Demoulin, 1985),

perhaps because they possess plant-like cell walls composed of chitin rather than
cellulose. In addition, they share other plant characteristics, such as vacuoles,
reproduction by spores such as mosses or ferns, growth in the soil, and lack of
locomotion.
Later, they were divided into a “separate” kingdom and grouped as “fungi”
(Whittaker, 1959), although some were part of the kingdom Protozoa (amoeboid
fungi and fungi with zoospores). In the Cavalier-Smith eight-kingdom scheme, they
belonged partly to the kingdom Protozoa (the amoeboid fungi), partly to the king-
dom Chromista (the Pseudofungi), and all others to the kingdom Fungi. Fungi pro-
duce L-lysine amino acids similar to euglenoids and bacteria (Zabriskie & Jackson,
2000). However, certain characteristics, such as the absence of chloroplasts (imply-
ing the impossibility of photosynthesis), heterotrophy (feeding by absorption), and
the accumulation of glycogen as a cellular reserve substance (and not starch-like
plants), make it evident that fungi are phylogenetically closer to animals (forming
the clade Opisthokonta by possessing flagellated cells) (Cavalier-Smith, 1987;
Stechmann & Cavalier-Smith, 2002). In other words, the rarity of these organisms
as an “exquisite corpse” has made it difficult to include them in a single group or to
group them with specific taxa.

Amoeboid Fungi

It is estimated that more than 5 million different species of fungi are on the planet,
but less than 15% are currently known. When we think of fungi, the first thing that
comes to mind is the charismatic “mushrooms” with prominent fruiting bodies,
generally multicellular, with sexual reproduction. Of course, these are abundant and
more showy and are called “true” mushrooms, belonging to the subkingdom
Eumycota. However, there is a very peculiar group of fungi known as “nontrue,”
“amoeboid,” “mucilaginous molds” or “pseudofungi,” with approximately 1200
species belonging to the group of Myxomycota or Mycetozoa (Phylum Amoebozoa
and Chromalveolata) (Hibbett et al., 2007). From an epistemological point of view,
it is interesting how the “true” is more showy or conspicuous, while the exceptional
is relegated to something “not true.” However, we have already seen scientists’ dif-
ficulty in determining what is and what is not a fungus. These organisms go through
unicellular free-living phases as amoebae (phagotrophic phase without a cell wall),
fusing into multicellular pseudoplasmodia within the same protoplasm (propagation
phase). In favorable environments, they grow and live single-celled in isolation.
Under environmental stress (e.g., lack of food, unfavorable edaphoclimate), these
organisms change phase, aggregate by chemical signals, and form pseudoplasmodia
that have defined anterior and posterior parts, respond to light and temperature gra-
dients, and can migrate. Under appropriate conditions, mature pseudoplasmodia
form a fruiting body (20% of cells die to form it) carrying one or more spore clusters
(Raper, 1984; Kessin, 2001). Spores are released into the soil after programmed cell
death of the fruiting body (Baldauf & Doolittle, 1997).
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 151

The simplicity of the life cycle of Dictyostelium discoideum, its cell movement,
chemical signaling, and development apply to human cancer research, as well as
other genetic, cellular, and biochemical processes in other organisms (Williams
et al., 2006; Annesley & Fisher, 2009; Müller-Taubenberger et al., 2013; Pears &
Gross, 2021) (Fig. 5.5a). This species is a model for studying cell differentiation, as
different environmental factors or certain cell–cell interactions affect cell fate (Kay
et al., 1978). It is a marvelous organism for studying chemotaxis, so it is used as a
model in investigations of human inflammation, arthritis, asthma, lymphocyte traf-
ficking, and axon guidance (Hashimura et al., 2019; Pal et al., 2019). The use of
D. discoideum to study disease mechanisms and identify drug modes of action and
toxicological effects, especially during cell development, is increasing (Schaf et al.,
2019). It is also known that Dictyostelium can be infected with the bacteria
Legionella pneumophila (Hägele et al., 2000; Solomon et al., 2000) and Salmonella
typhimurium (Jia et al., 2009; Sillo et al., 2011), which has prompted its use as a
model host in biomedical studies (Clarke, 2010; Bozzaro & Eichinger, 2011;
Steinert, 2011) (Table 5.2).
It has been described that in colonies of D. discoideum, there is a “primitive
breeding” behavior (Brock et al., 2011) of symbiotic bacteria within the fruiting
bodies, an incredible example of evolutionary convergence concerning other agri-
cultural organisms (e.g., insects). In general, this species is a solitary predator of
bacteria by phagocytosis, even though these use strategies to avoid predation (Raper,
1937; Matz & Kjelleberg, 2005). However, some populations of D. discoideum have
been found to stop feeding and incorporate the bacteria into their fruiting body. The
“seeding” of bacteria at the site of spore dispersal is very advantageous in environ-
ments with few food resources (Brock et al., 2011). However, not all colonies per-
form this behavior because this practice carries associated costs: colonies that do
not consume all the bacteria produce smaller spores or have less dispersal capacity.
In addition, the benefit is much lower for spores containing bacteria that reach food-­
rich environments (Brock et al., 2011). Interestingly, they can also host bacteria, not
for cultivation, but are defensive symbionts to inhibit the growth of nonfarmer
strains of D. discoideum that might “prey” on other crops (Brock et al., 2013). This
illustrates that microbes are capable of being prudent in the use of resources for
future use, which may be important for microbial markets to evolve (Werner et al.,
2014). Furthermore, successful breeding appears to be a complex evolutionary
adaptation, as it requires additional strategies, such as acquiring other symbionts to
defend and “privatize” crops (Brock et al., 2013).
However, within their multiple particularities, these species have proven to be
unique with respect to their “sociality” (Raper, 1935). Cellular aggregation could be
considered analogous to a social group or a chimeric multicellular organism (i.e.,
mixing of two or more genetically distinct clones) and is vulnerable to internal con-
flict since a “social dilemma” appears regarding cell fate. The expected “social con-
tract” is that the frequency of each clone between the spores and the stem is the
same. If this is not the case, we can say that the dominant clone cheated the minority
clone by obtaining more representation in the spores, and cooperation can be put at
risk when cheaters gain an advantage (Strassmann et al., 2000; Buttery et al., 2009).
152 5 When THAT Exception Persists Almost as THAT Exception

a b

e
c d

e ff

Fig. 5.5 Examples of exceptional fungi. (a) Multicellular organism of Dictyostelium discoideum
under the microscope (Credits: Bruno in Columbus). (b) The saprobe Panellus stipticus displaying
bioluminescence (Credits: Ylem.). (c) Distribution of Chorioactis geaster. (d) Chorioactis geaster
after spore dispersal. (e) Fruiting bodies of Armillaria ostoyae on a dead tree. (f) Rhizomorphic
network of Armillaria spp (Credits: Henk Monster.)
(a) Dictyostelium discoideum. License: Public domain. https://commons.wikimedia.org/wiki/
File:Dictyostelium_Aggregation.JPG. (b) Panellus stipticus. License: Public domain. https://com-
mons.wikimedia.org/wiki/File:PanellusStipticusAug12_2009.jpg. (c) Chorioactis geaster distribu-
tion. (d) Chorioactis geaster. License: CC BY 3.0 https://creativecommons.org/licenses/by/3.0, via
Wikimedia Commons. https://commons.wikimedia.org/wiki/File:Devil%27s_cigar_Chorioactis_
geaster.jpg. (e) Armillaria ostoyae. License: Public domain. (f) Rizomorphen. License: CC BY 3.0
https://creativecommons.org/licenses/by/3.0, via Wikimedia Commons. https://commons.wiki-
media.org/wiki/File:Rhizomorphen_or_Mycelial_chords_(rizomorfen_of_%22schoenveters),_
mostly_from_the_Honey_mushroom_at_a_dead_poplar_at_Schellingwoude._-­_panoramio.jpg
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 153

Because of these advantages, altruism is not expected to be evolutionarily stable

(i.e., evolutionary pitfall), whereas the “cheating” strategy should become dominant
(Medina et al., 2019). In this case, although cheating occurs, it is greatly reduced by
various means, including high relatedness, kin recognition, pleiotropy, and other
mechanisms (Gilbert et al., 2007; Ostrowski et al., 2008; Buttery et al., 2012). This
system is ideal for studying the evolution of conflict versus cooperation or altruism
and the molecular study of social evolution (Strassmann & Queller, 2011).

Glowing Fungi

The emission of light by living organisms is a phenomenon known as biolumines-

cence, produced by a chemical reaction of the enzyme luciferase with oxygen and
the substrate luciferin, producing energy in the form of cold light. This phenomenon
is distributed in several animal phyla, although it is rarely reported in sessile organ-
isms. There are approximately 70 species of bioluminescent fungi (many of the
genus Mycena and Armillaria), so it could be considered an exception of the fungi
group, although it is a widespread phenomenon in almost 17 phyla (Desjardin et al.,
2008) (Fig. 5.5b). All fungi that are bioluminescent share the same enzymatic path-
ways, suggesting that the biochemical pathway to bioluminescence appeared early
in the evolution of mushroom-forming Agaricales (Oliveira et al., 2012). Although
rare, this phenomenon in fungi has attracted the attention of humans since antiquity.
More than two thousand years ago, Aristotle marveled at wood illuminated by what
he called a “cold fire” (fox fire). The natives of Meghalaya in India used mushrooms
as torches to not get lost in the forests. More than 100 years ago, naturalist George
Gardner, watching children playing in the streets of Brazil with giant fireflies,
noticed that they were mushrooms.
Fluorescing fungi emit green light with maximum intensity in the range of
520–530 nm (Chew et al., 2014) and can fluoresce in different parts, such as myce-
lia, fruiting bodies, or both, in rhizomorphs or spores (Herring, 1994; Weitz, 2004;
Moore et al., 2021). One of the proposed functions for the existence of biolumines-
cence has to do with attracting pollinators. Glow-in-the-dark fungi would have
evolved to attract nocturnal insects and thus ensure the dispersal of their spores
(Desjardin et al., 2008). Sivinski (1981) showed that more arthropods were attracted
to leaf litter with Mycena mycelium than to leaf litter without this fungus; this attrac-
tion was visual and did not involve chemical signals. Similarly, Oliveira et al. (2015)
demonstrated this in Neonothopanus gardneri in the Brazilian coconut forest using
plastic models of fungi with green LED-emitting light that attracted a wide variety
of insects. Surprisingly, this bioluminescence followed a circadian rhythm, causing
the mushrooms to “light up” at night (Oliveira et al., 2015).
Panellus stipticus is one of the brightest mushrooms in the world. Interestingly,
this species is distributed worldwide, but only some strains, specifically those from
North America, are bioluminescent. This species and other bioluminescent species
have been tested as bioindicators of environmental contamination to heavy metals
(such as Cd and Cu), as bioluminescence can be very sensitive to different chemical
154 5 When THAT Exception Persists Almost as THAT Exception

compounds in soil (Weitz et al., 2002; Mendes & Stevani, 2010; Stevani et al., 2013;
Prasher et al., 2014; Ventura et al., 2020). Light emission appeared to decrease
because these toxic compounds are related to the uncoupling of mitochondrial oxi-
dative phosphorylation, leading to impaired ATP synthesis (Ventura et al., 2020).
Although these lines of research are still under development, there is evidence that
bioluminescence in these fungi can be considered an interesting variable as a bioin-
dicator of environmental pollution (Soares et al., 2022) (Table 5.2).

An Unusual Distribution

The fungus of the species Chorioactis geaster, known as “devil’s cigar,” is consid-
ered one of the rarest on the planet (Rudy & Keller, 1996). It has a strange shape in
itself, as the fruiting body resembles a dark brown cigar and grows on dead roots of
elm, cedar, or oak trees. For dispersal of its spores, the fungus opens radially in a
star shape (Otani, 1980), exposing the hymenium (Seaver, 1937) accompanied by
the release of the spore cloud (hence its name cigar), which may be accompanied by
a distinctive hissing sound audible up to a considerable distance (Rudy & Keller,
1996) (Fig. 5.5d).
However, it is not its morphology that makes this species so peculiar but its
geographic distribution (Wolf & Wolf, 1947). We are faced here with a very par-
ticular spatial exception since the devil’s cigar is only found in two places, sepa-
rated by more than 10,000 km: in Texas (United States) (Seaver, 1937) and southern
Japan (Imazeki, 1938) (Fig. 5.5c). These two localities on opposite sides of the
globe are at similar latitudes with similar annual photoperiods. In 1939, mycologist
Fred Jay Seaver wrote: “It would be difficult indeed to account for [this distribu-
tion], and we merely accept the facts as they are.” Paradoxically, it is still unknown
why this fungus has such an unusually disjunct distribution. Comparisons of the
genomes of the Texas and Japanese populations showed divergence approximately
19 million years ago, revealing that the colonization of the new habitat was not
related to Homo sapiens (Peterson et al., 2004). Meanwhile, due to deforestation
and replacing oak with cedar trees, the devil’s cigar is considered an endangered
species in Japan.

The Oregon Monster

Few would imagine that when asked about the largest organism on the planet, the
answer would be a fungus (Smith et al., 1992). However, with an extension of 9 km2,
weighing 650 tons (Stanosz et al., 1987) and glowing at night, the fungus known as
“the Oregon monster” (Armillaria gallica) occupies a large portion of the forests of
this state. This fungus has even become a tourist attraction in Michigan. This organ-
ism spreads its filaments or rhizomorphs (root-like multicellular structures of clonal
dispersal) through the root structure of coniferous forests, bridging its host plants,
as it is, in fact, a parasite (Baumgartner et al., 2011) (Fig. 5.5e, f). The expansion
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 155

and stability of these environments have allowed the colonization and growth of this
fungus between 2400 and 8650 years old. Rhizomorphs develop subways by aggre-
gation and coordinated parallel growth of hyphae occupying the surrounding soil
and colonizing new food resources (Heinzelmann et al., 2019). Rhizomorphs grow
1 meter per year and perform long-distance nutrient uptake and translocation func-
tions (Morrison, 1975; Baumgartner et al., 2011). The form of dispersal and patho-
genicity is unique to this species, involving ancestral genetic toolkits for wood
decay, morphogenesis, and complex multicellularity (Sipos et al., 2017).
Some of the extraordinary qualities of this fungal species have led scientists to
ask how these long-lived organisms can keep deleterious mutations to a minimum
during somatic growth. Very low genetic variations (≅3 orders of magnitude lower
than most filamentous fungi) and a very low mutation rate have been reported, mak-
ing the genome of this fungus highly stable (Aanen, 2014; Anderson & Catona,
2014; Anderson et al., 2018). The number of cell divisions is thought to be reduced,
and growth is similar to that of a plant shoot, with cell divisions occurring just
below the apex. This would reduce the number of new mutations in the apical zone,
preventing the accumulation of mutations in the population (Anderson & Catona,
2014). Most astonishingly, the “Oregon monster” characteristics could be useful in
fighting cancer (Han et al., 2009; Chen et al., 2016). In addition to the extremely low
mutation rate, Armillaria species could exhibit inherent resistance to DNA damage.
Studying the genetic mechanisms underlying this stability in the genome could pro-
vide potential new ways to treat cancer (Table 5.2).

5.4.1.8 Carnivore Plants: Exceptions in the Group Show Us

the Carnivore Rule

When we consider plants, we think of autotrophic and photosynthetic organisms,

which transform inorganic matter from the environment into organic molecules and
do not require the intervention of other organisms to obtain their energy (a rule I for
the plant kingdom) (Curtis et al., 2008). This definition is a great plant rule, but as
we saw above, some plants, such as parasitic plants, do not comply with this prem-
ise. Another exceptional example is carnivorous plants that acquire extra nutrients
from other organisms (heterotrophy), such as insects and even small vertebrates
(Adamec, 1997). The leaves of these plants have been modified to attract and trap
their prey, after which they absorb nutrients from the prey by producing enzymes or
digestive bacteria (Ellison, 2006; Barthlott et al., 2007) (Fig. 5.6a). These plants are
thought to have evolved this ability because they inhabit certain nutrient-poor soils,
especially nitrogen, such as acidic swampy soils and rocky bluffs (Feldman, 2009).
Some, such as pitcher plants (Nepenthaceae) and many Drosera, expect passive
prey, although they have intricate slippery edges and sticky-tipped hairs to secure
insects (Darwin, 1875; Juniper et al., 1989). Others are more active, such as certain
droseras that coil up, pushing prey into the sticky center of the trap, and others have
an outer ring of fast-moving tentacles, the most sophisticated being the Venus fly-
trap (Dionaea muscipula), of which we will discuss later.
156 5 When THAT Exception Persists Almost as THAT Exception

Murderous Plants Strange as Fiction

These plants have attracted the attention of botanists and ecologists for more than
200 years who have been trying to obtain answers about how these unique organ-
isms evolve and how their anatomy works. Charles Darwin wrote the first known
treatise on these plants in 1875 after spending more than 15 years studying them
with fascination. He wrote to Charles Lyell in the late 1860s about a species of
Drosera: “...at this present moment I care more about Drosera than the origin of all
the species in the world… Is it not curious that a plant should be far more sensitive
to a touch than any nerve in the human body!’. In his autobiography, he wrote: “The
fact that a plant should secrete, when properly excited, a fluid containing an acid
and ferment, closely analogous to the digestive fluid of an animal, was certainly a
remarkable discovery.” For Darwin, carnivorous plants were one of the most critical
points of evolutionary theory (Fig. 5.6c).
However, just as these “plant monsters” inspired Darwin’s fascination, they were
long considered by the popular imagination to be “killer” plants. These man-eating
plants appeared regularly in Anglo-American fictional accounts in the late nine-
teenth century, perpetuating pseudoscientific stories of explorers encountering hor-
rors such as the “man-eating tree” of Madagascar or the “vampiric vine” of Namibia
(Prior, 1939) (Fig. 5.6b). Sir Arthur Conan Doyle fanned this fiction by publishing
“The American’s Tale” (1880), a story in which an enormous Venus flytrap killed a
man in the forests of Arizona. Additionally, H.G. Wells wrote about a “blood-­
sucking orchid” laying the groundwork for the man-eating plants appearing in
future musical, film, and television adaptations in the twentieth century (Price,
2013). Interestingly, ideas and fables about killer plants began to emerge after
Darwin popularized them with his treatise on these wonderful (and harmless) plants.

A Molecular Recipe Behind the Evolution of Carnivory

The carnivorous habit has evolved in at least 12 lineages independently (more than
a dozen genera in 5 families and 810 species, so it is considered an example of
morphological convergence) (Albert et al., 1992; Givnish, 2015; Fleischmann
et al., 2018) (Fig. 5.6a). In each of these times, the evolutionary force that led to
carnivory seems to have been the need to find alternative sources of vital nutrients
such as nitrogen and phosphorus that they could not extract from the soil. The
amazing thing is that this exceptional adaptation follows the same “recipe” or
“rule” in all carnivorous plants! (Hedrich & Fukushima, 2021). The leaves of these
plants have acquired new enzymatic functions: chitinases (digest chitin, the main
component of the insect exoskeleton), proteases (breakdown proteins), and acid
phosphatases (release phosphate groups from molecules and help mobilize phos-
phorus from prey). The production and control of these enzymes are genetically
regulated and are acquired by a genetic phenomenon of co-option, where certain
genes that these plants already had to adapt to these new functions, somewhat like
a genetic “recycling” (Pavlovič & Saganová, 2015; Bemm et al., 2016; Pavlovič &
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 157

a b

c d

Fig. 5.6 Rare in the plant world: carnivorous plants. (a) Phylogenetic positions and trap types of
carnivorous plants. Carnivorous plants evolved multiple times across the angiosperm lineage
(modified from Hedrich & Fukushima, 2021). (b) Sacrificed to a man-­eating plant (from Buel,
1887). (c) Selected image of the insectivorous plant Drosera rotundifolia described by Darwin
(from Darwin, 1875). (d) A plant bug on a Pinguicula gigantea (Credits: Noah Elhardt).
(a) Phylogenetic positions and trap types of carnivorous plants. (b) Sacrificed to a man-
eating plant. License: CC BY 4.0. https://creativecommons.org/licenses/by/4.0. https://com-
mons.wikimedia.org/wiki/File:The_ya-te-veo.jpg (c) Selected image of the insectivorous plant
Drosera rotundifolia. License: Public domain. https://commons.wikimedia.org/wiki/File:C._
Darwin,_Insectivorous_Plants_Wellcome_L0031429.jpg. (d) Selected image of the insectivo-
rous plant Drosera rotundifolia. License: Public domain. https://commons.wikimedia.org/wiki/
File:Pinguicula_gigantea_ne.jpg
158 5 When THAT Exception Persists Almost as THAT Exception

Mithöfer, 2019). These genes were initially involved in immune defense or stress
response (jasmonate defense response), so they could be considered a case of exa-
ptation (Bemm et al., 2016; Fukushima et al., 2017). The genes for these enzymes
were reused when plants started to eat the organisms from which they were origi-
nally protected. Certain stimuli given by prey consumption increase the level of
jasmonates, which transcriptionally activate the genes encoding digestive enzymes
(Bemm et al., 2016; Yilamujiang et al., 2016; Pavlovič et al., 2017; Jakšová
et al., 2020).
Digestion by prey enzymes is the first part of the process, as the plant must then
transport these nutrients into the plant interior. In a typical plant, nutrients are trans-
ported through root transporter proteins. However, it has been recently discovered
that the Venus flytrap possesses these transporter proteins in its modified leaves
(Scherzer et al., 2013). Root genes were also co-opted to work at new sites, although
these transporters are only activated upon uptake in the traps, whereas in the roots,
they are always active. Co-optation appears to have originated from mutations
related to fixed gene duplications because they were adaptive (Ibarra-Laclette et al.,
2013; Palfalvi et al., 2020).

Vegetarian Carnivorous Plants

Gene co-option appears to be shared by many species; however, Kocáb et al. (2020)
investigated the carnivorous butterwort Pinguicula sp., a small, herbaceous, rosette-­
like plant that uses sticky leaves with sticky mucilage to attack insects (Fig. 5.6d).
The glands of this species would be like “sacs” that would undergo a type of autoph-
agy and discharge enzymes onto prey, unlike the more precise mechanism of
jasmonate-­ mediated digestive enzyme expression and secretion in carnivorous
plants of the order Caryophyllales (Heslop-Harrison & Knox, 1971; Heslop-­
Harrison & Heslop-Harrison, 1980). Kocáb et al. (2020) found that enzyme produc-
tion in Pinguicula does not appear to be regulated by the jasmonate pathway.
Instead, they found alpha-amylase in its digestive fluid, which is unique among
carnivorous plants.
Amylase is an enzyme that catalyzes the hydrolysis of starch, a polysaccharide
produced by green plants as an energy store. The rosette shape of Pinguicula would
serve to trap quite a bit of plant material (Darwin, 1875), and amylases can help
digest this alternative carbon source (mixotrophic organism). This “vegetarianism”
has been described for some Utricularia species (Peroutka et al., 2008; Koller-­
Peroutka et al., 2015), although until now, this compound has not been found in
digestive fluids. This discovery could mean that other genes unrelated to defense
have been coopted on the way to carnivory, although the mechanism triggering
enzyme secretion remains a mystery.
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 159

5.4.2 Extraordinary Phenomena

5.4.2.1 Exceptions from the World of Deception

One fascinating phenomenon that often surprises us is the remarkable similarities

observed among distantly related groups, be it in terms of morphology, behavior, or
physiology. Evolutionary convergences have long captivated biologists, even before
the times of Darwin himself. It was through his work that we started developing and
organizing our understanding of shared ancestry, distinguishing between homolo-
gies and analogies, and exploring the occurrence of multiple convergences within a
clade. In this context, some species deviate entirely from the typical pattern or rule
of a taxon to “resemble” other organisms or environmental characteristics (camou-
flage), to go unnoticed, or to obtain some kind of advantage to ensure their survival.
This remarkable capability is referred to as mimicry and encompasses various
forms, such as aposematism, Batesian mimicry, and Müllerian mimicry. It is exem-
plified by iconic species such as the chameleon, stick insects, caterpillars that mimic
branches or imitate the appearance of small snakes, butterflies that seamlessly blend
with tree trunks, and seahorses whose bodies mimic the texture of algae. In Table 5.3,
several examples are listed, with a summary of their main phenotypic characteris-
tics, the percentage of mimetic species concerning their clade, and references. These
examples have at least a couple of aspects in common: (1) they mimic something of
the phenotype of a taxonomic group distantly related to them and (2) they are
numerical rarities compared to the rest of the large clade that contains them. It is
intriguing to integrate the investigation of mimicry cases, encompassing the descrip-
tion of mimicry itself, its associated behavioral ecology, and phylogeny, to gain a
comprehensive understanding of its adaptive significance. Furthermore, with the
progress of developmental biology, it becomes increasingly valuable to explore the
ontogeny of mimicry in individuals displaying this trait.

Beetles That Mimic Ants

Army ants are ecologically dominant predatory insects in the tropics, with large
nomadic colonies harboring a great diversity of parasitic myrmecophiles (i.e.,
organisms living in association with ants) (Rettenmeyer et al., 2011). An interesting
case of mimicry is that of the army ant-parasitic rove beetles (Coleoptera). These
organisms, known as ant-mimics, closely resemble their ant counterparts in terms of
body shape (e.g., petiolate abdomen, geniculate antennae, and highly elongated
legs) and behavior. In fact, they mimic the ants so well that they are readily accepted
by the aggressive ants, joining their colonies and temporarily inhabiting their nests.
These ant-mimics not only feed alongside the ant workers but also consume the
workers’ offspring (Akre & Rettenmeyer, 1966; Parker, 2016) (Fig. 5.7a, b). What
is curious is that this phenomenon is not limited to a single species of staphylinid.
Instead, multiple unrelated groups of ant-mimics within the subfamily Aleocharinae
have independently developed this distinctive pattern at least 12 times (Maruyama
Table 5.3 Selected examples of mimetic species and models for mimicry, indicating the type of mimicry, the mimetic sex and trait, and the signal nature and
160

receiver
Mimetic species Vulgar Mimetic Signal
(signaler) name Model species Vulgar name sex Type of mimetism Mimetic trait Signal reciever nature
Automimicry, Browerian mimicry, Bakerian mimicry, or intraspecific mimicry: the same species of animal is imitated; (a) weakly defended members
of a species with warning coloration are parasitic on more strongly defended members of their species, mimicking them to provide the negative
reinforcement learning needed for warning signals to function; (b) a less vulnerable part of an animal’s body resembles a more vulnerable part, providing
an immediate selective advantage; (c) decieve prey so that it perceives that the attack is originating from where it is not (confounding effect); (d)
intersexual mimicry occurs when individuals of one sex in a species mimic members of the opposite sex to facilitate sneak mating
Chaetodon capistratus Foureye Chaetodon Foureye Both Automimicry Deceptive Body colors Predators Visual
butterflyfish capistratus butterflyfish (b) mimicry (ocelli)
Charina bottae, Rubber boa Charina Rubber boa Both Automimicry Deceptive Shape of Predators, Visual
Hydrophis pachycercos bottae, (b, c) mimicry tail-like head preys
Hydrophis
pachycercos
Danaus plexippus Monarch Danaus Monarch Both Automimicry Deceptive Warning Predators Visual
butterfly plexippus butterfly (a) mimicry coloration
Paracerceis sculpta Marine Paracerceis Marine isopod Males Automimicry Deceptive Color and Males Visual
isopod sculpta (beta, (d) mimicry shape
(female and gamma)
juveniles)
Subfamily Theclinae Hairstreak Subfamily Hairstreak Both Automimicry Deceptive Shape of Predators Visual
butterflies Theclinae butterflies (b) mimicry wing tail as
antenna
Uta stansburiana Common Uta Common Males Automimicry Deceptive Color, Males Visual,
side- stansburiana side-blotched (d) mimicry behavior tactile
blotched (female) lizards
lizards
5 When THAT Exception Persists Almost as THAT Exception
 5.4

Aggressive mimicry: copying by a predator or parasitic species of the appearance of another harmless species, in order to disguise its nature and have easy
access to its prey or host. The model suffers costs from being mimicked, due to the erosion of signal reliability and costs of being parasitized. Therefore,
host phenotypes evolve toward increased discriminability from their parasites. *Pouyannian mimicry: flowers mimic a potential female mate visually, but
the key stimuli are often chemical and tactile
Acherontia atropos Death’s- Honey bees colonies Both Aggressive Deceptive Epicuticular Prey Chemical
head mimicry mimicry lipid pattern
hawkmoth of the host
Anomalospiza imberbis Cuckoo- Prinia subflava Tawny- Female Aggressive Deceptive Egg color Host Visual
finch flanked prinia mimicry mimicry
Carrion flowers, corpse flowers Rotting flesh Both Aggressive Deceptive Color, shape, Pollinator Visual,
mimicry mimicry odor (necrophagous chemical,
(Pouyannian) (chemicals) insects) tactile
Chlorobalius Spotted Tribe Cicadas Both Aggressive Deceptive Song, Prey (males) Visual,
leucoviridis predatory Cicadettini mimicry mimicry behavior Acoustic
katydid (sexual)
(males)
Cuculus canorus Common Several Passeriformes species Female Aggressive Deceptive Egg color Host Visual
cuckoo mimicry mimicry
Drakaea spp. Hammer Female wasp Both Aggressive Deceptive visual and Pollinator Visual,
orchid mimicry mimicry olfactory (male wasps) chemical
(Pouyannian) cues.
Epipactis helleborine Broad- Cabbage leaves infested with Both Aggressive Deceptive Odor Pollinator Chemical
Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies

leaved caterpillars mimicry mimicry (chemicals: (social wasps)

helleborine (Pouyannian) green-leaf
orchid volatiles)
Hedychrum rutilans Cuckoo Philanthus European Female Aggressive Deceptive Composition Prey Chemical
wasps triangulum beewolf mimicry mimicry of cuticular
compound
(continued)
161
Table 5.3 (continued)
162

Mimetic species Vulgar Mimetic Signal

(signaler) name Model species Vulgar name sex Type of mimetism Mimetic trait Signal reciever nature
Hymenopus coronatus Malaysian Orchid flowers Both Aggressive Deceptive Color Prey Visual
orchid mimicry mimicry
mantis
Lanius excubitor great grey Several small Passeriformes Both Aggressive Deceptive Song Prey Acoustic
shrike species mimicry mimicry
Macrochelys temminckii alligator Worms Both Aggressive Deceptive Shape, Prey Visual
snapping mimicry mimicry movement
turtle
Mastophora hutchinsoni Bolas spider Moth species Both Aggressive Deceptive Sex Prey (males) Chemical
mimicry mimicry pheromone
of prey
Misumena vatia Crab spider Flowers Both Aggressive Deceptive Color Prey Visual
mimicry mimicry
Phengaris arion Large blue Myrmica Red ant Both Aggressive Deceptive Chemical Host, Prey Chemical,
sabuleti (larvae) mimicry mimicry compounds Acoustic
and sound
Photuris spp. Fireflies Photuris spp. Fireflies Female Aggressive Deceptive Visual light Prey (males) Visual
mimicry mimicry displays
Plagiotremus Bluestriped Labroides Bluestreak Both Aggressive Deceptive Body colors, Prey Visual
rhinorhynchos fangblenny dimidiatus cleaner wrasse mimicry mimicry behavior
(juvenile)
Stenolemus bituberus Assassin Prey of web-building spiders Both Aggressive Deceptive Vibrations Prey (spider) Vibrations
bug mimicry mimicry on spider
web
Stenoria analis Ivy bee Colletes Ivy bee Both Aggressive Deceptive Sex Host (male) Chemical
blister hederae (larvae) mimicry mimicry pheromone
beetle of host
5 When THAT Exception Persists Almost as THAT Exception
 5.4

Synemosyna formica Ant- Ants Both Aggressive Deceptive Shape, color Prey Visual
mimicking mimicry mimicry and behavior
jumping
spider
Volucella bombylans Hoverfly Bombus Red-tailed Both Aggressive Deceptive Shape, color Prey (larvae) Visual
bee lapidarius bumblebee mimicry mimicry and behavior
Batesian mimicry (defensive mimicry): an animal copies the appearance or behavior of a more dangerous or repugnant animal to discourage attacks by
predators. Models are predicted to benefit from evolving away from Batesian mimics because mimicry erodes signal reliability, which could reduce the
extent to which predators avoid the model
Chionactis occipitalis Northern Micrurus Coral snake Both Batesian Deceptive Body colors Predators Visual
shovel- fulvius mimicry mimicry
nosed snake
Cuculus spp. Cuckoo Accipiter nisus Eurasian Both Batesian Deceptive Shape, color, Predators Visual
species sparrowhawks mimicry mimicry behavior
Glaucidium Northern Eyes of a predator Both Batesian Deceptive Body colors Predator Visual
californicum pygmy owl mimicry mimicry (ocelli)
Lampropeltis elapsoides Scarlet king Micrurus Eastern coral Both Batesian Deceptive Body colors Predators Visual
snake fulvius snake mimicry mimicry
Laniocera hypopyrra Cinereous Megalopygidae caterpillars Both Batesian Deceptive Shape and Predators Visual
mourner (nestlings) mimicry mimicry color
Lycodon aulicus Indian Wolf Bungarus Common Both Batesian Deceptive Body colors Predators Visual
snake caeruleus Krait Snake mimicry mimicry
Onopordum sp., Arctium tomentosum Spider Web Both Batesian Deceptive Trichomes in Herbivores Visual,
Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies

mimicry mimicry stems and tactile

leave
Mycalesis patnia, Butterflies Eyes of a predator Both Batesian Deceptive Body colors Predator Visual
Caligo idomeneus, with ocelli mimicry mimicry (ocelli)
Haetera piera,
Hipparchia semele
(continued)
163
Table 5.3 (continued)
164

Mimetic species Vulgar Mimetic Signal

(signaler) name Model species Vulgar name sex Type of mimetism Mimetic trait Signal reciever nature
Papilio polytes Common Pachliopta Common rose Both Batesian Deceptive Shape and Predators Visual
mormon aristolochiae, butterfly, mimicry mimicry color
Atrophaneura red-bodied
polyphontes swallowtails
Thaumoctopus mimicus Mimic Various marine animals Both Batesian Deceptive Shape, color Predators Visual
octopus mimicry mimicry and behavior
Batesian food-source mimicry: in floral mimicry, rewardless flowers attract their pollinators through dishonest signaling of a resource. Rewardless flowers
mimic the morphology, color, and/or scent of rewarding flowers
Arisaema sikokianum Japanese Mushrooms Both Batesian Honest Chemical Pollinator Chemical
Jack-in-the- food-source mimicry compounds (mushroom-
pulpit mimicry associated
flies)
Dracula spp. Drac orchid Mushrooms Both Batesian Deceptive Chemical Pollinator Chemical
food-source mimicry compounds (mushroom-
mimicry associated
flies)
Epidendrum ibaguense Epiphytic Asclepias Tropical Both Batesian Deceptive Flower shape Pollinator Visual
orchid curassavica milkweed food-source mimicry and color (Agraulis
mimicry vanillae)
5 When THAT Exception Persists Almost as THAT Exception
 5.4

Müllerian mimicry (defensive mimicry): this is a collaborative mimicry where species with the same defense mechanism (bad taste, poison, etc.) and the
same predator develop a similar appearance to ensure greater survival. The predator will eat a single individual of either species and in the future will learn
to avoid them both
Apheloria spp. Millipedes Brachoria Millipedes Both Müllerian Honest Body colors Predator Visual
cedra mimicry mimicry
Danaus plexippus Monarch Limenitis Viceroy Both Müllerian Honest Body colors Predator Visual
butterfly archippus butterfly mimicry mimicry
Euploea core Common Other toxic butterflies Both Müllerian Honest Body colors Predator Visual
crow mimicry mimicry
butterfly
Heliconius erato Red passion Heliconius Postman Both Müllerian Honest Body colors Predator Visual
flower melpomene butterfly mimicry mimicry
butterfly
Morpho peleides Blue Other blue butterflies Both Müllerian Honest Body colors Predator Visual
morpho mimicry mimicry
butterfly
Pitohui dichrous Hooded Pitohui Southern Both Müllerian Honest Body colors Predator Visual
pitohui uropygialis variable mimicry mimicry
pitohui
Ranitomeya imitator Amazonian Dendrobatidae Poison dart Both Müllerian Honest Body colors Predator Visual
mimic frogs mimicry mimicry
poison frog
Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies
165
166 5 When THAT Exception Persists Almost as THAT Exception

a b

c d

e f

Fig. 5.7 The extraordinary world of mimicry. (a) Aleocharinae free-living beetle Athetavaga sp.
(from Pentinsaari et al., 2019). (b) Army ant social parasites of Aleocharinae with myrmecoid
morphology (Pseudomimeciton sp.). (c) Sea snake (Laticauda colubrina) mimicked by octopus.
(Credits: Christian Gloor). (d) Octopus (Thaumoctopus mimicus) mimicking a sea snake. (Credits:
Elias Levy.). (e–f) Mimetic fungus Leratiomyces erythrocephalus mimicking truffles of New
Zealand (Credits: Bernard Spragg; F. Tony Wills).
(a) Athetavaga sp. License: CC BY 4.0 https://creativecommons.org/licenses/by/4.0, via
Wikimedia Commons. (b) Pseudomimeciton sp. License: Public domain. https://commons.wiki-
media.org/w/index.php?search=Pseudomimeciton+&title=Special:MediaSearch&go=Go&type=i
mage. (c) Laticauda colubrina. License: CC BY 2.0. https://creativecommons.org/licenses/by/2.0,
via Wikimedia Commons. https://commons.wikimedia.org/wiki/File:Laticauda_colubrina_
(27567428624).jpg. (d) Thaumoctopus mimicus. License: CC BY 2.0. https://creativecommons.
org/licenses/by/2.0, via Wikimedia https://commons.wikimedia.org/wiki/File:Mimic_Octopus_
(14280646758).jpg. (e) Leratiomyces erythrocephalus. License: Public domain, via Wikimedia
Commons. https://commons.wikimedia.org/wiki/File:Scarlet_Pouch_Leratiomyces_erythroceph-
alus_(52149653411).jpg. (f) Leratiomyces erythrocephalus. License: CC BY 2.5 https://creative-
commons.org/licenses/by/2.5, via Wikimedia Commons. https://commons.wikimedia.org/wiki/
File:Red_pouch_fungus_01.jpg
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 167

& Parker, 2017). Each independent clade is restricted to one zoogeographic region
and is highly specific to a single ant genus. This could be an intermediate-type
exception involving several species. However, considering the number of mimetic
beetles throughout the order, it is clear that we are still dealing with a strategy that
remains rare at the taxonomic level. However, mimicry generally involves a highly
complex system of morpho-behavioral modifications. In the case mentioned, these
changes occurred in diverse groups and at different points in time. Natural selection
would have played a great role since it can hardly be argued that it resulted from a
mere evolutionary convergence phenomenon.

Cephalopods as Masters of Camouflage

Octopuses, in particular, have an exceptional defensive system and are considered

“masters of camouflage.” Camouflaging is one of the most iconic examples of their
behavioral flexibility. Their nervous system allows them to mimic their environment
and to make extremely rapid changes in color and skin texture (Messenger, 2001)
(Fig. 5.7c, d). They present pigment cells in the mantle called chromatophores that
possess pigments that expand or condense using muscle contractions controlled by
the nervous system (Messenger, 2001; Hanlon & Messenger, 2018). In addition,
cephalopods can modify their strategies according to substrate and predator type
(Langridge et al., 2007; Josef et al., 2012; Staudinger et al., 2013). For example, cut-
tlefishes may change coloration when facing visual predators but opt for flight strate-
gies when dealing with predators that use chemical signals (Langridge et al., 2007).

Mushrooms That Look Like Berries

Fungal spores are primarily dispersed through anemochory, where the wind carries
lightweight spores over significant distances. However, alternative methods of dis-
persal exist, including consumption by mammals, as seen in the case of truffles.
Truffle-like fungi have rare and even unique forms of dispersal within the fungal
world. The species Leratiomyces erythrocephalus grows in Australia and New
Zealand, possessing a vivid red fruiting body with a “pouch” shape on a delicate
stalk (Fig. 5.7e, f). These mushrooms mimic red berries, and in these geographic
areas, they are believed to visually attract birds rather than attract mammals by
smell (Medway, 2000). Because they closely resemble berries, these fungi are dis-
persed by birds over long distances and benefit from their nitrogenous resources in
the digestive system.

Defensive Masquerade in Plants

As we have seen above, plant variegation could be considered teratology or chro-

matic aberration. Variegation involves a photosynthetic loss for the plant and has
negative consequences. However, it has been found that in Caladium
168 5 When THAT Exception Persists Almost as THAT Exception

steudneriifolium, it could be a defensive strategy or a form of “masquerading” (i.e.,

organisms assimilate to inanimate or inedible objects in their environment)
(Skelhorn, 2015). Leaf-mining moths frequently attack these plants, and some indi-
viduals have been found to develop variegated patterns similar to the damage pro-
duced by these insects to avoid further moth visits (Soltau et al., 2009). These
authors painted nonvariegated leaves by copying the variegated patterns and found
that within three months, these leaves were significantly less frequently damaged by
moths than healthy leaves (Soltau et al., 2009). Moths were found to infest almost
10% of nonvariegated leaves, whereas they only mined approximately 2% of varie-
gated leaves (Soltau et al., 2009). These herbivores may avoid leaves with visible
markings, implying that damage-mimicry may reduce oviposition, consistent with
the mimicry hypothesis (Smith, 1986; Lev-Yadun et al., 2002). Interestingly, in the
populations where this variegation was found, there are also nonvariegated indi-
viduals, so it would seem that both morphs could be successful and maintained in
the population (Smith, 1986; Soltau et al., 2009).

5.4.2.2 Strange Forms of Pollination

In angiosperms, pollination is the process by which pollen is transferred from the

stamens to the stigma of the flowers, where it germinates and fertilizes the flower’s
ovules with the consequent production of seeds, fruits, and a new generation of
plants. As we will see in detail in Chap. 6, this ecological process is of utmost
importance in the evolution of flowering plants and typically involves a vector
responsible for transport that can be biotic or abiotic (Kay & Sargent, 2009; Willmer,
2011). Pollen transfer can take place via wind (anemophilous) or water (hydrophi-
lous), but in the vast majority of plants, it takes place by pollinating animals (zooph-
ilous). In general, animals (e.g., butterflies, bees, hummingbirds, bats, mammals)
seek to feed on the nectar and pollen of flowers, and in doing so, they become
impregnated with the pollen that they carry to other flowers.
Darwin greatly contributed to this fascinating topic by studying orchids, their
varied forms, and the relationship of these patterns with the interaction of pollina-
tors (Darwin, 1862, 1877; Micheneau et al., 2009). Orchids present unique flowers
that attract suitable pollinators for each species, being frequent examples of plant–
insect coevolution. An iconic example discussed above was the moth predicted by
Darwin when studying the Madagascar orchid Angraecum sesquipedale, which had
a spur of more than 30 cm long with nectar only in its basal part. This unique mor-
phology led Darwin to conclude that there must be a nocturnal moth with a long
proboscis capable of releasing this nectar. It was not until 1903, more than 40 years
later, that the moth with a 30 cm long proboscis was discovered: Xanthopan morga-
nii praedicta, whose subspecific epithet alludes to Darwin’s prediction of its exis-
tence. The case of the predicted moth is an example of the morphospaces imagined
but not found (at that time). It is interesting how exceptional morphologies could be
predicted from other coevolution examples.
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 169

“(…) I must say a few words on the Angraecum sesquipedale (…). A whip-like
green nectary of astonishing length hangs down beneath the labellum. (…) We shall,
I think, see that the fertilization of the plant depends on this length and on nectar
being contained only within the lower and attenuated extremity. It is, however, sur-
prising that any insect should be able to reach the nectar: (…) in Madagascar there
must be moths with probosces capable of extension to a length of between ten and
eleven inches”—Charles Darwin, 1862

Pollinators Not as Ridiculous as Previously Assumed

Pollination by snails and slugs is known as malacophily and is considered one of the
rarest forms of pollination (Abrol, 2012) since these animals feed on soft vegetation
and floral organs and are more likely to inhibit pollination than to promote it. Many
researchers consider malacophily to be “notorious and obscure” (Faegri & van der
Pijl, 1979) or even “ridiculous” (Atwood Jr., 1982). However, although infrequent,
some cases of malacophily are known (Pammel & King, 1930; Sarma et al., 2007;
Tandon & Ram, 2010; Abrol, 2012; Raju et al., 2014; Gardère, 2018). Plants gener-
ally grow in clusters, and flowers possess nonprotruding stigmas and anthers, which
allows snails or slugs to crawl over the flowers, take up pollen, and deposit it on
adjacent stigmas (Pammel & King, 1930). Strictly malacophilous plants have not
been documented, although Evolvulus nummularius plants, for example, use snails
(Lamellaxis gracile) as supplementary pollinators to bees (Sarma et al., 2007). Even
on rainy days, snails are exclusive pollinators (Sarma et al., 2007). More recently,
Raju et al. (2014) reported that Euplecta subdecussata pollinated Ipomoea pes-­
caprae during the flowering season, moving between flowers without damaging the
style or stigma, being an essential pollinator and affecting self and cross-pollination.
In this species, bees and wasps are pollinators, but snails are equally crucial as these
insects (Raju et al., 2014).

Underwater Pollination

Unlike in terrestrial environments, animals do not participate in pollination under

the sea (Vermeij & Grosberg, 2010). As a result, hydrophily is common to these
plants and is considered a particular and near-exclusive adaptation of plants to life
in the marine habitat. These plants usually have small, inconspicuous male flowers
that release large numbers of pollen grains that drift into the water, where the large,
feathery stigmas of the female flowers catch them. Hydrophily occurs in only 14 of
the 14,000 genera of angiosperms, and 10 of these genera occur in marine environ-
ments (Ackerman, 2006). In the large group of flowering plants, hydrophilia could
be considered a rarity, although it would be the rule for aquatic plants. However, a
group of aquatic angiosperms presents a different form of pollination, being, in turn,
a rarity among those of their group. As we saw in the case of schizomids, this could
be a chain of exceptions and rules within a group.
170 5 When THAT Exception Persists Almost as THAT Exception

Flowering plants in the marine environment are known as seagrasses and are
generally hydrophilic (Cox, 1988; Ackerman, 2006). Flowers are ephemeral, female
flowers have tentacle-like stigmas, and male flowers produce copious filiform or
spherical pollen released in mucilage strands (Cox, 1988; Ackerman, 2006).
However, the species known as turtle grass (Thalassia testudinum) can be consid-
ered an exception because, in addition to being hydrophilic, complementarily, its
flowers are pollinated by marine invertebrates (zoobenthophily) (van Tussenbroek
et al., 2012, 2016). These invertebrates, during the night, visit the flowers and trans-
port and transfer the pollen-encrusted mucilage masses from male flowers to the
stigmas of female flowers, and in turn, this pollen would be a food reward for these
pollinators (van Tussenbroek et al., 2016). Like insect pollination, pollination by
marine invertebrate fauna may have played a role in the transition from terrestrial to
underwater abiotic pollination by water flow (van Tussenbroek et al., 2016).
These findings in seagrasses have prompted research on pollination in other
marine organisms. Recently, the red algal species Gracilaria gracilis has been
observed in symbiosis or mutualism with the marine isopod species Idotea balthica
(Lavaut et al., 2022). The result of this symbiosis is isopod-mediated pollination of
the algae, as biotic interactions dramatically increase the success of algal fertiliza-
tion through the transport of spermatozoa in the animal’s body. This is extremely
interesting because the female gametes are not released, and the male gametes are
not flagellated. This algal species would be ambophilous and could use both water
and the isopod as pollinators (Lavaut et al., 2022). The isopod also engages in a
double mutualism with the algae since it not only transports its pollen but also
removes it by foraging epiphytic algae growing on the red algae (Ollerton & Ren,
2022). It appears that the symbiosis between the alga and the isopod was established
approximately 300 million years ago. However, the alga is much older, and it is
thought that perhaps pollination at that time was only water-mediated or perhaps by
some other organism that we do not know about (Ollerton & Ren, 2022). This find-
ing suggests that animal-mediated fertilization may have evolved independently in
terrestrial and marine environments and raises the possibility of its appearance in
the sea before plants moved onto land.

Intermediary Pollinators of “Armed” Plants

It is believed that plants, due to their immobility and lack of sensory perception, are
not able to physically compete for reproductive opportunities (male–male competi-
tion) (Willson, 1990; Andersson, 1994; Arnold, 1994; Skogsmyr & Lankinen, 2002;
Delph & Ashman, 2006). However, direct physical competition between individuals
has been described in milkweeds (Oxypetalinae) during pollination (Cocucci et al.,
2014) (Fig. 5.8a). In these species, large amounts of pollen aggregate in two pollinia
connected by sterile accessory structures, forming a complex pollinarium (Harder
& Johnson, 2008; Wiemer et al., 2012) (Fig. 5.8b). At the time pollinating insects
visit the flowers, a process of “concatenation” occurs, where a pollinarium can join
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 171

a b

c d

Fig. 5.8 A strange case of pollination. (a) Morrenia odorata (Familia Apocynaceae). (b–d)
Pollinaria and pollinators of Morrenia odorata (Credits: Cody H.)
Credits: (a) Morrenia odorata. License: CC BY 2.0 https://creativecommons.org/licenses/
by/2.0, via Wikimedia Commons. https://commons.wikimedia.org/wiki/File:Morrenia_odorata_
(Hook._%26_Arn.)_Lindl.jpg. (b–d) Pollinaria and pollinators of Morrenia odorata License:
Author permission

others already present on the pollinator (Coombs et al., 2012) (Fig. 5.8c, d).
Interestingly, pollinaria have evolved “horn-like” structures to physically compete
with other pollinaria to gain a “privileged” place on the pollinator’s body, as it
would be advantageous to prevent new pollinaria from chaining together.
These horns would be botanical equivalents of the horns in many male verte-
brates, and the reproductive performance of a pollinarium depends on its position in
a chain, which in turn will depend on the characteristics of the horns of those pol-
linaria (Cocucci et al., 2014). In the phylogeny of Oxypetalinae, horns were signifi-
cantly associated with loss of concatenation, whereas the loss of horns caused a
return to concatenation (Cocucci et al., 2014). If horns are experimentally removed
in Oxypetalum solanoides, pollinaria are reattached, whereby horns are evolution-
arily acquired or lost to avoid or promote concatenations (Cocucci et al., 2014).
172 5 When THAT Exception Persists Almost as THAT Exception

These studies suggest that self-propulsion and well-developed sensory percep-

tion are not necessary for sexual selection through intrasexual competition to take
place (Cocucci et al., 2014). Only physical contact would be sufficient to influence
competitors’ reproductive success and promote the evolution of defensive and
attack weaponry. Due to a scientific tradition, some research questions are more
studied or considered more important in some taxa than others (Lankinen &
Karlsson Green, 2015). With this in mind, we wonder if these “exceptional” cases
are truly exceptional or if they represent a bias in studies of sexual selection or
search for trait explanations in plants. What is clear is that fields such as botany
could benefit greatly by incorporating and testing the impact of selective pressures
generated by sexual selection and sexual conflict (Lankinen & Karlsson Green,
2015). Furthermore, the fact that there are intermediary “mediators” or “agents”
such as pollinators that have coevolved with plants provides a new perspective to
enrich studies of sexual selection in plants.

5.4.2.3 Reproductive Biology: Source of Valuable “Exceptions” at

the Evolutionary Level

Reproductive biology is a field that exhibits numerous remarkable exceptions across

morphology, behavior, and physiology. As we will see below, we discover that many
of the so-called “exceptions” have become more like “cryptic” rules, perhaps not
visible to the inexpert eye. This evolution stems partly from the profound influence
of sexual selection on various reproductive traits and the continuous progress and
evolving perspectives within the field (the example of how the real and widespread
existence of monogamy in birds was relativized made it clear that these compart-
ments of “rules” and “exceptions” in reproductive biology can be relatively weak).
However, here, we will highlight some considerations regarding evolutionarily
maintained minorities or extraordinary exceptions at the morphological and behav-
ioral level, although we will also emphasize some phenomena that may be more
common than we think.

Minorities That Remain: Alternative and Conditional Sexual Strategies

A context in which minorities can have an important evolutionary value is when we

refer to tactics or strategies adopted by a part of the population. A strategy is the
decision-making rules involved in certain reproductive behaviors. Individuals allo-
cate resources to one or another (mutually exclusive) strategy to achieve the same
functional end (Brockmann, 2001). These strategies can be alternative, conditional,
or mixed (Gross, 1996; Taborsky et al., 2008). In the case of alternative reproductive
tactics (ARTs), there is genetic polymorphism, with the same fitness for morphs
given by frequency-dependent selection (i.e., a tactic is more successful when it is
rarer but less successful when it is more common). Under strong selective pressures,
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 173

for example, small males at a disadvantage in physical fights with other males or
display against females adopt ARTs (Oliveira et al., 2008). This selective pressure
sets the stage for the disruptive selection of morphologies (i.e., morphs) (Gadgil,
1972) or behaviors. There are numerous cases of these reproductive strategies. In
these cases, we can consider that alternative tactics will not always be represented
in equal frequency of occurrence in a given species or population of the same spe-
cies. In some cases, the occurrence of “morphs” does not have a behavioral correla-
tion, so it is necessary to be cautious with speculations about alternative strategies.
On the other hand, conditional strategies involve individuals’ decisions based on
the context or state of the individuals who optimize their fitness. The organisms are
genetically monomorphic, and the fitnesses of the strategies are not the same (but
the fitnesses of the alternatives at the switch point are equal). A well-known exam-
ple is that of dung beetles of the genus Onthophagus that can exhibit a fighting or
sneaking phenotype as adults depending on the body size that is determined by
larval feeding (Emlen, 1994; Moczek & Emlen, 2000; Hunt & Simmons, 2001)
(Fig. 5.9a). Adult body size distribution is discontinuous, reflecting different devel-
opmental trajectories (Eberhard & Gutiérrez, 1991). Switch points can be sensitive
to ecological and demographic events (Eadie & Fryxell, 1992; Reynolds et al.,
1993; Carroll & Corneli, 1995). For example, in addition to body size, population
density affects the success of alternative tactics (fighter and nonfighter male pheno-
types) (Radwan, 1993).
Individuals of the alternative male morph are usually called “sneakers,” and in
many cases, they do not invest in “armament” but rather in other adaptations to
maximize fertilization (e.g., gonadal investment, sperm number, etc.) (Taborsky,
1998; Simmons et al., 1999). Because copulations of females with sneaker males
and with males of the main morph (e.g., territorial, fighting, older) are common, it
is frequent that ejaculates from both males compete for egg fertilization (Parker,
1990; Simmons, 2001). The example of male sneakers is very illustrative of ignor-
ing or neglecting a less noticed phenomenon, such as sperm competition, either
because of its range in conspicuousness to the bias of our sensory universe or its
frequency of occurrence. This changed with the advancement of the conceptual
framework of sexual conflict and postcopulatory sexual selection, under which tac-
tics of copulation and sperm competition were more readily identified and inter-
preted in an evolutionary framework (Gross, 1982, 1985). Nor is it appropriate to
take lower frequency tactics or strategies as the main pattern of a species, perhaps
because they are so conspicuous. For example, it would be a mistake to overesti-
mate a minority alternative or conditional strategy as the main pattern (Peretti &
Córdoba-Aguilar, 2007).
In numerous instances, the origins of these strategies, whether they are alterna-
tive, conditional, minor, or even exceedingly rare, remain elusive. They may repre-
sent minority strategies today, but no one knows if they may represent the norm in
the future. Many of them may represent differences at the genetic level or pheno-
typic plasticity of the trait we are analyzing, which could well form the tipping point
for future evolutionary strategies of these types. There is much to be discovered in
174 5 When THAT Exception Persists Almost as THAT Exception

a b

c d

Fig. 5.9 Uncommon and incredible examples in the world of animal reproduction. (a) Examples
of alternative male morphs in Onthophagus taurus (top) and O. nigriventris (bottom). Large males
are shown on the left and small males on the right (from Kijimoto et al., 2013). (b) Homosexuality
in kudu males. (Credits: Brian Ralphs.) (c) A male Kobudai (Semicossyphus reticulatus) in Japan.
In this species the females have the ability to turn into males, an example of a transgender fish.
(Credits: Cinz) (d) Egg-­carrying male of Ibalonius sp. with magnification of egg clutches (from
Sharma et al., 2017)
Credits: (a) License: Used with permission granted by the publisher on 04 January 2023. (b)
License: CC BY 2.0. https://creativecommons.org/licenses/by/2.0, via Wikimedia Commons.
https://commons.wikimedia.org/wiki/File:BVR_8158_(33817940031).jpg. (c) License: CC BY
2.0. https://creativecommons.org/licenses/by/2.0, via Wikimedia Commons. https://commons.
wikimedia.org/wiki/File:Semicossyphus_reticulatus.jpg. (d) License: used with permission
granted by the publisher on January 4, 2023.

the world of reproductive strategies, but it will be challenging if we do not reinforce

the focus on rare extreme cases or outliers as the basis for them. In other words, if
we always wait for them to appear to a minimal but remarkable degree to be consid-
ered in our studies, we are missing the beginning of everything. The beginning of
life may have been marked by something like this, rarities that later became regular,
as we have already mentioned and will see in the following chapters in detail.
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 175

Animal Homosexuality

Homosexuality can be regarded as an exceptional occurrence when compared to the

overall number of heterosexual individuals within a species with a dioecious repro-
ductive system (Thornhill & Alcock, 1983; Maklakov & Bonduriansky, 2009).
However, there are an increasing number of species where cases of homosexuality
are reported, so we wondered whether this phenomenon could become a rule (Bailey
& Zuk, 2009; Poiani, 2010) (Fig. 5.9b). In other words, it is not the pattern, the norm
(although here, this word runs the risk of falling into the anthropological in terms of
normal versus abnormal from the “moral” point of view, which we will not debate
in this book). Strict homosexuality is limited to humans, domesticated sheep, and
other unconfirmed species (Munévar, 2014). However, more than 1,500 species of
animals present “atypical” sexual practices such as mating with individuals of the
same sex between males (e.g., lions, giraffes, bison, dolphins, and elephants),
females (e.g., seagulls, koalas, lizards, birds, beetles), bisexual behaviors (e.g.,
bonobos, bats), and long-term homosexual relationships (e.g., penguins, alba-
trosses) (Munévar, 2014).
Cases of homosexual behaviors have also been reported in animals taxonomi-
cally far from vertebrates, such as insects (e.g., fruit flies, weevils, seed and flour
beetles, damselflies, field crickets) (McRobert & Tompkins, 1988; Castro et al.,
1994; Harari et al., 2000; Van Gossum et al., 2005b; Bailey & French, 2012; Scharf
& Martin, 2013; Olivero & Robillard, 2017) and arachnids (e.g., spiders, pseudo-
scorpions) (Scharf & Martin, 2013; R. Palen Pietri, pers. comm.) in more or less
detail. Sometimes up to 50% of male mating attempts are directed at other males
(Aiken, 1981; Serrano et al., 1991, 2000). At present, it is more often the case that
“strange” reports of homosexuality can still be found in these groups, but these are
increasingly embedded in an evolutionary context (Scharf & Martin, 2013). For
example, YouTube videos have reported that a male of the cricket Xenogryllus mar-
moratus has mounted another male (Olivero & Robillard, 2017). In this case, the
male appears to be pretending to be a female in order to consume a nutritious glan-
dular secretion from the other male when mounting him (generally in this species
the female mounts the male). In many insect species, the explanation for these
behaviors has to do with recognition failures, lack of experience, or benefits of
increased overall mating frequency to males (Thornhill & Alcock, 1983; Serrano
et al., 1991, 2000; Harari et al., 2000; Switzer et al., 2004; Scharf & Martin, 2013).
The phenomenon of homosexuality has been cited or studied tentatively since
the eighteenth century by George Edwards, who sought the causes of the “abnor-
mal” behaviors he saw in birds and attributed them to captivity (Sommer & Vasey,
2006). Darwin himself made some observations of behaviors between individuals
of the same sex, although he was evasive in his explanations of them, describing
them as superficial and transitory (Brooks, 2021). For example, when faced with
birds courting same-sex individuals after the loss of a mate, he said: “How is it that
so many birds are ready immediately to replace a lost mate? Magpies, jays, carrion-­
crows, partridges (...) offer at first sight the most perplexing case. But birds of the
same sex, although of course not truly paired, sometimes live in pairs or in small
176 5 When THAT Exception Persists Almost as THAT Exception

parties (...) With partridges two females have been known to live with one male, and
two males with one female. In all such cases, it is probable that the union would be
easily broken” (Darwin, 1871). In the years that followed, numerous observations of
homosexual behavior or intersexuality were reported as curiosities by various natu-
ralists. These observations in that historical context led to strong academic disputes,
such as the one that followed the publication of “Perversion sexuelle chez des
Coléoptères mâles” by the French entomologist Henri Gadeau de Kerville in 1896.
After several observations, Gadeau asserted the existence of a “homosexual instinct,”
which led to heated debate and detailed studies of the behavior of these insects
(Brooks, 2009, 2021).
Classical interpretations attribute these behaviors to failures in recognizing the
other sex, although gradually, the study of animal homosexuality has gone from
being a simple “curiosity” to becoming more relevant because of its socioecological
implications. In this context, with the publication of the controversial but challeng-
ing book “Evolution’s Rainbow” by Joan Roughgarden in 2004, this topic was dis-
cussed concerning sexual diversity in nature, including men, from a more “social”
perspective within biology. Roughgarden illustrates multiple and fascinating exam-
ples within the animal kingdom and from cultures beyond occidental ones, showing
a “range” of options in terms of sexuality, which the author analyzes as a natural
variation. In this framework, it is necessary to look not only subjectively but also
objectively at homosexuality more broadly and more integrated with the social
aspects of the species. Evaluating homosexuality with a precise approach, free of
prejudices, is difficult, and the attempts made thus far are inconsistent in their
results.
In recent decades, evidence has begun to accumulate that homosexuality is a
behavior that arises primarily from biological or genetic factors (although there is a
role for environmental factors in the expression of a homosexual phenotype) (Pillard
& Bailey, 1998; Swaab, 2008; Bao & Swaab, 2010; Ganna et al., 2019). If faculta-
tive homosexual organisms reproduce at a lower rate than heterosexual organisms,
how can the maintenance of homosexuality be explained? This question is what
makes the issue of homosexuality an “evolutionary puzzle” or known as “Darwin’s
paradox” since it supposedly contradicts the theory of evolution by implying sexual
behavior without reproductive purposes, or at least it is adaptive value not immedi-
ately apparent (Gavrilets & Rice, 2006; Bailey & Zuk, 2009; Poiani, 2010). There
are multiple hypotheses to explain the evolution and maintenance of homosexuality,
and many are not mutually exclusive (Sommer & Vasey, 2006; Bailey & Zuk, 2009;
Dukas, 2010; Poiani, 2010). Among these are kin selection (i.e., the reproductive
success of relatives who might pass on the genes for homosexuality is encouraged),
genetic overdominance (i.e., a heterozygous version of a gene provides an organism
with some reproductive advantage), maternal effects (i.e., the fetus is influenced by
the environment of the mother’s womb, leading to changes that predispose to homo-
sexuality), and antagonistic sexual selection (i.e., genes are spread through a popu-
lation giving a reproductive advantage to one sex and disadvantaging another, e.g.,
the mother may increase her fertility at the expense of her child’s ability to procre-
ate). There is also evidence in birds and mammals that homosexuality can be a form
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 177

of “practice” for juveniles and a way to maintain alliances within social groups
(Sommer & Vasey, 2006; Bailey & Zuk, 2009). Of course, the causes and conse-
quences of homosexuality can vary greatly among species and contexts, although
genetic studies in model organisms have helped to understand common patterns in
the evolution of this phenomenon (Bailey & Zuk, 2009). As we previously stated,
particularly in humans, we must be very cautious with the search for explanations
for homosexuality, and here, it is argued that sexual orientation is the product of a
relationship between human biology and the sociocultural environment and that
many times the cultural meaning of sexual orientation surpasses biological explana-
tions (Roughgarden, 2004; Alonso, 2014, Ganna et al., 2019; but see Hamer et al.,
2021; Ganna et al., 2019).

On Female Andromorph Dragonflies

Color polymorphism (i.e., the presence of two or more genetically determined color
morphs within a population) is widespread in diverse taxa, such as fish, mammals,
birds, and insects (Roulin, 2004). When polymorphisms are observed in a single sex
(intrasexual), their evolution and maintenance are explained by sexual conflict
(Schluter, 2001; Roulin, 2004; Svensson et al., 2009) or by differences in immuno-
competence (i.e., different morphs adapt to environments with different exposures
to parasites, leading to differential resistance to parasites) (Roulin, 2004; McKinnon
& Pierotti, 2010; Sánchez-Guillén et al., 2013). As mentioned above, these poly-
morphisms are maintained by frequency-dependent negative selection (Bots et al.,
2015). Among insects, odonates in particular are characterized by color polymor-
phism, especially in females. (Fincke et al., 2005). Females usually show a “gyno-
chrome” morph (i.e., female coloration) and an “androchrome” morph (i.e., male
coloration). Females mimic males not only in coloration but also in some behaviors
(e.g., territoriality, aggressiveness) (Sherratt 2001; Robertson, 1985; Hinnekint,
1987; Cordero, 1992; Cordero & Pérez, 1998; Andrés et al., 2002; Sirot et al., 2003)
and even in other morphological traits (Abbott & Gosden, 2009). In this way, these
females remain relatively unnoticed, at least initially, avoiding sexual “harassment”
by males and minimizing the cost of unwanted mating and the risk of physical
injury. (Svensson et al., 2005; Takahashi & Watanabe, 2010; Takahashi et al., 2010;
Iserbyt et al., 2013). However, these females may suffer increased predation and
parasitism (Robertson, 1985; Svensson et al., 2005), as well as decreased fecundity
due to morphological changes (e.g., narrowing of the abdomen) (Gosden &
Svensson, 2009; Sánchez-Guillén et al., 2017). As an evolutionary response to this
confusion of the multiple morphs, males may develop a reversible preference for
mating and harassing the most common female type in the population (Van Gossum
et al., 2001).
The damselfly genus Ischnura has species with polymorphic females and is an
evolutionary and ecological model system for studying the selective forces that
maintain this polychromatism (Wellenreuther et al., 2014). This genus has females
with one androchrome morph and one or more gynochrome morphs controlled by
178 5 When THAT Exception Persists Almost as THAT Exception

three alleles with complete and hierarchical dominance (Sánchez-Guillén et al.,

2005). In this genus, Sánchez-Guillén et al. (2017) wondered whether these morphs
might signal different alternative reproductive tactics. These authors found that
behavior differed significantly between morphs but not within morphs, while in
males, the tactics were affected by the abundance of female morphs in the popula-
tion to avoid lost mating opportunities (Van Gossum et al., 2005a; Sánchez-­Guillén
et al., 2013, 2017).

Fluid Sex in Fish

Among the possible reproductive strategies, we find animals with “fluid sex,” i.e.,
that change sex under certain conditions (at the embryonic stage or as adults) (Avise
& Mank, 2009). Among fishes, 2% of species (approximately 500 species) exhibit
this phenomenon to some degree (Devlin & Nagahama, 2002; De Mitcheson & Liu,
2008; Avise & Mank, 2009). For example, the kobudai fish, Semicossyphus reticu-
latus, transforms from female to male (i.e., protogynous sequential hermaphrodite)
by increasing in size and bulbous forehead, developing testes and an aggressive
character (Ochi et al., 2017) (Fig. 5.9c). Others are more extreme, such as the angel-
fish Centropyge potteri, in which all fish begin life as females and all males were
once females (Bauer Jr & Bauer, 1981). Although less common, some fishes may
change from males to females (i.e., sequential protandric hermaphrodites), such as
the famous clownfish Amphiprion clarkii (Moyer & Nakazono, 1978). In these spe-
cies, a pair of reproductive females and males live together with subordinate nonre-
productive fishes inside sea anemones. When the dominant female dies, the larger
male becomes a female. These sex changes of both a protogynous and a protandrous
system seem to occur because of the “size advantage hypothesis,” as it would be
advantageous for some fishes to be of different sexes once they have reached a spe-
cific size (Ghiselin, 1969; Warner, 1975). Other species, such as gobies (Gobiodon
and Paragobiodon), can adopt both sexes depending on the circumstances (i.e.,
bidirectional hermaphrodites) (Nakashima et al., 1996; Munday et al., 1998; Cole &
Hoese, 2001). These species live in crevices within coral reefs, are poorly mobile
and have little opportunity to find mates. It is therefore an advantage that two fish
that meet by chance can form a pair regardless of their sex (Nakashima et al., 1996;
Munday et al., 1998).
These sex-switching strategies in fish testify to a remarkable plasticity in this
group of vertebrates, which is probably due to the great diversity of species adapted
to a variety of environments. These strategies would be highly adaptive, especially
in changing environments, as they would in many cases allow fish to double their
reproductive output (as both males and females) (Leonard, 2006). “Fluid sex” has
occurred several times in different fish families over the course of evolution, and
although a number of genetic and hormonal triggers come into play in all of them,
the one responsible for sex change would be the enzyme aromatase (Piferrer et al.,
1994). It is important to remember that temperature can determine sex in fish
(Conover & Kynard, 1981). This enzyme in particular is temperature sensitive and
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 179

can be activated or deactivated depending on the temperature (e.g., male develop-

ment is more frequent in warm waters) (Devlin & Nagahama, 2002; Uchida et al.,
2004; Ospina-Alvarez & Piferrer, 2008). In addition, certain chemical pollutants,
water acidity, and parasites, such as Wolbachia, affect aromatase in developing fish
embryos (Jobling et al., 1998; Kidd et al., 2007; Brown et al., 2015), which could
have serious consequences in a climate change scenario (Devlin & Nagahama,
2002; Ospina-Alvarez & Piferrer, 2008).

Speculating Behavior from Morphological Observations

When observing a “rarity,” it is important to be cautious in assessing its significance

and evolutionary or phylogenetic implications. This is particularly true when
attempting to predict specific behavioral patterns based on morphological observa-
tions, especially if those predicted behaviors are infrequent compared to the more
common behaviors within those groups. For example, if we never saw a butterfly fly,
could we claim that wings are for flight? Intuitively, we appeal to the comparison
with other animals that possess this trait, and therefore, from these “models,” we
deduce that since wings serve for flight, they most likely have the same function in
butterflies. The problem occurs when there are no models against which to compare
or when what exists is phylogenetically very distant, which makes extrapolation
between groups riskier. These extrapolations have occurred numerous times in the
history of ethology, and associations between traits and behaviors have been made
without direct observation. This has led to premature “paradigms” with implications
for phylogenetic interpretations in certain taxonomic groups. Remember the catego-
rization of Porifera, cnidarians, or fungi as plants in the past because many of them
are sessile.
An example that illustrates this topic comes from a very interesting group of
arachnids of the family Podoctidae, order Opiliones known as harvestmen. A char-
acteristic feature of this family is the males’ peculiar paternal care of the eggs
(Martens, 1993; Kury & Machado, 2003). In the vast majority of harvestmen, males
take care of the eggs deposited by females on substrates such as plant leaves, under
logs, or stones (Machado & Raimundo, 2001; Machado & Macías-Ordóñez, 2007).
However, the difference and particularity presented by this family are that males
carry eggs attached (individually or grouped) to their hind legs. This was reported
long ago (Martens, 1993) and echoed by other authors as a unique case among har-
vestmen (Tallamy, 2001; Kury & Machado, 2003; Requena et al., 2014). In an evo-
lutionary context, this showed an interesting convergence with other arthropods,
such as insects, such as water bugs, where males carry the eggs laid by the insemi-
nated female on their dorsum (Munguía-Steyer et al., 2019; Ohba, 2019), or other
chelicerates, such as pycnogonids (Lee & Kim, 2020).
We had a case of a rarity from the perspective of the order Opiliones and arach-
nids in general and even in an arthropod context. In that “relative” perspective, this
may be considered a rarity or exception (i.e., the rule would be that when there is
egg care, this occurs on an “extrabodily” substrate). However, in these harvestmen,
180 5 When THAT Exception Persists Almost as THAT Exception

there are no observations or studies describing female egg-laying behavior in this

male body zone or behavior where the male picks up eggs from the substrate. There
is no “direct” evidence that the eggs are from harvestmen. Unexpectedly and as part
of a molecular phylogenetic study of this family of harvestmen, a DNA analysis of
these eggs indicated that they did not belong to harvestmen but to spiders (Sharma
et al., 2017) (Fig. 5.9d). The publication of this study sparked a substantial debate
between the authors and proponents of the paternal care hypothesis, such as
Machado & Wolff (2018), regarding the presence of eggs in this particular male
body zone. Machado and Wolf base their arguments on knowledge of the morphol-
ogy, behavior, and specific characteristics of both harvestmen and spiders. Against
this, Sharma et al. (2018) performed new and more detailed DNA analyses and
reconfirmed that the eggs belonged to spiders and not harvestmen. This debate
seems to be still ongoing and highlights the relative importance of different sources
and methodologies to sustain specific hypotheses and postulates. We must be cau-
tious in inferring a particular behavior from a trait that would “indicate” or “sug-
gest” it.

5.4.3 Evolutionary and Ecological Exceptions

5.4.3.1 Evolutionary Simplification

O’Malley et al. (2016) reviewed the situation of increasing complexity in living

organisms, evaluating the role of simplification (e.g., morphological, physiological,
etc.) in macroevolution. These authors emphasize that simplification should be con-
sidered together with complexification in the generation of macroevolutionary pat-
terns. The evolutionary importance of simplification is evident in several eukaryotic
taxa, including protists adapted to parasitism, in addition to algae, plants (e.g., by
loss of the flagellum), and metazoan animals (O’Malley et al., 2016). We could
draw an association between some examples of simplification and exceptional cases
in biology since this simplification process can generate true rarities.

How To Be a Good Parasite?

In groups with parasitism, a simplification or organic reduction is common, leading

to the loss of genes, characteristics, and/or functions essential for survival outside
the host. An example of simplification could be the loss of photosynthetic capacity
that led to the emergence of particular groups of eukaryotes. Particularly notable are
some parasites derived from green algae, which do not photosynthesize and parasit-
ize insects (Blouin & Lane, 2012; Pombert et al., 2014). One of the best-known
cases is the apicomplexan protist Plasmodium, which is vectored by mosquitoes and
hosted by humans, causing Malaria disease. This apicomplexan has plastids (apico-
plast) derived from red algae (McFadden et al., 1996; Kohler et al., 1997). In
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 181

particular, the evolution of the parasite lifestyle is associated with a genomic reduc-
tion with a loss of functions no longer necessary in their novel environment.
Surprisingly, some parasites, such as Helicosporidium derived from green algae,
undergo some nuclear genome reduction, but most ancestral metabolic functions are
retained, including some photosynthesis-related functions, such as those of the
Calvin cycle. While some gene families lost complexity, others, such as those asso-
ciated with chitinases, expanded in response to parasitism. Helicosporidium repre-
sents an example of a transition from an autotrophic to a heterotrophic parasitic
organism where certain functions independent of the new lifestyle are preserved
(Pombert et al., 2014).
Another example linked to parasitism occurs in insects within the superfamily of
dipteran Hippoboscoidea, which contains tsetse flies (Glossinidae), louse flies
(Hippoboscidae), and two families of bat flies (Streblidae and Nycteribiidae).
Except for tsetse flies that are free-living and contact their host during feeding, all
hypobioscids are highly specialized obligate ectoparasitic flies that spend all or
most of their adult lives on their hosts. Several species, particularly within the bat
parasites of the family Nycteribiidae, are notable for their simplified morphologies,
which are extreme specializations of their life form. These flies are similar to spi-
ders, with completely reduced wings, dorsoventrally flattened thorax, and dorsally
inserted legs. Because of these simplifications and “extreme” modifications, homol-
ogy determination has been extremely difficult, and phylogenetic relationships
based on morphology have been almost impossible to elucidate (Petersen
et al., 2007).
Taken together, all these examples highlight how the path of simplification to
become a “good parasite” would be a common evolutionary process, as a “rule,” in
groups that are phylogenetically very distant from each other. However, we again
encounter the “paradox” of a chain of exceptions and rules. With the exception of
having reduced morphologies, we find the rule, which would be a “common” way
in parasites. However, returning to the last example, if morphological simplification
is beneficial for parasitism (Andersen, 1997), why are not all species of
Hippoboscoidea apterous? This is because extreme simplification may entail certain
costs, which in this case would have to do with the dispersal of the organisms. As
we said, Nycteribiidae species parasitize bats that, in general, have gregarious hab-
its, and this is why more than 50% of the species of this family could have faced this
extreme simplification since dispersal could be achieved in the same way due to the
proximity between individuals (Petersen et al., 2007).

On De-evolution and When the Simple Deceives Us

Another interesting example occurs in geckos, where an innovation such as the

adhesive system suffers a secondary loss or simplification. This may sound counter-
intuitive since many structural innovations have enabled many animal groups’
diversification and ecological specialization, so why lose it? (Hale, 1996; Garber &
Rehg, 1999; Zippel et al., 1999). Sometimes, however, the simplification or loss of
182 5 When THAT Exception Persists Almost as THAT Exception

these innovations can be even more advantageous (Wiens & Slingluff, 2001; Bejder
& Hall, 2002; Skinner et al., 2008). In geckos, the adhesive system evolved inde-
pendently at least 11 times, allowing these organisms to occupy inaccessible regions
due to increased climbing effectiveness (Autumn & Peattie, 2002). However, the
adhesive system appears to have been simplified or lost at least nine times (Gamble
et al., 2012). This could be due to certain constraints imposed by these adhesive
structures to run, making these organisms much slower (Russell & Higham, 2009).
Higham et al. (2014) found that the rate of morphological evolution was higher for
gecko species that had lost or simplified their adhesive systems, so these species
appear to have overcome these constraints. The African gecko lineages of
Phyllodactylidae suffered morphological simplifications in their adhesive systems
associated with a shift from a rupicolous lifestyle to burrowing in loose sand (Lamb
& Bauer, 2006; Gamble et al., 2012).
Interestingly, sometimes these “simplifications” resulted in derived morpholo-
gies different from the ancestral states without the character, such as Chondrodactylus
angulifer, which lost the adhesive system but retained structures such as tendons,
muscles, and associated skeleton (Lamb & Bauer, 2006; Johnson & Russell, 2009).
The “at first sight” morphological simplifications turned out to be reductions of
functionally integrated modules rather than dissolutions of them (Von Dassow &
Munro, 1999). This interesting pattern of secondary loss leading to derived mor-
phologies that are not necessarily “simpler” can be framed in what is known as
Dollo’s law (Law of Phylogenetic Irreversibility or the Law of Irreversible Evolution)
(Dollo, 1893; Gould, 1970). This law states that “an organism never returns exactly
to a former state, even if it finds itself placed in conditions of existence identical to
those in which it has previously lived... it always keeps some trace of the intermedi-
ate stages through which it has passed” (Gould, 1970). A well-known example is
the loss in many animals, including humans, of gulonolactone oxidase, the final
enzyme in the vitamin C biosynthetic pathway, necessitating its exogenous supple-
mentation (Chaudhuri & Chatterjee, 1969; Nishikimi et al., 1994; Cui et al., 2011).
During vertebrate evolution, many species lost gulonolactone oxidase enzyme-­
encoding genes, never reverting to ancestral gene expression states (Yang, 2013).
Phylogenetic reconstructions generally follow parsimony methods, and relation-
ships can be reconstructed by “Dollo parsimony,” i.e., making it impossible to revert
to ancestral states after losses (Quesne, 1974; Farris, 1977; but see Fitch, 1971).
However, as we have stressed repeatedly in this book, there are no absolutes, and
all rules have their exceptions. In the case of this law, there are examples where
structures appear to have effectively “reverted” to “simpler” character states. An
iconic case occurs in certain gastropods that have lost their spiral shell to be replaced
by limpet-like morphology (Collin & Cipriani, 2003). Genera of the family
Calyptraeidae (Trochita, Sigapatella, and Zegalerus) appear to have recovered a
coiled shell from limpet morphologies (Pagel, 2004). Although it could be argued
that these gastropods have evolved a different type of coiling from their coiled
ancestor, Collin & Cipriani (2003) hypothesize that the genes responsible for coil-
ing were silenced and that the genetic architecture was maintained by pleiotropy, as
has been proposed in other examples (West-Eberhard, 2003; Whiting et al., 2003;
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 183

Wiens et al., 2007; Lynch & Wagner, 2010; Lynch, 2022). Many of these species
have larval stages with spiral shells (Collin, 2003), so the expression of genes
involved in spiralization may have been maintained and “reactivated” in adult stages
as a form of heterochrony. This juvenilization would indicate that the “spiral shell”
state that could be considered “more complex” is simpler since it involves the reten-
tion of juvenile stages (heterochrony) (Collin & Cipriani, 2003).

5.4.3.2 Exceptions at First Sight

“Nonanimal” Eyes

Initially, photoreceptor structures were considered exclusively animal characteris-

tics, although we will see some exceptions. Eye structures in the form of spots are
considered the simplest form of photoreception. These are known as “eye spots”
and are formed by specific photoreceptor proteins and a signal transduction mecha-
nism that results in a photovoltaic-type response (Hegemann, 1997). Eye spots are
present in certain flagellated microorganisms and algae. We will return to the idea
of senses in plants in Chap. 6. One of the best-known examples of vision outside
animals is Euglena. This flagellate belonging to the phylum Euglenozoa is famous
for having both heterotrophic (via osmotrophy) and autotrophic (photosynthesis)
feeding facultatively, depending on the light conditions of the environment. The
more light there is, the more autotrophic feeding tends to occur.
Euglena has a red-­colored stigma or “eyespot” in its cytoplasm and is close to the
flagellum, which consists of a cell organelle made up of a concentration of carotenoid
pigment granules (flavoproteins). The function of the Euglena eyespot is to filter
sunlight falling on a light-detecting structure at the base of the flagellum (the parafla-
gellar body), allowing only certain wavelengths of light to reach it. In other words,
the eye spot is not a photoreceptor but a filter or selector of light waves. As the cell
rotates with respect to the light source, the eye spot partially blocks the source, allow-
ing Euglena to find the light and move toward it. In this case, there is positive photo-
taxis, but in other flagellates, it can be negative. Eye spots are also found in some
algae. For example, in Chlamydomonas, the eye spot is part of the chloroplast, and
the pigment is formed by rhodopsins (Suzuki et al., 2003). Kreimer (2009) refers to
the presence of eyespots in algae as constituting a “primordial visual system.”

Cave Dwellers: Blind Fish

The sensory world and how organisms process the information surrounding them is
a wonderful field of biology. Many species have adapted to specific environmental
conditions by showing drastic modifications of their phenotype regarding their sen-
sory organs and structures. Just as the appearance of a new sensory structure is
important in this context, the loss of sensory structures and/or their modification to
the minimum expression are also relevant. This occurs in many subterranean
184 5 When THAT Exception Persists Almost as THAT Exception

species of troglofauna (cavities and caves) and stygofauna (aquifers, underwater

caves, and fissures). Many species inhabiting these regions share characteristics
such as loss of vision and pigmentation and enhancement of other senses such as
hearing, touch, and smell (Chapman, 1982). Since the ideas of Lankester (1893),
who postulated that cave dwellers were descendants of eyeless mutants that had
become trapped and unable to leave the caves, much progress has been made in the
study of troglobitic species and the functional and evolutionary significance of their
morphological adaptations.
Examples could be blind cavefish, blind snakes, and moles. These animals are
taxonomically rare, standing out from the other species in their clade. If we focus on
fish, it is interesting to note that there are 111 species of blind fish out of 35000 total
species worldwide. A well-studied example is the Mexican tetra (Astyanax mexica-
nus), which has an epigean form (surface fish) and at least 30 populations of eyeless
hypogean forms (cavefish) (Jeffery, 2001, 2020). Therefore, they are considered
excellent models of parallel and convergent evolution. Current alternative hypothe-
ses suggest that adaptation to cave environments may have occurred either once or
multiple times during the evolutionary history of this species (Dowling et al., 2002).
The loss of eyes in cave populations has provided an excellent model for studying
the “plasticity-first” hypothesis. This suggests that previously hidden variations in
plastic responses may be exposed following the colonization of a new environment
in which different induced phenotypes are beneficial, thereby exposing this varia-
tion to selection and facilitating adaptive evolution. Indeed, the cave environment is
evolutionarily novel, and the populations that inhabit it are derived from surface
populations, in which vision was highly evolved. There is evidence that embryos
begin to develop eyes, but then this process stops, and a layer of skin develops over
the eye. On the other hand, another theory states that there is a disruption of genes
necessary for eye development that would then be maintained by neutral selection.
A very interesting experiment was conducted by Yamamoto & Jeffery (2000),
who transplanted crystallins from embryos of surface individuals into cave embryos
and vice versa. They found that the surface tetras failed to develop eyes, while the
cave forms could fully develop eyes. This would indicate that the lens of cave forms
produces signals indicative of eye degeneration (Yamamoto & Jeffery, 2000).
However, why do cavefish lenses undergo this “cell death”? Yamamoto et al. (2004)
seem to have found the answer by analyzing the expression of genes involved in
organ- and tissue-specific cell differentiation. These fish produce large amounts of
Sonic hedgehog (Shh) genes in the area that will become the head, leaving few (and
not enough) cells for eye formation (Yamamoto et al., 2004; Pottin et al., 2011). As
previously mentioned, the loss of specific morphological features or sensory abilities
in tetras may result in the acquisition of other traits. Among the losses, in addition to
vision and eyes, these fish had modifications and losses of melanin pigmentation,
heart regenerative capacity, changes in circadian rhythms, and social behaviors
(Jeffery, 2020). New traits included increased olfactory lobes, hypothalamus, jaws,
taste buds, teeth, neuromasts, and body fat. The trade-off between the loss of eyes and
the increase in other senses is controlled by Shh signaling, which is overexpressed in
the cave tetra form (Yamamoto et al., 2009; Pottin et al., 2011; Hinaux et al., 2016).
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 185

The Whites of Your Eyes Are More Unique Than You Think

“Don’t fire till you see the whites of their eyes!” was one of the most iconic phrases
supposedly exclaimed in June 1775 by Colonel William Prescott at the Battle of
Bunker Hill. On that occasion, the British army was approaching, and the American
militia had them in their sights, waiting until they were close enough to attack.
However, beyond the historical fact, we are concerned here with an interesting
issue, something that makes us unique among animals and that is precisely the
whites of our eyes. This portion of our eyes is known as the “sclera,” an opaque
protective layer that surrounds the eyeball, in addition to the transparent cornea at
the front of the eye. Humans are characterized by a white sclera, while most animals
have dark or iris-colored sclera (except for goats and crows) (Kobayashi &
Kohshima, 1997, 2001). In addition, humans have the highest proportion of exposed
sclerae in the eye contour, which is horizontally elongated (Kobayashi &
Kohshima, 1997).
However, why is this marked difference that makes us unique? It is thought that
the nonwhite sclera in most mammals may have evolved so that a flash of white
would not attract the attention of predators. The risk of predation may have decreased
with the evolution of increased body size and the use of tools and fire. Thus, in
humans, the white sclera may be an adaptation to expand the visual field by allow-
ing greater eye movement, especially in the horizontal direction, and to improve the
detection of the gaze direction of another individual (Kobayashi & Kohshima,
1997). This is known as the “cooperative eye hypothesis” (framed in the “gaze-­
signaling hypothesis”), which makes it easier to see in which direction we are look-
ing (Kobayashi & Kohshima, 2001; Tomasello et al., 2007; Kano et al., 2022). This
would be a fundamental part of nonverbal communication in humans, as the gaze is
used in many social activities, such as cooperation, teaching, and language learning
(Tomasello et al., 2007; Kano et al., 2022). This ability in our ancestors might have
been advantageous during hunts, where particular eye movements and gazes might
have been key to alerting other hunters to potential prey or dangers.
Eyes with white sclerae, on the other hand, are rare among other great apes
(Kobayashi & Kohshima, 2001). In general, great apes have dark sclerae that make
it difficult to locate the edge of their irises and, thus, to estimate their line of sight
(Kobayashi & Kohshima, 2001). This may be because their societies are less coop-
erative, and it is more important for them to hide the direction of their gaze from
others, for example, so that they do not reveal the location of food. The “gaze cam-
ouflage” hypothesis predicts that dark pigments serve to camouflage gaze direction
in competitive social environments. One study compared the reaction of nonhuman
apes and human infants to an experimenter’s head and eye movements, finding that
while human infants followed the experimenter’s gaze, apes only followed head
movements (Tomasello et al., 2007). In canids, for example, it has been found that
species that hunt in groups are more likely to have eyes with white sclera than soli-
tary ones.
On the other hand, the “self-domestication” hypothesis posits white sclerae as a
by-product of this process. During domestication, selection for tolerance and against
186 5 When THAT Exception Persists Almost as THAT Exception

aggression is linked to a reduction in the number and speed of migration of neural

crest cells in early embryogenesis (Wilkins et al., 2014). The melanocytes that color
the sclera are derived from neural crest cells, so reducing melanocytes in white
sclerae could be a by-product of selection for increased docility during domestica-
tion (Wilkins et al., 2014). Another theory explains the white coloring of the sclera
as a fundamental part of transmitting emotional signals in combination with the fine
musculature around the eyes (Jessen & Grossmann, 2014). It could also indicate the
health status of individuals through color variations (e.g., people associate yellow-
ish sclera as less healthy) (Provine et al., 2013a, 2013b). In one study, humans with
more reddish or yellowish sclerae were found to be rated as less healthy, attractive,
and less young (Provine et al., 2013a, 2013b). In addition, human adults and infants
show preferences for animals with white sclera (Segal et al., 2016). These hypoth-
eses are not mutually exclusive, and highly visible eyes may serve all or several of
these functions and have evolved under various selection pressures (Tomasello
et al., 2007; Mearing et al., 2022).

5.4.3.3 Value of “Rare” Species in Ecosystems

Due to significant levels of disturbance, many ecosystems are currently experienc-

ing what is widely recognized as the “sixth mass extinction” (Barnosky et al., 2011).
In this context, “rare” species are more vulnerable than widespread or abundant
species (Purvis et al., 2000; Davies et al., 2004; Sekercioglu et al., 2008). However,
what is the basis for considering a species as “rare”? It is important to clarify that
rarity is always context dependent, as rare species in one system may not be rare in
other geographically or temporally different systems (Lawler et al., 2003). There are
many ways to define rarity, but the most common are considering species with very
small population sizes, restricted geographic ranges, or narrow habitat or feeding
tolerances (Rabinowitz, 1981; Harnik et al., 2012) (Fig. 5.10a). Thus, rare species
have received attention in conservation biology, although little is known about the
functional consequences of their decline or extinction (Lyons et al., 2005).
Rarity can result from different processes, from stochastic processes to inherent
trade-offs in life-history strategies (Ai et al., 2013). In addition, rarity can be a con-
sequence of biotic and abiotic interactions. Highly specialized species with very
restricted environmental niches may be abundant in a few environments but rare in
many others. Alternatively, for example, noncompetitive species or species that
depend on the abundance of others (frequency-dependent selection) may remain
rare (Meyer & Kassen, 2007). In the second case, it is known that, for example, the
greater the frequency dependence of another species, the more persistent the rare
species will be (Yenni et al., 2012). Finally, rare species may arise and be main-
tained by abiotic changes, as they are known to be more sensitive to environmental
fluctuations and more prone to extinction (Gaston, 2008) (Fig. 5.10a).
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 187

Fig. 5.10 Species rare in their distribution and abundance and processes that generate these pat-
terns. (a) Potential mechanisms that can drive local rarity: (i, ii) mechanisms related to species
characteristics and (ii, iv) mechanisms related to local biotic and abiotic conditions (modified from
Jousset et al., 2017). (b) Geographically restricted species and species with small population sizes:
geographically restricted giant sequoia; Atlantic bluefin tuna is widespread but has a small popula-
tion size; giant panda and glandular bush-cricket are rare in number and are geographically
restricted (modified from Dee et al., 2019) (Bradyporus macrogaster. Image courtesy of Otto
Bylén Claess on)
(a) License: own creation. (b) Bradyporus Macrogaster: https://colombia.inaturalist.org/observa-
tions/119406275. License: Author permission. Bluefin tuna: License: Public domain. https://pixa-
bay.com/es/photos/pez-submarino-mar-oceano-agua-5999306/; Giant sequoia: License: Public
domain. https://pixabay.com/es/photos/secoya-secuoya-gigante-2406954/; Giant panda: License:
Public domain. https://www.pexels.com/es-es/foto/animal-pelo-fauna-mamifero-7619818/

The study of rare species can often lead to difficulties regarding the limited eco-
logical knowledge about them (Lyons et al., 2005). The commonness-dominance
paradigm argues that the focus on common species is justified because they possess
greater biomass and use more energy in communities (mass–ratio hypothesis)
(Grime, 1998). Meanwhile, rare species that use marginal resources or habitats play
a minimal role in ecosystems (resource availability hypothesis, Venier & Fahrig,
1996) (Gaston, 2011). However, multiple studies have found that rare species can
188 5 When THAT Exception Persists Almost as THAT Exception

have a significant value and contribute to various ecosystem services (Mouillot

et al., 2013; Jain et al., 2014; Leitão et al., 2016; Dee et al., 2019).

Ecosystem Services of Rare Species

The focus of conservation has broadened to protect the contributions that animals
and plants make to humans, known as “ecosystem services,” and it is known that
many rare species can provide these services (Dee et al., 2019). Rare species can
make significant contributions through their mere presence, regardless of their
abundance. This can be particularly evident in various experience contexts, such as
safaris, natural sightings, or visits to zoos (Booth et al., 2011; Daniel et al., 2012).
Additionally, rare species provide cultural services, fostering cultural identity, a
sense of place, and fulfilling iconic or spiritual roles, thereby holding relational
value (e.g., bald eagles Haliaeetus leucocephalus or the giant panda Ailuropoda
melanoleuca) (Garibaldi & Turner, 2004). Notably, they can also enhance biodiver-
sity in settings such as urban gardens (Ong et al., 2022). Paradoxically, other rare
species possess more “value” as they become rarer. In this case, humans value them
for being “unique” (Courchamp et al., 2006; Hall et al., 2008) as species harvested
for luxury goods (e.g., sturgeons for caviar, bluefin tuna) (Gault et al., 2008), ani-
mals targeted for trophy hunting (Palazy et al., 2012), used for traditional medicine
(e.g., rhino horns), ornamental species (e.g., orchids), or exotic pets (e.g., Banggai
cardinal fish) (Courchamp et al., 2006; Dee et al., 2019) (Fig. 5.10b).
In contrast, other rare species will provide greater services if they are more abun-
dant. This is the case for the Giant Sequoia Sequoiadendron giganteum, which is
geographically restricted but locally abundant and contributes greatly to its local
community services through carbon storage (Fauset et al., 2015). This case shows
that previously abundant and keystone species in their communities that suffered
declines or disappeared led to the loss of ecosystem structure and services. Due to
the introduction of a pathogen from Asia (Cryphonectria parasitica), the American
chestnut Castanea dentata, which was a foundation species in eastern North
American forests and which previously sequestered carbon and affected stream
hydrology, suffered a decline due to chestnut blight (Paillet, 2002; Ellison et al.,
2005). Fundamental ecosystem services (decomposition, nutrient cycling, produc-
tivity) changed drastically following chestnut replacement by other species, altering
terrestrial and aquatic processes. For example, in many cases, chestnut was replaced
by oak trees (Quercus spp.) with leaves with lower nutritional quality, which, when
falling into the water, produced a decline in leaf processing and consumption,
decreasing growth rates and adult body mass in macroinvertebrate shredder com-
munities (Ellison et al., 2005). We will return to the role of alien introductions and
species declines in Chaps. 6 and 7.
On the other hand, there are species that, despite being rare, contribute dispro-
portionately through indirect interspecific interactions, providing unique functional
roles or facilitating them (Lyons et al., 2005; Mouillot et al., 2013;
5.4 Unfolded Life Diversity: Some Rare Taxa and Amazing Strategies 189

Delgado-­Baquerizo et al., 2016; Jousset et al., 2017; Ziegler et al., 2018). For exam-
ple, some rare or threatened nitrogen-fixing species and their microbial mutualists
enhance soil fertility, which significantly benefits biomass production in nitrogen-
limited grasslands associated with higher biofuel yields (Leach & Givnish, 1996;
Tilman et al., 2006). Mouillot et al. (2013) studied the role of rare species and their
functional traits in ecosystems such as coral reef fishes, alpine plants, and tropical
trees. They found that rare species supported a diverse combination of functional
traits. In addition, rare species can stabilize food webs (O’Gorman et al., 2011),
reduce competition between service providers (Holt et al., 1994; Tilman et al.,
1997), or be keystone species or predatory species with disproportionate roles in
structuring communities (Lyons et al., 2005; Mouillot et al., 2013). This is the case
for rare sea otters (Enhydra lutris) in Aleutian kelp forests that limit the presence
and abundance of sea urchins, which indirectly increases kelp biomass and carbon
available for carbon storage (Estes et al., 1998; Wilmers et al., 2012).

Rare Species Loss Affects Functional Assemblages in Tropics

Leitão et al. (2016) conducted a study that explored the impact of the loss of rare
species in the tropics on the structure of functional assemblages (i.e., diversity and
distribution of functional traits). The tropics are characterized by numerous rare
species (Hercos et al., 2013; Hubbell, 2013), with a high rate of species extinction
(Brook et al., 2006). These authors found that several rare species support unique
roles in assemblages with common species, so their loss would be critical for the
functional structure of these communities, leading to declines in ecological pro-
cesses at both local and regional scales (Leitão et al., 2016). The effect they found
on the communities was disproportionately high, leading to a drastic decrease in
functional richness, specialization, and originality.
Surprisingly, these results were found in three taxonomic groups that are very dif-
ferent in terms of their ecology or evolutionary history. For example, the cassowary
Casuarius casuarius, classified as a vulnerable species by the International Union for
Conservation of Nature (IUCN), is considered rare, being the only large-­bodied dis-
perser of plants over long distances in Australian tropical rainforests. Its loss would
impact plant population dynamics and in turn, strongly affect the functional structure
of bird assemblages in the Australian Wet Tropics. Another example was the periph-
yton-grazing fishes, with superrestricted geographic ranges in small Amazonian
Forest streams. The importance of these fishes is key, as they are the only species
involved in the incorporation of carbon along the river continuum through the exploi-
tation of periphyton (complex mixture of algae, heterotrophic microbes, cyanobacte-
ria, and detritus attached to submerged surfaces in aquatic ecosystems).
The last example these authors addressed was that of the rainforest trees
Brosimum acutifolium and Protium giganteum from French Guiana. The first spe-
cies has leaves with a milky latex, associated with the ability to resist herbivores and
fungal infections. Protium giganteum has a particular bark that protects it from the
190 5 When THAT Exception Persists Almost as THAT Exception

wildfires that may occur in the region. These species provide resistance and resil-
ience to various disturbances and environmental fluctuations in the region. These
results allow us to conclude that beyond taxonomic or esthetic losses, the extinction
of rare species can result in the loss of irreplaceable functions, a decrease in ecologi-
cal niches in the communities, and a disruption of interactions between species,
drastically impacting the integrity of many ecological processes (Leitão et al., 2016).

The Rare Biosphere

In general, microbial communities are composed of a large number of rare species

(with low abundances), which is globally known as “the rare biosphere” (Sogin
et al., 2006; Skopina et al., 2016). Between 1.5 and 28% of all microbes are “condi-
tionally rare taxa” (Shade et al., 2014), meaning that under favorable conditions,
these species can disproportionately affect ecosystem functions such as biogeo-
chemical cycles (Falkowski et al., 2008; Lynch & Neufeld, 2015; Jousset et al.,
2017). Rare species are important in nutrient cycling, greenhouse gas emissions, and
pollutant degradation. They also prevent the invasion of new species by supporting
the structure of specific communities and stabilizing community functions in fluctu-
ating environments. Other rare microbes are essential in associations with plants and
animals, preventing infection by pathogens and stimulating host immunity (Jousset
et al., 2017). These microbes have diverse enzymes, some of which are key in indus-
trial processes, such as thermophilic cellulases for biofuel applications (Rubin,
2008). The rare biosphere is not exempt from the consequences of global climate
change and land-use alterations, so it is susceptible to these impacts and changes in
its ecosystem functions (Rodrigues et al., 2013). This is why the “rare biosphere” is
considered at the frontier of microbial ecology research (Jousset et al., 2017).
Microbial systems are characterized by high functional redundancy (Rousk
et al., 2009); that is, many species share similar functions, so rare species are not as
important in functional diversity. However, species that are not relevant in certain
conditions may be relevant in changing conditions, offering a pool of genetic
resources and providing necessary functions or facilitating particular interspecific
interactions (Shade et al., 2014; Fetzer et al., 2015). An interesting example is that
of microbial communities with a role in the degradation of organic compounds such
as pollutants. Removing rare species in activated sludge and freshwater dramati-
cally reduces the ability to degrade pollutants and toxins (Hernandez-Raquet et al.,
2013; Delgado-Baquerizo et al., 2016). On the other hand, the removal of rare spe-
cies in the soil can lead to an increase in new unwanted pathogenic species (Mallon
et al., 2015), which demonstrates the crucial role of rare species in biotechnological
applications such as crop protection (Xiong et al., 2021).
An example illustrating the importance of the rare biosphere is found in associa-
tions between corals and photosynthetic dinoflagellates (Symbiodinium spp.).
Although reef ecosystems cover a small percentage of the world’s oceans, nearly
one-third of the world’s marine biodiversity depends on their functional integrity
5.5 Key Concepts and Ideas in This Chapter 191

(Reaka-Kudla, 1997). Association with photosynthetic dinoflagellates is crucial in

coral reefs but in turn, possesses a high vulnerability to local stressors and the
effects of climate change (Hoegh-Guldberg et al., 2007) since ocean warming and
other impacts destroy coral–symbiodinium symbiosis (coral bleaching). The domi-
nant Symbiodinium type is the most studied and stress-susceptible in the associa-
tions, but new molecular techniques are allowing the discovery of many rare
Symbiodinium species in low abundances that would be stress-resistant and would
allow a replacement of the dominant types (Berkelmans & van Oppen, 2006;
Boulotte et al., 2016). These rare Symbiodinium taxa contribute to host–symbiont
community stability and promote the environmental resilience of the coral holobi-
ont (Ziegler et al., 2018). Interestingly, these “microbiome” switches or flexibility
of change could facilitate relatively rapid responses to environmental changes in
other organisms (Ziegler et al., 2019; Voolstra & Ziegler, 2020). We will return to
this symbiotic association later in the book.

5.5 Key Concepts and Ideas in This Chapter

• Aberrant species represent both teratological cases and exceptional organisms.

These species that captivated Darwin and still amaze us today may be unique in
their taxonomic groups, rare in their geographic range, hyperderived groups, or
“living fossils.”
• Teratology examines abnormal morpho-physiological developments in various
taxa and can be useful for understanding possible morphological pathways by
linking internal developmental rules, as well as adaptive and functional explana-
tions. This has led to a vindication of the reporting of teratological cases, as well
as the study of their causes and their inclusion in fields such as Evo-Devo.
• Teratologies have inspired great theories such as homeotic genes or the ABC
model in plants. Their study can alert us to current or past environmental pollu-
tion, certain teratologies in plants are intentionally produced, and other teratolo-
gies are combated because of the ecological damage they cause.
• Exceptions and rarities are invaluable in the study of biology and should be more
emphasized in the definitions of taxonomic groups. Sometimes there are particu-
lar rarities, but in other cases, there are “intermediate exceptions” with minorities
of species or clades with certain characteristics compared to the majority.
• We can find exceptions in many animal and plant groups; we just have to know
how to observe, relativize, and value these cases. In some cases, we face a “para-
dox” of a chain of exceptions and rules, demonstrating how interesting and com-
plex the analysis of these cases can be.
• We review groups that, due to their rarities, have been difficult to classify, rarities
that can be used to human benefit, exceptional groups that make us reconsider
phylogenetic relationships, phenomena with incredible exceptions, animals and
plants that are not what they seem or do not do what is expected, and evolution-
ary and ecological aspects of rare species.
192 5 When THAT Exception Persists Almost as THAT Exception

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Chapter 6
Focusing on Dynamics: When an Exception
Becomes a Rule

The historian of science may be tempted to exclaim that when

paradigms change, the world itself changes with them
—Thomas Khun

Contents
6.1 Introduction    225
6.2 E-R Changes by Nature’s Action    227
6.2.1 At Crucial Moments of Biological Evolution    227
6.2.1.1 Origin of Life    227
6.2.1.2 “Energy Expansions” of Evolution    230
6.2.1.3 Origin of Eukaryotes (and Protist Radiation)    232
6.2.1.4 Symbiotic Evolution: From the Restricted to the Rule?    234
Toward a Symbiogenic Phylogenetics (SYMPHY)?    236
6.2.1.5 Origin of Sex    237
Sex Chromosomes and Their Entity as an Exception    240
A Pluralistic Approach to Hypotheses    241
6.2.1.6 Origin of Multicellularity    242
6.2.1.7 Multicellularity and Cancer    246
6.2.1.8 Changes Linked to the “Initial” Invasion of the Earth    247
Changes Associated with Ecological Succession Mechanisms
Among Land Colonizers    251
6.2.2 Perspectives and Cases of when “Oddities” Become the Pattern    252
6.2.2.1 Nonrepresentative Individuals Are Settlers    252
6.2.2.2 Minorities Channeled Via Phenotypic Plasticity    257
6.2.2.3 Beginning of Coevolution Between Plants and Pollinators    261
A Little History    262
The Flower and Its Rewards    263
Mutualism and Deception    264
6.2.3 A More Bidirectional E-R Dynamic in the Short Term: Facultative
Organisms    267

© Springer Nature Switzerland AG 2024 223

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_6
224 6 Focusing on Dynamics: When an Exception Becomes a Rule

6.3  -R Changes Due to Human Activity on Nature

E    271
6.3.1 Exotic Groups that Become Local Pests    271
6.3.1.1 Introduced Animals    271
6.3.1.2 Introduced Plants    274
Other Witness Cases in Different Regions of the World    275
Witness Cases from the South of the World    276
6.3.2 A Look at the Disease Cycle and the Role of Man    278
6.3.2.1 General Epidemiological Context    278
6.3.2.2 Historical Review and Some Emblematic Cases    279
Some Witness Cases    281
6.3.3 Influence of Environmental Pollution and Climate Change    288
6.3.3.1 Water and Air Pollution    289
6.3.3.2 Spill    290
6.3.3.3 Soil    291
6.3.3.4 Nuclear Energy    291
6.3.3.5 Micro and Nanoplastics    291
6.3.4 Manipulating Organisms to a Destination    293
6.3.4.1 Artificial Selection: Turning Exceptions into Rules    293
6.3.4.2 “Artificial” Cloning, the Transition from Exceptions to Rules?    299
6.3.4.3 Synthetic Biology: On the Way to Becoming Something Common?   302
Some Fields where Synthetic Biology Could Become Very
Common    304
Synthetic Biodiversity Conservation    306
Ethical Aspects    307
6.4 E-R Changes Due to Modifications in Scientific Interpretations    308
6.4.1 Key Factors Associated with Change    308
6.4.1.1 Scientific and Sociocultural School Biases    308
6.4.1.2 Knowledge of Diversity and Evolutionary Framework    309
6.4.1.3 Related to Current Equipment and Methodologies    309
6.4.2 Some Case Histories of E - R Change by Scientific Vision    310
6.4.2.1 Learning and Animal Personality    310
Animal Learning    310
Animal Personality    314
6.4.2.2 Neuronal Plasticity: Regeneration and New Connections    316
6.4.2.3 Communication in Plants    322
Herbivory, Communication and Reaction in Plants    323
Plant Senses    325
Memory and Vegetable Intelligence?    329
6.4.2.4 Epigenetics: When Environment Matters    330
6.4.2.5 Genome Transposons    334
6.4.2.6 Microbiome and Host    336
Holobionts    338
6.4.2.7 About “Cryptic” in Biology    340
Cryptic Genetic Variation    341
Cryptic Female Choice: From Restricted to Rule    342
6.4.2.8 Sexual Selection in Plants: From Simple Curiosities to a
Generalized Fact    347
Analogies Between Plants and Animals    349
6.5 Key Concepts and Ideas in This Chapter    351
References    353
6.1 Introduction 225

Abstract In this chapter, we deal with the change from the exception to the rule in
biological systems, both by the action of nature and by the changes that occur due
to human action. We talk about the origin of life on planet Earth, the first organisms
that colonized primitive environments and changed the atmosphere, giving rise to
new forms of life, the appearance of eukaryotic, multicellular organisms, and the
different forms of reproduction. We focus on events and changes that were initially
considered teratological and that are familiar to our current vision. We also mention
adaptations, plasticity, and different phenotypes that became advantages and
allowed organisms to continue living in different environments. On the other hand,
we point to global processes that affect humans and that in many cases are caused
by humans. We discuss examples of diseases that turn into pandemics, the processes
of environmental pollution, and accelerated climate change. Finally, we will discuss
the changes in scientific ideas, which are closely linked to the social context at each
moment in human history, the changes in the different fields of study and within
society itself.

6.1 Introduction

At the beginning of the section that covers this chapter, we saw that stability and
dynamism are states that can be ephemeral in many situations at the scale of time,
space, or group. Accordingly, in the two previous chapters, we have seen cases in
which stability, the “conserved,” prevails over change at any scale or level, depend-
ing on the point of comparison. In this chapter, we focus on the situation that we
could describe as a change from “exception to rule,” when the uncommon becomes
the pattern. It is one of the most exciting and striking situations for scientists and
nature. The least interesting would be that nothing changes or is simply a matter of
changes from rules to other rules (e.g., modulating their scope), but without imply-
ing that this change is for something previously considered a rarity.
There is perhaps a solid epistemological view whenever the word change is used
in the dynamics of rules, often inherently implying the concept of exceptions. As
discussed in the chapter on rules, Kuhn’s epistemology emphasizes the significance
of change and revolution, which are typically preceded by a crisis. However, it is
important to note that this perspective does not solely or exclusively attribute the
emergence of exceptions to the evolution of rules. Indeed, the idea of scientific revo-
lutions implies the fall of a paradigm from the growth of a new body of arguments
and data that refute that preexisting paradigm. In the beginning, the new idea was
like a bottle in the sea, an undervalued exception for its acceptance in the commu-
nity. Kuhn’s epistemology inherently embodies the essence of change. In addition
to the advancements made in refining his fundamental concepts, contemporary
226 6 Focusing on Dynamics: When an Exception Becomes a Rule

contributions by scholars such as Lakatos have helped to provide a clearer under-

standing of what aspects are more prone to change. Furthermore, Feyerabend’s
notion of nonacceptance of rules in a strict sense adds to the understanding of
change. Nevertheless, one undeniable fact remains: change does indeed exist.
The phrase by Kuhn (1976) that heads this chapter alludes to that strange sensa-
tion of perceiving that the world has also changed because the scientific paradigm
with which we understood it (or at least tried to understand it) has changed. This
new perception is understandable since the change in the scientific gaze influences
the way we perceive the surrounding world. As he argues, to the extent that scien-
tists’ only recourse to that world is what they see and do, we can say that they will
respond to a different world after a revolution. It is a somewhat circular argument
that reflects what often happens to us. In other words, although the world has not
changed, by changing our gaze, it is presented to us as if it has changed. Technological
advances are certainly promoters of these changes and new perspectives. It is feed-
back between science and technology. For example, the development of electron
microscopy has allowed the exploration of cell ultrastructure and the structure of
materials. It promoted exploring previously uninvestigated aspects with new dis-
coveries, which again pushed for improving that technology. Additionally, as Kuhn
argues, during revolutions, scientists see new and different things when they look at
new instruments in places where they have looked before. This metaphor master-
fully illustrates this concept of looking again at the known with new eyes: “It is as
if the professional community has suddenly been transported to another planet
where familiar objects are seen in a different light and join the unknown. Of course,
nothing of the sort happens: there is no geographical transplantation; outside the
laboratory, everyday affairs usually continue as before”—Kuhn, 1976.
However, it is crucial to avoid the temptation of solely engaging in an epistemo-
logical exercise focused on examining the dynamics between rules and exceptions
within the context of the history of biological knowledge. This narrow approach
only considers changes resulting from shifts in scientific paradigms, such as altera-
tions in schools of thought and technological advancements. Although this is
extremely interesting and important, the truth is that it responds to a specific
dynamic framework: our history of knowledge. We have to balance our approach
and assessment of exceptions from the other significant dynamics framework: the
one based on changes in biology both in the short or medium term (e.g., at the physi-
ological, behavioral, and ecological level) and in the long term (e.g., at the genetic,
evolutionary level). The dynamics of the history of knowledge could be considered
analogous to the Darwinian approach to biological evolution (Ruíz & Ayala, 1998).
Thus, considering an evolutionary approach, we have already seen that, from an
adaptive functional point of view, oddities can become a rule to be generalized.
There may be a mixture of biological changes and changes in the scientific com-
munity’s interpretation and view of the “knowledge” of these changes. Hence, the
confusion or being able to easily fall, or be trapped, in the strictly epistemological.
Therefore, this chapter will address some “witness” cases of dynamism from
exception to rule in biological systems. These will begin with the changes from
exceptions to rules occurring at the biological level by the action of nature itself or
6.2 E-R Changes by Nature’s Action 227

the man on it. Subsequently, we will examine these changes within the framework
of scientific knowledge of biology, driven by changes in schools of thought and
technological advances.

6.2 E-R Changes by Nature’s Action

6.2.1 At Crucial Moments of Biological Evolution

6.2.1.1 Origin of Life

Currently, the existence of life on planet Earth is the rule. Therefore, we find life
forms adapted even to extreme environments of temperature, altitude, pressure, and
humidity (Rampelotto, 2013). Therefore, the rarity on our planet is not to find traces
of life somewhere. Life is massive and present everywhere, from large vertebrates,
invertebrate organisms, and plants to simple microorganisms such as thermophilic
bacteria. However, we know that life was not always the rule on Earth. Life was
initially an absolute exception because it was a singular event on our planet.
Moreover, the abundance of the initial organisms would logically have been low
until a new stage was reached, in which the density of descendants progressively
increased.
If someone from outside the Earth had observed our planet at that remote time,
perhaps so great would be the magnitude of exception or rarity in the existence of
life that they might not even have detected it. The question is whether something
similar might happen to us when looking for life elsewhere in the solar system or the
universe. Thus, that exception (i.e., initial life on Earth) could have remained as
such. However, life began to develop, biological systems diversified, and the num-
ber of representatives increased and evolved (Solomon et al., 2018; Curtis et al.,
2008). Given these circumstances, it is not surprising that while this book explores
the concepts of rules and exceptions within the realm of life, including animals,
plants, and other organisms, it is noteworthy that life itself, in its early origins, rep-
resented a remarkable exception marked by genuine innovation.
We will not discuss the hypotheses explaining the origin of life. It has been
addressed in classic books, such as the pioneering work of Aleksandr Oparin (1924)
and John B. S. Haldane (1929) and the subsequent writings of Francis Crick (1981),
Robert Shapiro (1988), Leslie Orgel (1998a, 1998b), and Freeman Dyson (1999),
among others. Laboratory experiments such as those of Stanley Miller (1953) have
become classic examples in the field, despite the inherent limitations that their
results may possess. The results obtained by Miller can also be obtained under con-
ditions of atmospheric neutrality closer to an environment dominated by volcanic
gases, as prevailed on the early Earth (Harold, 2001; Fitz et al., 2007). In addition,
discussions on the possibility of the extraterrestrial origin of life through pansper-
mia (Tepfer, 2008; Wickramasinghe, 2012; Cockell, 2016) or the bombardment of
prebiotic foreign organic compounds (Lazcano-Araujo & Oró, 1981; Chyba et al.,
228 6 Focusing on Dynamics: When an Exception Becomes a Rule

1990; Whittet, 1997; Callahan et al., 2011) also add exciting ideas to the hypotheses
of the origin of life.
What is certain is that for our examples for the present book, the origin of life or
“abiogenesis” combines the three contexts analyzed in this book. The context of a
group, or individual, is represented by the appearance of the first living being
(FUCA aka First Universal Common Ancestor—Prosdocimi et al., 2018).
Meanwhile, the context of space refers to a particular place where life began, for
example, a specific site in the primordial sea, rather than happening massively at
various points. However, no one can say for sure! (Raup & Valentine, 1983, Shapiro,
2007; Velasco, 2018). Finally, the time context alludes to the millions of years it
would have taken for the first living thing to appear since the formation of the Earth.
Its appearance took place approximately between 3000 and 4000 million years
(Schopf, 2006; Schopf et al., 2007; Raven et al., 2002; Dodd et al., 2017; Freeman
et al., 2017; Betts et al., 2018) from precursors that were not categorized as living
beings (e.g., complex and clustered organic molecules but not organized within a
protective layer). The cell membrane was crucial for giving entity to that unit, the
primitive cell, which progressively began to evolve and diversify.
Chaos and entropy ruled in that primitive world. Unlike today, on primitive
Earth, there is no atmospheric oxygen and no ozone layer to filter out dangerous UV
rays (Towe, 1981; Cockell, 2016). Thus, the mere existence and maintenance of
certain complex organic compounds was already an exception (Solomon et al.,
2018). Not only were these compounds challenging to generate, but they were dif-
ficult to maintain and replicate once they were generated by chance. Thus, once
these molecules were formed and stabilized, it was possible to make further prog-
ress and improve the work, catalyzing processes that were previously unnecessary.
Take, for example, the formation of a molecule such as RNA or a related primitive
precursor. The RNA world theory (Gilbert, 1986) assumes that in the beginning,
RNA was responsible for carrying genetic information and catalyzing protein for-
mation processes (Cech, 1990; Altman, 1990, 2000). This model today can be seen
as an exception, contrasting with the current model in living systems where the
RNA/protein/DNA complex is in charge of performing such a task and with sub-
stantial improvements (Bernhardt, 2012). The rule at that primitive time of biotic
origin was the circulation of molecules dissolved in the medium (Kauffman, 2011).
The formation of a compound such as RNA requires the polymerization of a long
chain of nucleotides. This chain is very unstable in an aquatic environment (Shapiro,
2007), requiring extra help from other coexisting compounds in the environment.
The appearance of simple, selectively permeable membranes, combined with ions
and the presence of amino acids, likely played a crucial role in preserving, stabiliz-
ing, and facilitating the evolution of this organic compound. Otherwise, it would
have been exposed to bombardment and eliminated in the primordial broth (Carny
& Gazit, 2005; Higgs & Lehman, 2015; Pressman et al., 2015). These future mem-
branes were perhaps in the medium as soap droplets (micelles) in an aqueous solu-
tion (Luisi, 1996; Benner et al., 2010). The use of these structures to shelter
molecules, especially with genetic information, may have been rare. However, it has
become the rule maintained today in all living organisms and other biological
6.2 E-R Changes by Nature’s Action 229

entities, such as viruses. A pivotal transition occurred, leading to a change in the

level of complexity commonly referred to as life. At the heart of this transformation
lies the fundamental ability to reproduce, serving as a key defining characteristic.
We see that the sum of oddities of a particular moment generated the landscape we
now see as usual.
Among the oldest organisms (3.4–3.8 BYA), both autotrophs and heterotrophs
were represented (Solomon et al., 2018). For a long time, it was thought that the first
living cell was a heterotroph, consuming molecules and metabolizing them through
fermentation since the absence of oxygen was the rule at that time (Dismukes et al.,
2001). Gradually, however, more recent discoveries have turned that hypothesis
toward chemoautotrophs or photoautotrophs (Ward & Kirschvink, 2015; Solomon
et al., 2018). Notably, various groups of chemosynthetic bacteria have been discov-
ered, which were likely well adapted to thrive under harsh environmental condi-
tions, including extreme temperatures, prevailing on Earth during that period (Raven
et al., 2002; Martin & Russell, 2003; Curtis et al., 2008; Martin et al., 2018; Freeman
et al., 2017). These primitive organisms laid the foundation for subsequent Earth
changes. Primitive autotrophs, such as photosynthetic cyanobacteria, gradually
oxygenated the atmosphere and changed the environment forever (Des-Marais,
2000). The presence of a sufficient quantity of oxygen in the atmosphere allows the
appearance and evolution of heterotrophic organisms. This represents a new change
where something once regarded as an exception has now become the rule. In the
next section of this chapter, we will review that critical moment, which is linked to
a chain of energetic expansions in life.
In the context related to the origins of living beings, we cannot fail to mention the
concept of LUCA (an acronym for Last Universal Common Ancestor), as it is
known to be the immediate ancestor of all living beings (Woese, 1987; Forterre
et al., 2005; Glansdorff et al., 2008; Weiss et al., 2018). LUCA is not considered the
first life form on the planet (as we said, that is FUCA—Prosdocimi et al., 2019).
LUCA represents the only kind of organism of that time that still has living descen-
dants and gave rise to the three domains of life (Prosdocimi et al., 2019). In a frame-
work similar to the one posed for the first living organism, LUCA’s emergence,
propagation, and diversification are framed in a transition from exception to rule; of
course, a rule is represented by an expansion in descendants that reach up to the
present epoch. Initially, it was also an exception that this organism, and perhaps
earlier forms of it, were subject to natural selection (Darwin, 1859). Some studies
suggest that prebiotic organic compounds may have been subject to selective forces
(Ponnamperuma, 1978; Anderson, 1983; Lazcano & Miller, 1996; Subramanian
et al., 2020). The ability of early organisms to undergo changes over time was a
fundamental breakthrough that, as we discussed, currently stands as one of the fun-
damental principles defining all living entities: the capacity for evolution
(Chodasewicz, 2014; Schulze-Makuch & Irwin, 2018).
A question that elicits a sense of fear or desolation within humanity is whether
life on Earth is an exception in relation to the rest of the vast universe. Exobiology,
research, and space missions seek to decipher this big question (Cockell, 2020;
Schulze-Makuch & Irwin, 2018). Enrico Fermi once wondered “where is
230 6 Focusing on Dynamics: When an Exception Becomes a Rule

everyone?,” alluding to the absence of contact with other extraterrestrial organisms

or civilizations (Gray, 2015). Thus far, the existence of intelligent life forms and the
technological development to make contact seems scarce or absent in the universe.
However, the hypothesis that simple or inferior life forms are present on different
exoplanets located within the habitability zone of their stars or even the possibility
that life exists on planets or moons within the solar system would not seem at all
far-fetched (Cockell, 2016). For now, the rule remains the general absence of life
outside the Earth. We will return to this enigmatic field toward the end of Chaps.
7 and 8.

6.2.1.2 “Energy Expansions” of Evolution

When hypotheses about the origin of life are discussed, there is one point in com-
mon among them, the existence at that time of macro and microclimatic conditions
very different from those that today form the pattern on earth. The combination of
water, which is an essential component, along with specific critical chemical ele-
ments, serves as the building blocks for the formation of more intricate molecules.
These molecules act as the foundation for cellular structures, even in their simplest
form, thus laying the groundwork for the emergence of minimal yet living organ-
isms. However, until recently, evolutionary biologists have not placed much empha-
sis on the effect of the type of energy prevailing at “x time” in favoring or not
favoring the emergence and evolution of certain life forms. A look at the feedback
between abiotic and biotic conditions, referring mainly to the association in “ener-
getic” terms at each moment, has been missing.
The approach finally arrived very recently, in the hand of an inspiring study by
Olivia P. Judson (Judson, 2017), an author well known in the field of science com-
munication. She has proposed to pay attention to the “energy expansions” associ-
ated with the evolution of living beings, considering the type of source and factors
that propitiate their appearance. She argues that the life system on earth can be
divided into five “energy” epochs, each of which is conducive to the evolution of
life forms that can exploit new energy sources. These sources are geochemical
energy, sunlight, oxygen, flesh, and fire. Judson argues that both geochemical
energy and sunlight were present from the beginning but that the others are already
a consequence of evolutionary events (i.e., produced by the concrete activity of liv-
ing organisms, such as the effect of cyanobacteria on the production of oxygen). If
we consider that none of these energy sources have disappeared over time, this has
directly resulted in an expansion of available energy resources for living organisms.
Consequently, this has fostered an associated increase in the diversity and complex-
ity of ecosystems. In addition, these expansions have implied transformations of
crucial aspects of the terrestrial environment, which in turn have mediated future
evolutionary changes. Incorporating this energetic perspective potentially empow-
ers us to anticipate the trajectories of life systems on planetary scales, regardless of
their location. Indeed, in the current era of exploring exoplanets similar to Earth
throughout the universe, this approach holds significant value, as it enables us to
6.2 E-R Changes by Nature’s Action 231

make predictions about the expected conditions on a particular planet based on its
known energetic state. We do not intend here to make an exhaustive presentation of
their arguments, but we express the value of this approach for our book.
On the other hand, something that derives from this new vision is that many of
the sources first alluded to did not exist, or if they did, they were infrequent. We can
trace geochemical and solar energy from the beginning (although initially billions
of years old, these were still in the process of becoming a rule). However, for exam-
ple, oxygen in its free state is initially the product of the action of organisms such as
cyanobacteria. Free oxygen initially represented an exceptional occurrence but
gradually emerged as the prevailing pattern from an energetic perspective. The pre-
vious energy sources were incorporated to varying degrees alongside the rise of free
oxygen. The same happened with the age of meat. Predators appeared when there
were enough autotrophic organisms, and the ingestion of “meat” became general-
ized. When predators appeared, it was necessary for a minimum of autotroph pho-
tosynthesis systems or detritivorous organisms. The idea is going from a nonexistent
fact or strategy to exception, from exception to rarity, from rarity to something in
between, and then to something more generalized up to a specific limit (e.g., avail-
ability of “prey” at each time and site, sensu the predator–prey model). The fire
epoch, also an exception at the beginning, appears only when atmospheric oxygen
(produced by life) is sufficient and shapes regions by its drastic effect on plant and
animal communities. Additionally, when humans appear, they learn to use it. Again,
in the beginning, it was an exception, but little by little, it became a habit. It has
already become the rule for cooking food and modifying the environment (e.g.,
burning pastures and forests to favor the growth of certain species humans wish to
exploit for their use). Thus, we have at least three epochs, that of oxygen, that of
meat, and that of fire, that at the beginning were exceptions but gradually
became rules.
Judson also argues that all five forms of energy have been recovered. In the glo-
bality of the terrestrial life system, an additive effect of energy sources predomi-
nated. However, today, species have not been evenly distributed in the exploitation
of energy sources, but rather those linked to oxygen and meat predominate (for
example, consider the million species of insects vs. the few species that live on
geochemical energy alone), or so it is believed. Some estimates suggest that the
biosphere operating below the surface still rivals in terms of mass that of the surface
(Whitman et al., 1998). That is, the magnitude of the contribution of each energy
source to sustaining life activities in the taxa is different. In terms of direct contribu-
tion, from a relative point of view, specific energy sources, such as geochemical
sources, became the exception. Geochemical energy went from an almost “abso-
lute” rule billions of years ago to a more circumscribed rule, at least as a direct
energy source in the strict sense. Finally, this new perspective that emphasizes the
role of energy sources and feedback in evolution represents, in a way, a modification
of the current paradigm regarding our understanding of evolution, as has happened
with so many theories and hypotheses. This view does not challenge the classical
neo-Darwinian framework but rather adds additional elements that enrich our previ-
ous ideas.
232 6 Focusing on Dynamics: When an Exception Becomes a Rule

6.2.1.3 Origin of Eukaryotes (and Protist Radiation)

For almost 2000 million years, the only living organisms on earth were prokaryotes
(Alegado & King, 2014). It is postulated that eukaryotic cells appeared approxi-
mately 1500 million years ago (Knoll et al., 2006). This “appearance” is, in itself,
an enigma. Initially, the “first” eukaryote was not of the standard type or pattern. We
could even say it was a “quasi” teratology in a prokaryotes’ world. The appearance
of an organism, still a cell, containing its genetic material enclosed within a double
membrane, along with a prokaryote within its cytoplasm (which would eventually
become the mitochondrion), might initially appear as an anomaly, deviating from
the prevailing understanding of what constitutes an organism (cell) based on com-
mon knowledge. Its functionality made this appearance “monstrous” from the point
of view of a “prokaryotic observer.”
There have been many models to explain the origin of eukaryotes, and to date,
this subject is still much debated. Among them, autogenous theories postulate that a
prokaryotic cell is the ancestor of eukaryotes, and some organelles arise from invag-
inations of the plasma membrane (Reid, 1985). However, following these theories,
it is still impossible to explain the origin of organelles, such as mitochondria and
chloroplasts, with critical functions for modern eukaryotes. Thus, the endosymbio-
sis theory between two prokaryotic organisms has gained relevance (Margulis,
1981). While it may not provide a comprehensive explanation for the origin of all
cellular structures, it remains a highly remarkable theory. Some authors have even
developed theories explaining the origin and evolution of eukaryotes in two phases.
These phases involve autogenous and symbiogenesis processes to explain the com-
plexity of the eukaryotic cell, its organelles, and even the nuclear membrane’s struc-
ture and cytoskeleton’s structure (Poole & Penny, 2001; Cavalier-Smith, 2002a).
The role of endosymbiosis (from phagocytosis of a cell by its host) was and is
questioned by many authors (Martin et al., 2001). However, there is more consensus
to support the notion that the mitochondrion and chloroplast were indeed acquired
through such a process, whereby they were originally separate organisms ingested
by the host (López-García et al., 2017). Whether the host was a prokaryote, an inter-
mediate prokaryote-half-eukaryote with a defined nucleus but still without mito-
chondria, or an archaeon is a matter of debate. Some authors suggest that the process
of endosymbiosis that gave rise to mitochondria occurred after an earlier fusion
between bacteria and archaea (Zillig et al., 1989). However, other works propose
that more than one endosymbiosis originated the mitochondria and the nucleus from
a bacterium and archaea phagocytosed by a host (Lake & Rivera, 1994; Horiike
et al., 2001). However, the origin of the nucleus by endosymbiosis has been firmly
rejected (Martin, 1999; Poole & Penny, 2001). Finally, it has also been postulated
that the origin of mitochondria was one of the last steps in the evolution toward
eukaryogenesis (Karlberg et al., 2000; Cavalier-Smith, 2002a; Andersson et al.,
2003). The significant problem is that there is no agreement on what constitutes a
valid hypothesis, but it is most widely accepted to postulate that the initial phagocy-
tosed element was a bacterium (McFadden & van Dooren, 2004; Zimorski et al.,
2014; López-García et al., 2017).
6.2 E-R Changes by Nature’s Action 233

Recent advancements in genetics, our understanding of marine microfauna,

research on viruses and the emergence of new domain classifications have proved to
be crucial in the scientific interpretation of this ongoing discussion, which continues
to be of great significance today. For example, the conservation of choanocytes in
choanoflagellates and primitive animals such as sponges suggests that the animal
progenitors were bacterivorous (Alegado & King, 2014). On the other hand, the
diversification of animals coincides with a rapid reduction in the abundance of stro-
matolites, and from this, it could be thought that the bacteria involved in those for-
mations were preyed upon by primitive animals (Garrett, 1970; Awramik, 1971;
Walter & Heys, 1985). These phagocytosed bacteria could have impacted genome
evolution by lateral gene transfer, providing new genetic material in animals and
their origins (Alegado & King, 2014). There is a continuous stream of intriguing
news claiming the discovery of the long-awaited “key” piece, whether through fos-
sil findings, theoretical advancements, or breakthroughs in genetics and physiology.
These findings aim to unravel the mystery surrounding the origin of eukaryotes
(e.g., Keeling & Doolittle, 1995; Rivera & Lake, 2004; Gribaldo et al., 2010; Spang
et al., 2015). In any case, the initial appearance of this “proto-eukaryote” was not a
massive event. Even if it occurred more than once, it remained something scarce.
One could well say “teratological,” as we have already emphasized. The idea that
the process of phagocytosis of another organism could eventually lead to a close
relationship, such as the one observed between a whole cell and the mitochondrion,
may initially seem far-fetched. However, it is undeniable that this process under-
went numerous trials and errors before the emergence of a primitive “eukaryote”
where it proved successful. In these early stages, the relationship likely began as a
commensal one, without any adverse effects on the host organism.
Since the Paleozoic era, approximately 550 million years ago, eukaryotes have
been extraordinarily successful. In addition to the multicellular plants, animals, and
fungi that define the biosphere we know today, many simple groups of protists still
contribute fundamentally to ecosystem function (Butterfield, 2015). However, this
was not always the case. Eukaryote evolution represents one of the most elemental
transitions in the history of life on Earth, yet there is considerable debate and a lack
of consensus regarding the exact timing of this event. The increase in cellular com-
plexity from prokaryotic cells would inevitably have generated explosive radiation
of protists into every available ecosystem niche (Cavalier-Smith, 2002a). The cyto-
skeleton, molecular motors, and cellular endomembrane system exhibited the most
far-reaching changes. Without these innovations, the existence of complex proto-
zoa, as well as the diverse array of animals, plants, and fungi that we observe today,
would not have been possible. Their functional diversification was accentuated by
their new ability to ingest and digest other cells as food or keep them in place as
“slaves” that provide energy and valuable metabolites (Cavalier-Smith, 2002b). The
abundance, diversity, and evolutionary revolution of protists and their genetic mate-
rial undoubtedly characterize them as transitional organisms (Lynch & Conery,
2003). The manner in which selection and genetic drift influence mutations in pro-
tists can be compared to the processes observed in large populations of evolution-
arily significant prokaryotes, as well as in small populations of multicellular
234 6 Focusing on Dynamics: When an Exception Becomes a Rule

eukaryotes. This is due to this intermediate state in which protists can be considered
precursors to other eukaryotes, as described by O’Malley et al. (2013).
In summary, the origin of eukaryotes represents an actual example of the passage
from the abnormal to something that later resulted in the appearance of protists and
then to the rest of the animal, plant, and fungal phyla. The controversy about this
origin does not prevent us from tracing the reasoning that we could pose as a rule:
“everything that became massive, expanded, generalized, began as a rarity.” Is this
something that sounds logical, obvious, or even naive, although it is something that
we do not value and do not think about in our view of biological evolution, at least
not enough.

6.2.1.4 Symbiotic Evolution: From the Restricted to the Rule?

As we have seen, the origin of eukaryotes is closely connected to the concept of

symbiogenesis, which is defined as an evolutionary mechanism that generates varia-
tion and produces new species through symbiotic associations between two indi-
viduals (Mereschkowsky, 1910; Margulis, 2010). This process has been recognized
as a significant means of generating “biological novelties.” While it has consider-
able support, it also faces criticism, particularly from proponents of neo-Darwinism
(Speidel, 2000).
There are currently many symbiotic associations, and we have reviewed some of
them in Chap. 5. An exceptional case is represented by lichens, which are the result
of symbiosis between a fungus and an alga or a cyanobacterium. One-fifth of all
known fungal species form symbiotic associations with green algae, cyanobacteria,
or both to generate lichens as new organisms. It allows fungi to fulfill their carbohy-
drate requirements (Hawksworth, 1991; Hawksworth et al., 1995). This symbiotic
association confers exceptional resistance to various environmental conditions,
enabling them to occupy ecological niches characterized by conditions that indi-
vidual organisms involved in the symbiosis would be unable to survive in (Schne
et al., 2008). Lichens are believed to have arisen independently, which explains their
high diversity and the occurrence of lichenized and nonlichenized fungal species
within the same phylogenetic group (Lutzoni et al., 2001). Furthermore, indepen-
dent losses of symbiotic associations may have occurred during the evolution of
fungi, and thus, there are nonlichen-forming species derived from lichen-forming
ancestors. However, the typical pattern observed in all these cases, as in many oth-
ers, is similar, and symbiosis facilitates evolutionary innovation, although it may be
lost later.
In addition, fungi can establish symbiotic associations with plant roots, forming
mycorrhizae. Fungi play a crucial role in converting soil minerals, such as phospho-
rus, into a form that is readily available and usable by plant roots. They facilitate the
transfer of nutrients from the soil to the plant (Selosse et al., 2006). Certain groups
of cnidarians, such as corals, can also form symbiotic associations with algae. These
algae provide them with energy through photosynthesis, enabling corals to meet
their energy needs for processes such as calcification (Inoue et al., 2018). In the
6.2 E-R Changes by Nature’s Action 235

following chapters, we will see that variations in temperature, light, and nutrients
can affect this symbiosis, modifying the abundance of microalgae and thus having
secondary effects on coral physiology (Dubinsky & Jokiel, 1994; Anthony et al.,
2008). The study of coral reefs can provide insights into fundamental processes in
symbiotic relationships between species and demonstrate how they can adapt to
environmental changes (Apprill, 2017). In addition, bacteria and fungi contribute to
the cycling of organic matter, forming these characteristic multimembered marine
microbiomes. Interestingly, many of these cases form an initial exception to a rule
in their respective groups. By evolution, we move from an initial (fortuitous?) asso-
ciation between an organism and its endosymbiont to a persistent linkage over time.
Thus, group and time contexts are present. For example, the colonization of land by
plants approximately 400 million years ago was made possible by symbiosis with
fungi (Lewis, 1987; Selosse & Le Tacon, 1998). These fungi formed associations
with roots in approximately 90% of higher plant species and even with ferns and
some mosses (Selosse & Le Tacon, 1998). The first plants that colonized terrestrial
life probably lacked roots and therefore needed an association with fungi for water
and mineral uptake (Aanen & Eggleton, 2017). However, this symbiosis was gradu-
ally lost or replaced in some lineages by other symbionts, such as nitrogen-fixing
bacteria or ectomycorrhizal fungi, or by new adaptations such as advanced root
morphologies.
Everything concerning endosymbiosis is also connected with changes in scien-
tific interpretations. As mentioned earlier, the endosymbiotic hypothesis was pro-
moted by Lynn Margulis. The postulates of this framework make it appear as an
evolutionary theory in itself, holistic, cohesive to all living beings (Margulis &
Sagan, 2002). Margulis’s advocacy for this theory was so influential that it was
often regarded as an alternative to the classical neo-Darwinian synthetic theory of
evolution (i.e., classical neo-Darwinism). More recently, building upon the concept
of symbiogenesis, Gilbert et al. (2012) proposed a “symbiotic” perspective on life.
According to these researchers, the concept of a “biological individual” was useful
in studying various aspects, such as anatomy, physiology, and genetics, which con-
tributed to the development of specific biological subdisciplines, each with its own
understanding of individuality. Nevertheless, with the advancements in genetics and
physiology that have unveiled the close association between animals, plants, and
their respective symbiotic microorganisms, there is a growing need to consider the
“holobiont” as the natural biological unit. The term “holobiont” refers to the multi-
cellular eukaryote and its persistent symbiont colonies, acknowledging the inte-
grated nature of these organisms and their symbiotic partners. In other words, the
barrier of the “individual” has long been crossed not only in scientific interpretation
but also in organic evolution. Consequently, the concept of the “biological individ-
ual” is considered outdated. This shift in perspective leads to the understanding that
symbiotic associations are no longer viewed as exceptions but rather as a wide-
spread phenomenon. It prompts the exploration of a new notion of biological unity,
wherein a group of multiple organisms comes together to achieve functional inte-
gration (Gilbert, 2014). Symbiont diversity plays a crucial role in the metabolism
and development of individuals, as observed in symbiont microbes within the
236 6 Focusing on Dynamics: When an Exception Becomes a Rule

animal kingdom. These symbionts contribute to a second mode of gene inheritance,

introducing variability to the host organism (Gilbert, 2011).
In the same line of analysis and curiously linked to the terminology of the present
book, we highlight the statement of Munzi et al. (2019). Indeed, symbiosis is now
recognized as a widespread phenomenon that was previously regarded as an “excep-
tion,” limited to certain organisms such as corals, lichens, or mycorrhizae, as men-
tioned earlier. However, with the advancement of knowledge, it has become evident
that symbiotic relationships are not exclusive to a few organisms but rather a “rule”
applicable across all living systems and entities. The microbiome has emerged as an
integral part of all life forms, underscoring the ubiquity and importance of symbi-
otic associations. Therefore, they emphasize that symbiosis could be seen as a fun-
damental strategy for life and that it represents biodiversity in action, where
communication, information exchange, and regulation between the parts guarantee
stability and adaptability.

Toward a Symbiogenic Phylogenetics (SYMPHY)?

In this framework of the implications of more integrative views claimed by symbio-

genesis theory, with greater or lesser emphasis, it is interesting to note the recent
study by Tripp et al. (2017) on their claim that current phylogenetics should take a
more integrative view in terms of considering symbiomes in the tree of life. The title
of their paper, “Reshaping Darwin’s Tree: Impact of the Symbiome,” refers to that
claim about the hitherto overlooked or at least underestimated the impact of symbi-
omes. That is, he aims to leave behind a classical systematic vision, more focused
on taking each species as a “unit” and instead be aware that in many cases (if not
all?), it is a complex of species forming a unit, as is the case for symbiomes.
The term symbiome refers to taxa intimately associated in physical space (colo-
calized) and coevolve together under selection, i.e., as a consortium. It is different
from the term holobionts. Although they can be taken as synonyms (as many of the
already cited and discussed previously in this chapter), it is better to use holobionts
when referring to physically associated taxa that do not coevolve or are necessarily
codependent (obligate). Examples of symbiomes are intimate interactions such as
those we observed above between plants with fungi, plants-cyanobacteria, algae-­
fungi, such as in the case of lichens, and even the intestinal insect-microbiome. For
example, phylogenetic studies in aphids showed that endosymbiont bacteria of the
genus Buchnera are one of the fundamental causes of aphid diversification. This
indicates that the acquisition of a free-living ancestor of the bacterium was followed
by the coevolution of both host and symbiont and the specialization of the host to
different feeding niches (Moran et al., 1993). Thus, each aphid species harbors a
strain of bacteria suitable for providing specific nutrients that are deficient in its diet
(Gil & Latorre, 2019). With the availability of known host and symbiont genomes,
it is now evident that it is the aphid that controls nutrient production by the bacteria
in finely tuned metabolic complementation (Eisen, 2010; Wilson & Duncan, 2015).
Another example is observed in most terrestrial plants, including cereals, which, as
6.2 E-R Changes by Nature’s Action 237

mentioned, can establish symbiotic associations with fungi and generate arbuscular
mycorrhizae. These mycorrhizae help plants acquire nutrients and protect them
from biotic and abiotic stresses (Harrison et al., 2002; Govindarajulu et al., 2005).
Fossil records suggest that this symbiosis coincides with the emergence of the first
land plants (Redecker et al., 2000). In recent years, genetic studies have identified
genetic components necessary for establishing this symbiosis in model plants
(Harrison, 2005; Bonfante & Genre, 2010).
In this context, it is imperative to consider the symbiotic phylogenetic vision of
these authors, considering that much of the diversity not yet described on Earth is
microbial, whether in mutualistic or parasitic associations. Indeed, for prokaryotes,
the classical model of species as a single exclusive unit would not be appropriate or
sufficient. The implications of considering a symbiotic phylogenetics (SYMPHY)
vision would allow better decisions and management of species conservation tasks,
invasive species, alternative fuels, technology, and biomedicine applications, among
others (Tripp et al., 2017).

6.2.1.5 Origin of Sex

One aspect of biology that was an exception millions of years ago but evolved to
become a rule in almost all organisms is that of sex. Countless books have been
written on this subject, from the time of Darwin (1871) to the essay by Margulis &
Sagan (1986), or now classic books on evolution by sexual selection (e.g., Andersson,
1994). In all cases, addressing how the first organisms reproduced and when sex
appeared, its advantages and disadvantages have been the subject of multiple views,
which have not always been in joint agreement with each other. We know that one
of the fundamental properties of life is reproduction, which has evolved from simple
to more complex forms. Initially, the rule was asexual reproduction, a process that
involves the replication of genetic information so that the offspring are the same as
the original individual. This mode of reproduction is still used by many unicellular
species and some multicellular organisms (Cook, 1979). The evolution of sexual
reproduction is an adaptive and specific characteristic of eukaryotic organisms.
Here, the offspring’s genetic material came from two different individuals, involv-
ing the combination of genetic traits where the gametes of both parents combined to
form the offspring (Grützner et al., 2004; Avise, 2011).
The origin of sexual reproduction has long been a mystery. However, the form of
reproduction used by organisms may have depended on the environmental circum-
stances surrounding them. For example, sexual reproduction could have been
favored under stressful conditions (Baker & Parker, 1973). Indeed, considering that
a very changing environment prevailed millions of years ago, high mutation rates
could have promoted an asexual organism to become sexual. Sexual reproduction
has numerous advantages that make it the rule. Among them, sex evolved as a mech-
anism to produce genetic variation through allelic recombination, which allowed
organisms to adapt to changing environments (Baker & Parker, 1973; Bernstein
et al., 1984, 1985, 1987). Other advantages of sex are that sex facilitates the
238 6 Focusing on Dynamics: When an Exception Becomes a Rule

propagation of advantageous traits (Crow, 1994), eliminates deleterious mutations

from the genome (Kondrashov, 1988; Griffiths et al., 1999), and facilitates germline
DNA repair (Crow, 1994). One of the most discussed hypotheses about sex mainte-
nance (a fundamental fact for it to be constituted as a rule) is that it helps organisms
resist parasites, a statement known as the Red Queen hypothesis (Barrière & Félix,
2005; Otto, 2008; Morran et al., 2011). Although sexual reproduction has advan-
tages, it also entails certain associated costs. For example, when reproducing asexu-
ally, organisms do not need to invest time and energy in searching for and choosing
a mate. At the level of population expansion, the disadvantage of sexual reproduc-
tion is that it grows less than an asexually reproducing population in each genera-
tion. In addition, an individual who reproduces sexually passes 50% of its genes to
its offspring, whereas it would have passed 100% of its genes to the progeny if
reproduction had been asexual. Therefore, an organism that reproduces sexually
transmits fewer copies of its genes than an organism that reproduces asexually
(Otto, 2008).
The origin of sexual reproduction dates back to the first prokaryotes, approxi-
mately 2 billion years ago, when bacteria began to exchange genes through conjuga-
tion, transformation, and translation. Although these processes differ from sexual
reproduction, they share basic similarities (Otto, 2008). In eukaryotes, it is believed
that actual sex emerged approximately 1.2 billion years ago in the Proterozoic Eon
in algal species, so sex through different successful processes managed to persist
over time (Butterfield, 2000). If environmental changes that produced DNA damage
were maintained over time, then selection would have acted continuously in the
transition from prokaryotes to eukaryotes, and adaptive mechanisms would have
caused asexual reproduction to give way to sexual reproduction (Lodé, 2012;
Bernstein & Bernstein, 2013).
Both types of reproduction coexist in numerous invertebrates and plants, known
as heterogamy. For example, when population density is low in rotifer species,
females reproduce asexually, and at higher densities, they accumulate a chemical
signal that induces the transition to sexual reproduction (Snell et al., 2006). Within
insects, ants, bees, and wasps exhibit sexual and asexual reproductive strategies.
Aphids are one group that has this dual type of reproduction. By asexual reproduc-
tion, they quickly create winged offspring that colonize new plants and then use
sexual reproduction in the fall to lay eggs for the next season (Stern, 2008). The
water flea Daphnia reproduces by parthenogenesis to quickly populate ponds and
then uses sexual reproduction as competition and predation increase (Burns, 2013;
Walsh, 2013). Meanwhile, at the level of higher organisms, including vertebrates,
most arthropods, and a significant portion of other invertebrates, sexual reproduc-
tion has become the main method of reproduction, predominantly the rule. Curiously,
this does not rule out the presence of “reversed” exceptions, i.e., the presence of
those primitive reproductive options in some of them (Table 6.1). There are cases
where the costs of sexual reproduction are very high, for example, because of the
difficulty of finding a mate; here, asexual reproduction, particularly parthenogene-
sis, is a common strategy in many species. Parthenogenetic organisms can be
divided into facultative (where females can reproduce sexually and asexually) and
6.2 E-R Changes by Nature’s Action 239

Table 6.1 Hypotheses about the advantages of sexual reproduction and examples of sexual and
asexual reproduction
Hypotheses about the advantages of sexual reproduction
Hypothesis Description Examples References
Evolutionary advantage Sexual reproduction Sexual: Humans, Bell (1982);
increases genetic birds, mammals, Kondrashov (1982);
variability and reptiles, amphibians Rice (2002); Otto &
facilitates Asexual: Bacteria, Lenormand (2002);
adaptation to some plants, Acari Lenormand (2003);
environmental Otto (2009)
changes
Quick evolution of Genetic Sexual: Humans, Bell (1982); Hedrick
resistance recombination of insects, amphibians, (2005); Hughes et al.
sexual reproduction birds (2008); Frankham
allows populations Asexual: Some virus, (2010); Frankham
to evolve rapidly fungus, Acari (2015)
resistance to
diseases and
parasites
Sexual selection The competition to Sexual: Birds, Andersson (1994);
mate and the mammals, some Tregenza & Wedell
selective choice by insects (2000); Brooks &
females leads to an Asexual: None Kemp (2001); Møller
improvement in the & Jennions (2001);
genetic quality of Kokko & Jennions
offspring (2008)
Types of sexual and asexual reproduction in different living organisms
Types of reproduction Description Examples Reference
Sexual reproduction: Combination of (usually haploid, or having a single set of unpaired
chromosomes) reproductive cells from two individuals to form a third (usually diploid, or
having a pair of each type of chromosome) unique offspring. Sexual reproduction produces
offspring with novel genetic combinations
Syngamy Takes place in Humans and other Kondrashov (1993);
multicellular animals. Plants. Algae Otto & Lenormand
organisms. It as Chlamydomonas. (2002); Campbell &
involves the fusion Fungi such as Reece (2005);
of two haploid aspergillus Bernstein &
gametes to create a Bernstein (2010);
genetically distinct Raven et al. (2002);
diploid offspring Tortora et al. (2016)
Conjugation Takes place in Bacteria. Unicellular
single-celled organisms such as
organisms. It paramecium. Fungi
involves the such as
exchange of genetic saccharomyces. Algae
material between such as spirogyra
two individuals
(continued)
240 6 Focusing on Dynamics: When an Exception Becomes a Rule

Table 6.1 (continued)

Hypotheses about the advantages of sexual reproduction
Hypothesis Description Examples References
Asexual reproduction: Produces offspring that are genetically identical to the parent because
the offspring are all clones of the original parent. This type of reproduction occurs in prokaryotic
microorganisms (bacteria) and in some eukaryotic single-celled and multi-celled organisms
Fission The splitting of a Binary fission Steele (2002);
parent cell into two Bacteria E. Coli, Ruppert et al. (2004);
or more daughter multiple fission Sánchez Alvarado
cells protozoa plasmodium, (2006); Popham
Schizogamy in (2013); Pechenik
apicomplexa (2015); Winfield &
toxoplasma Hoare (2015);
Budding The growth of a Cnidarians hydra, Booth & Deimel
new individual from unicellular fungus (2019); Kim et al.
a small projection yeast, sponges (2019)
on the surface of the Ephydatia
parent
Fragmentation The breaking of the Flatworms Dugesia,
parent into pieces, echinoderms starfish,
each of which can algae Ulva
grow into a new
individual
Parthenogenesis The development of Arachnids scorpions.
an embryo from an Insects aphids,
unfertilized egg reptiles lizards,
Rotifera

obligate (where females reproduce only asexually). Among vertebrate species with
facultative parthenogenesis, we can name scorpionfish species (Seiter & Stockmann,
2017), zebra sharks (Dudgeon et al., 2017), blacktip sharks (Feldheim et al., 2010),
and Komodo dragon (Watts et al., 2006). In species with obligate parthenogenesis,
we can name the lizard genus Cnemidophorus (Crews & Fitzgerald, 1980).

Sex Chromosomes and Their Entity as an Exception

It is important to note that the emergence of sex chromosomes, carrying genetic

information associated with traits defining one sex (male or female), represents a
unique novelty within the framework of what an exception is. Indeed, sex chromo-
somes can be regarded as an “exception to the rule” since they differ from all other
chromosomes in the organism, not containing the same genes; they deviate from the
pattern followed by homologous chromosomes (Audesirk et al., 2008). Before the
appearance of sex chromosomes, all chromosomes shared the same genes in their
pairs, maintained by mitotic cell division and subsequent regeneration. Nothing
changed. In contrast, meiosis, as a new form of chromosome division, is closely
6.2 E-R Changes by Nature’s Action 241

linked to the appearance of sex chromosomes (Grützner et al., 2004). If, as the evi-
dence indicates, sexual reproduction arose very early in eukaryotic evolution, pos-
sibly the essential features of meiosis were already present in prokaryotic ancestors
(Bernstein & Bernstein, 2010, 2013). In genetic sex determination systems, the sex
of an organism is determined by the genome it inherits. Different sex determination
systems depend on the sex chromosomes, e.g., XY in mammals (Piprek, 2009;
Fusco & Minelli, 2019), ZW in birds (Smith et al., 2003), and X0 in insects
(Charlesworth, 2003; Kaiser & Bachtrog, 2010), among others.
Sex has evolved along with the reproductive system, starting with similar gam-
etes (isogamy) and progressing to systems that have different types of gametes
(anisogamy) (Gee, 1999; Freeman & Herron, 2007). The most morphologically
simple organisms in any lineage tend toward isogamy, and the most complex organ-
isms tend toward anisogamy (Margulis & Sagan, 1986). Therefore, the transition
from isogamy to anisogamy represented a significant and crucial step in the evolu-
tion of sex, moving from exception to rule. This transition also played a vital role in
the progressive definition of distinct phenotypic traits between the two sexes
(Stearns, 1987). Classical schemes illustrate in a hypothetical Gaussian bell how
disruptive selection favored the most extreme varieties from isogamy. On the one
hand, a heavy, less mobile cell containing nutrients (e.g., yolk); on the other hand, a
cell with fewer nutrients is smaller and more mobile. As a consequence, eggs and
sperm emerged and became established as definitive gametes (Gee, 1999; Freeman
& Herron, 2007).
In summary, we can say that when sex first evolved, isogamy was the rule. Sexual
partners were nearly identical in appearance. However, many organisms and their
reproductive mechanisms have evolved, giving rise to anisogamy, which is now the
most widespread mechanism (Margulis & Sagan, 1986).

A Pluralistic Approach to Hypotheses

To the classical discussions of considering only one hypothesis or another to explain

the reason for sex, we now bet on a more “pluralistic” approach. That is, several
hypotheses should not be interpreted as mutually exclusive. The recent review by
Neiman et al. (2017) alludes to this point as to why sex is maintained in evolution.
The authors discuss the mechanisms underlying the maintenance of sexual repro-
duction from the perspective that different mechanisms could combine to prevent
the replacement of sexual populations by asexuals. Although leading evolutionary
biologists, such as R. A. Fisher, H. J. Muller, and A. Weismann, have already shown
the advantages of sexual reproduction, the question is, what maintains sex as a
widely used strategy as a reproductive mechanism? Numerous hypotheses are based
on it, for example, Muller’s ratchet (Muller, 1964), Lottery (Williams, 1975), Red
Queen (Jaenike, 1987), and deterministic mutation accumulation (Kondrashov,
1984), among others. At this point, numerous articles published in the 1990s sup-
port the idea that several hypotheses complement each other to explain sex mainte-
nance (Peck, 1993; Howard & Lively, 1998; Neiman et al., 2017). In this sense, in
242 6 Focusing on Dynamics: When an Exception Becomes a Rule

1999, West and collaborators developed what is known as the “pluralistic approach
to sex,” which posits the combination and interaction between different hypotheses.
Thus, the idea that a single mechanism is not sufficient to be able to explain the
maintenance of sex is widely accepted in the scientific community. West et al.
(1999) propose that different hypotheses coincide (some of them named above) and
raise the possibility that different mechanisms may vary in their influence among
different taxa (Neiman et al., 2017).

6.2.1.6 Origin of Multicellularity

Another remarkable example in biological evolution is the emergence of multicel-

lularity, marking a transition from rarity to a rule. Perhaps one of the most signifi-
cant examples of “generalized pattern.” In the previous paragraphs, we have
commented on the basics, that is, the origin of eukaryotes, which led to their radia-
tion at the unicellular level through protists. However, evolution would take another
even more significant step by forming closely associated groupings of cells and thus
producing more complex beings. It would lay the foundations for the appearance of
representatives of the various kingdoms that make up life on Earth. Interestingly,
despite the advantages that multicellularity provides, it has not hindered the coexis-
tence of unicellular organisms alongside multicellular life forms. This phenomenon
continues to persist even after millions of years of evolution.
The origin of eukaryotic multicellular organisms represents a significant evo-
lutionary milestone (Butterfield, 2000; Schlichting, 2003; Niklas & Newman,
2013, 2016). Interestingly, this milestone occurred not as a unique event but inde-
pendently in numerous groups. In its simplest sense, it has been observed at least
25 times, even when considering simple cell aggregation (Grosberg & Strathmann,
2007; Niklas & Newman, 2013; Niklas et al., 2019; Claessen et al., 2014;
Hammerschmidt et al., 2014). In a narrower sense, the definition of complex mul-
ticellularity suggests that the activities of cells must be coordinated effectively
(Kaiser, 2001; Mian & Rose, 2011). Thus, this complex multicellularity would
have appeared in separate events (Whittaker, 1969): two times in eukaryotes (once
in Amoebae and Animalia [Metazoa]), three times in fungi, and six times in pho-
tosynthetic eukaryotes (Knoll, 2011; Niklas & Newman, 2020). What is clear
from current phylogenetic analyses is that metazoans all derive from a common
Precambrian unicellular ancestor (Sebé-Pedrós et al., 2017; Giribet &
Edgecombe, 2020).
Let us consider a hypothetical primordial environment dominated by unicellular
organisms (prokaryotes and eukaryotes). In this environment, a new organism arises
either due to a failure to separate cells during division or through simple cell aggre-
gation (Rokas, 2008). Regardless of the specific mechanisms, this new organism
would have been a rarity during its initial stages. At that time, given our current
knowledge of the evolution and success of multicellularity, this phenomenon might
have been regarded as an abnormal form or a “teratology of unicellularity,” particu-
larly if we consider the hypothesis of cell separation failure.
6.2 E-R Changes by Nature’s Action 243

Let us review what the “rules” were thus far. First, there was no persistent group-
ing of individuals. While unicellular organisms can form groups over time, their
communication is limited, eventually relying on chemical signaling in their envi-
ronment (Knoll, 2011). Second, cells lacked specialization or differentiation, mean-
ing that all cells performed all functions. This lack of specialization may have
hindered their exploration of specific niches (Umen, 2014). Third, physiological
limitations and constraints were present during this period. For instance, the size of
single-celled organisms was determined, in part, by diffusion distances within the
cell (Niklas & Newman, 2013). Finally, size also made them prey for other single-­
celled predatory organisms and limited the prey size to be ingested (Niklas &
Newman, 2016).
With this panorama, we see that a novel and unique aspect at that time is the
intimate cooperation between cells, which goes beyond a simple momentary and
random interaction. Then, and here is the rare or at least surprising, it jumps to a
symbiotic relationship between different types of founder cells (Margulis &
Chapman, 1998; Niklas & Newman, 2013). The cells stay together and begin to
specialize, each doing a particular job and getting better and better as they evolve. It
is another process that can be taken as a rarity since the rule was that all the work
was concentrated in one individual, the same cell. After the appearance of multicel-
lularity, the work was distributed. Each cell group was specialized in performing
better actions than the individual cell because, as the famous saying goes: “Jack of
all trades, master of none.” Among several examples, the specialization and differ-
entiation of vegetative or somatic and reproductive cells are notorious (Michod
et al., 2006; Knoll, 2011; Umen, 2014). We previously observed that sex appeared
in metazoans. Among unicellular organisms, reproduction by cell division is the
rule. Some authors even argue that a modification in the cell division phenomenon
could have given way to multicellularity (Bonner, 2003; Niklas & Newman, 2016).
Returning to the division between cell lines, multicellularity brought something
novel to reproduction: restricting it to specific cells. In addition, reproduction was
not through mitosis but through the process of meiosis (Grosberg & Strathmann,
2007) (was it an aberrant process at some point?). As mentioned earlier, meiosis
introduces genetic recombination, leading to a significant increase in diversity
among organisms. This process helped prevent the existence of clonal individuals
who could be easily wiped out by unfavorable changes (Curtis et al., 2008).
Additionally, as we saw, sexual reproduction in unicellular organisms was mainly
by isogamy but changed with the advent of multicellularity that incorporated oog-
amy (Wiese et al., 1979; Umen, 2014; Ruiz-Trillo & Nedelcu, 2015). Oogamy is a
feature that, as we saw, brings many advantages over isogamy. For example, the
nutritional investment in the progeny and the increased chances of collision between
gametes due to the presence of numerous small gametes associated with the males.
Phylogeny and genomics propose a “generalized” trajectory for the evolution of
multicellularity, which initially involves the cooption of existing genes for adhesion
(for further details, refer to the comprehensive review by Knoll, 2011). However,
upon closer examination, this explanation fails to account for the diverse transitions
observed among different groups. For example, plants and fungi followed different
244 6 Focusing on Dynamics: When an Exception Becomes a Rule

trajectories for their respective multicellularity patterns from the initial elements
they had in common (Niklas & Newman, 2013). Indeed, the genetics of organisms
underwent significant changes. To illustrate, imagine the genome as a blueprint out-
lining the execution of routine cellular functions. However, as multicellular organ-
isms evolved with division of labor and cell differentiation, these blueprints had to
be modified since the functions differed from their unicellular counterparts or were
possibly absent in them (Rokas, 2008). This adaptation was necessary to accom-
modate the new complexities arising from multicellularity. Thus, the cells of a mul-
ticellular organism need communication and coordination between different cell
groups, cohesion between cells to form the individual, and differential development
of cell lines that compose it (Rokas, 2008). All aspects are little exploited, totally
absent, or exceptional in unicellular individuals.
Most strikingly, studies in unicellular counterparts show the presence of genes
needed to generate proteins involved in cell–cell junctions and cell–cell signaling
(King et al., 2008; Sebé-Pedrós et al., 2017; Paps & Holland, 2018; Richter et al.,
2018). For example, choanocytes are cells present in sponges (Porifera). These cells
closely resemble free unicellular forms called choanoflagellates. For a long time,
the rule was to associate them directly, but recent studies have suggested that these
are analogous forms that seek to solve the water flow problem at the microscopic
level in a similar way. Indeed, this solution appears in several groups outside
Porifera (Giribet & Edgecombe, 2020). However, choanoflagellates have demon-
strated the ability to coalesce and generate small colonies and are considered the
closest single-celled relatives of animals (King, 2005). The ability to form colonies
suggests that these organisms potentially have the necessary genetic elements.
Studies in a choanoflagellate species, Monosiga brevicollis, demonstrate that the
genome possesses genes ready to encode the protein domains necessary for multi-
cellularity (King et al., 2008; Fairclough et al., 2013; Suga et al., 2013; Sebé-
Pedrós & de Mendoza, 2015).
How can we interpret this from the orbit of rules and exceptions? Imagine that
one would have expected the appearance of these genes to be something fortuitous
that triggered the appearance of the characters linked to multicellular organization.
However, the presence of that information may have been the rule in unicellular
organisms, but what may have been the exception was the manifestation of those
characters that remained deactivated. While there was innovation in the genetic rep-
ertoire at the origin of metazoans, the unicellular ancestor had the basis for cell
adhesion, signaling, and transcriptional regulation (Sebé-Pedrós et al., 2017). In
contrast, some groups lose entirely some of the genes linked to multicellularity. A
case present in current cnidarians is that of myxozoans, an exception among modern
cnidarians. Myxozoans are highly modified cnidarians of parasitic life (Lom &
Dyková, 2006) and are composed of a few cells. They were long considered protists
and presented some of the smallest genomes in the animal kingdom (Chang et al.,
2015). These authors claim that genes that are considered the stars of animal multi-
cellularity were eliminated within this massive genome reduction. This elimination
drastically modified the structural plan of the organism, which is very convenient
for parasitic life. It is conceivable that this should have been the beginning among
6.2 E-R Changes by Nature’s Action 245

unicellular organisms, the absence of the genes for multicellularity and that a modi-
fication in the genome would generate these genes, whose expression would result
in the characteristics that multicellularity, as a phenomenon, needs. However, we
saw that the rule was probably the presence of these genes from the beginning, and
then, they were lost in more derived groups, as in the case of the group of parasites
mentioned above.
It is exciting that currently, we can use analysis models and somehow see the
evolutionary path different organisms could have taken to go from unicellular to
multicellular life. In this sense, sponges are organisms that would present the
first level of organization within eumetazoans. As we saw, the presence of cho-
anocytes makes Porifera a good candidate for the closest ancestor of metazoans,
a place disputed with sea acorns (Ctenophora) (Giribet & Edgecombe, 2020).
This cellular organization is more complex than other unicellular groupings but
less complex than the tissue and organismic types of organizations present, for
example, in cnidarians and Platyhelminthes. Sponges, unlike other animals, can
dissociate their cells and regroup them, forming a new adult organism (Lavrov
& Kosevich, 2014). Although the rule in this group is the absence of actual tis-
sues, it does not prevent some kind of integration, communication, and differen-
tiation in the cells that make up the individual. As we saw, the exception to this
group, in terms of poriferous body constitution, is represented in the class
Homoscleromorpha. Recall that what stands out most in this group is the pres-
ence of an actual basement membrane with type IV collagen underlying the
pinacoderm and choanoderm and more complex cellular connections than in the
rest of the sponges (Chap. 5). These features connect Porifera directly to actual
animals (Gazave et al., 2012).
On the other hand, the green algae Volvocales, also called Chlamydomonadales,
represent a fascinating group from an evolutionary point of view (Umen, 2014).
They represent a rarity for the study of multicellularity because they are one of the
few groups whose representatives can reconstruct the theoretical evolutionary steps
from a unicellular to a multicellular organism. This evolutionary path is shown very
clearly by Umen (2014) and by Niklas & Newman (2013). It starts with the genus
Chlamydomonas, where no cell grouping can be seen, and unicellularity is the rule.
Then, we have Gonium, where we already see cell polarity, cell number modulation,
and cell junctions. Pandorina and Eudorina, on the other hand, are two genera that
show slightly more complex and extensive colonies. Even greater complexity can be
seen in Pleodorina, as it possesses specialization between somatic cells and germ
cells and the presence of anisogamy but not yet oogamy. Finally, the whole level of
multicellular organization is found in Volvox, where oogamy already appears, along
with some other more specific characteristics that determine the conformation of a
multicellular individual (Umen, 2014). The study of this algae group also showed an
“innate” tendency toward multicellularity. What do we mean by this? In this sce-
nario, the initial explanation does not always explicitly involve natural selection.
Imagine, for example, that there was already a combination of multiple cells, pri-
mordial cell mixing, which may have occurred through cooperation, symbiogene-
sis, or a combination of various mechanisms. The role of natural selection may
246 6 Focusing on Dynamics: When an Exception Becomes a Rule

come into play at later stages of evolution, once these multicellular entities have
formed and begun to undergo further changes and adaptations. It is interesting the
comment of Furusawa & Kaneko (2002) in the conclusion of their work when they
state that rather than emphasizing the “emergence” of multicellularity as “a difficult
problem” in evolution, they consider that it arose as a natural consequence of a pri-
mordial colony of cells that could grow continuously. In other words, they perceive
this event (i.e., the origin of multicellular organisms) as an expected and inevitable
consequence of dynamical systems (Niklas & Newman, 2013; Lyons & Kolter,
2015). With a precise computer simulation analysis, Furusawa & Kaneko (2002)
showed that cell differentiation could be triggered spontaneously mainly due to the
intrinsic composition of the cell pool. While the internal composition of cells is, in
principle, very similar, subtle differences ultimately cause differences to exist and
generate cell types.
Thus, transitions between different cell types follow restrictive rules on transi-
tion dynamics. A clear example is transitioning from a totipotent cell to another cell
type of lower rank. The totipotent cell can generate another cell of the same type and
one of lower rank but once differentiated. A cell can only continue to generate its
same type without being able to return to the possibility of generating any cell type
(i.e., it loses totipotency). In this case, it is the growth of a cell colony over time,
where sooner or later, finer cooperation, with a division of tasks, will occur. At least,
this could be seen in the experiment of Boraas et al. (1998) in Chlorella vulgaris,
where after a hundred generations of a unicellular colony, multicellularity emerged
in the presence of a predator.
It showed the adaptive value of cooperating in a multicellular manner, in this
case through colonies of eight cells acting as a functional unit (Stearns &
Hoekstra, 2005).

6.2.1.7 Multicellularity and Cancer

In biology and medicine, there is often a necessity to analyze situations where mul-
ticellularity deviates from a controlled program (Trigos et al., 2018). As we have
seen, the rule in multicellularity is that the cells that compose the organism repro-
duce within a plan and perform the assigned tasks for the organism’s good.
Sometimes these cells get out of control, stop reproducing and working for the
organism’s good, and start doing it selfishly for themselves (Aktipis et al., 2015). It
is the case of cancer cell proliferation. Cancer is rare for multicellular organisms, an
exception for a group of cells that do not differentiate as they should in the tissue
where they are located. The oddity is that these cells selfishly seize control of
resources and do not respond to the communication patterns established within the
organism (Nedelcu, 2020). Therefore, they grow out of control, exhausting
resources, invading tissues, and ultimately killing the organism. Nondifferentiation
as an isolated error may occur in the tissue, but when it becomes widespread
(becoming the pattern or rule within an organ or location within the individual), it is
classified as a disease.
6.2 E-R Changes by Nature’s Action 247

Evolutionarily, cancer is closely linked to the phenomenon of multicellularity

(Davies & Lineweaver, 2011). Aktipis et al. (2015) argue that the generation of a
multicellular organism requires cooperation between cells and mechanisms to sup-
press somatic deception, as cellular-level fitness must be restrained to promote the
overall fitness of the organism. Many genes identified in cancer cells are primitive
and conserved (Weinberg, 1983; Hartl et al., 2010; Srivastava et al., 2010). It is
interesting to note where the exception lies in how these cells work. Studies suggest
that the properties of multicellularity are lost or deregulated as genes associated
with unicellularity are turned on specifically for cancer proliferation (Trigos et al.,
2018). The fact that they are evolutionarily highly conserved suggests that they
serve essential functions in cellular physiology and that their role in carcinogenesis
represents a total exception or an aberrant deviation from the original functions
(Weinberg, 1983). Thus, the genes needed for multicellular cooperation are the
same genes that function incorrectly in cancer cells (Weinberg, 2007).
Currently, cancer is an exception from a natural point of view. However, some
works ponder that very primitive metazoans are tumor-like neoplasms (Davies &
Lineweaver, 2011) since they are colonies where cooperation, adhesion, and
exchange of chemical information are relatively poor. Then, evolutionarily, these
protozoa advanced by improving signaling and coordination. Thus, in the begin-
ning, colonies that behaved analogously to “tumors” may have been the rule.

6.2.1.8 Changes Linked to the “Initial” Invasion of the Earth

In the history of life, there was a time when no organisms inhabited Earth. It is listed
in any textbook of paleontology and evolution. Indeed, it is believed that most life
forms initially evolved in marine habitats. Until the Ediacaran period (ca. 600 mil-
lion years ago), many single-celled organisms inhabited the seas, such as eukary-
otes, prokaryotes, and archaea (Cavalier-Smith, 2006; DeLong & Pace, 2001). From
that time on, a wide variety of multicellular organisms began to develop, including
algae, plants, fungi, and animals that evolved in the sea and, to a lesser extent, in
freshwater habitats (Heckman et al., 2001).
The invasion, conquest, or colonization of land was one of the most fundamental
events in evolution. This new environment without any competitors allowed the
diversification of many organisms, leading to the evolution of new forms, behaviors,
and life strategies. At that particular moment, immediately before this colonization
began, the prevailing rule was “marine life” or, in other words, the sea as the “only”
environment for life. As the invasion of land began, it was evident that, from a group
perspective (in terms of diversity) and the number of individuals per group (den-
sity), living on land was only an exception rather than the norm. At this moment, life
would be unnoticed outside water environments.
It is intriguing to consider that the first individuals to colonize the land may have
been members of a relatively “marginal” population within their species. For exam-
ple, if we were to imagine arthropods that went to land, it would be hard to imagine
individuals well adapted to a deeper life in the sea or freshwater. Instead, it seems
248 6 Focusing on Dynamics: When an Exception Becomes a Rule

more plausible to think of individuals accustomed to living in intertidal zones or

temporary pools, where water availability is subject to evaporation or runoff. That
is, zones where amphibious life could be the intermediate “nexus” to move from
water to land. The data also suggest that marine organisms may have undergone
changes and tolerated brackish waters, such as estuaries. The salt content of the
water is an essential initial aspect to control, so adapting to an estuary may have
been a first step in colonizing terrestrial environments (Sánchez, 2007). Those indi-
viduals of the species accustomed to intermediate, amphibious areas would be the
most suitable for colonizing areas already dominated by air rather than water. Once
again, we highlight the significance of intrapopulation variability, particularly the
individuals exhibiting “extreme” traits (e.g., internalized gills or cutaneous respira-
tion in animals, plant cuticles, and well-defined stomata in plants, which are benefi-
cial for terrestrial life). These specific traits render them better adapted for the
successful colonization of the new environment.
Furthermore, in this context, the initial colonization of land is also linked to a
concept we will discuss later in this book, known as the founder’s principle, which
explores at the genetic level how exceptions can become the rule. Specifically, we
refer to how rare genes within the gene pool of the original population (e.g., marine
organisms) may become prevalent in the population that has already established
itself in the new terrestrial environment (Templeton, 1980; Provine, 2004). Indeed,
if such genetic shifts can occur during the colonization of uninhabited islands, it is
reasonable to assume that even more significant genetic changes must have taken
place during the critical moments of colonization in such an extensive environment
entirely devoid of living organisms. These rare genes (in frequency), which later
become dominant in descendants, likely had significant implications for subsequent
evolutionary patterns in plant and animal lineages. However, the implications of
what was implicitly present, such as the founder principle, during the initial coloni-
zation of a new environment are often overlooked or not frequently mentioned. It
could have been further enhanced if those original pioneer populations suffered a
bottleneck effect by temporarily reducing those new gene pools due to environmen-
tal events or contingency phenomena, such as volcanic eruptions, solid and sudden
climatic changes, etc. In this world of gradual colonization of new environments
and associated processes, such as the founder principle, we should pause to contem-
plate the profound impact exceptions can have on shaping future patterns and rules
in evolution. It is just a sample of the multidimensionality linked to exceptions (e.g.,
exceptions of different types, at different levels—time, space, group—of patterns,
processes, etc.). This book may not fully illustrate all these variants. Nevertheless,
the initial spark will ignite, paving the way for interdisciplinary collaboration among
researchers and readers.
The first living organisms to colonize the land are believed to have been photo-
synthetic prokaryotes that inhabited humid environments near ocean shores, prob-
ably 2.6 billion years ago (Horodyski & Knauth, 1994; Prave, 2002). Thus, despite
the lack of water, terrestrial environments offer an ideal location, with plenty of
sunlight and carbon dioxide for photosynthesis, which makes the colonization of
these spaces possible (Pisani et al., 2004; Sanford et al., 2012; Wu et al., 2014).
6.2 E-R Changes by Nature’s Action 249

Subsequently, the ancestors of present-day plants were able to colonize drier envi-
ronments. It is postulated that a group of freshwater plants gradually advanced to
muddy shores, and actual land plants evolved from there (Heckman et al., 2001).
The flora during the Cambrian was fully marine (Gradstein & Kerp, 2012). Evidence
for the appearance of the first, still rare, land plants occurs in the Ordovician period
(ca. 450 million years ago) in the form of fossil spores, and they began to diversify
later in the late Silurian, approximately 430 million years ago (Wellman et al.,
2003). Conditions improved for plant colonization. The climate was colder and wet-
ter, coastal zones were wide and stable, and soil formation occurred. Spore produc-
tion is considered key in the evolution of land plants (Gradstein & Kerp, 2012; Lei,
2017). It is interesting to see lignin as something that could be considered terato-
logical in a marine aquatic environment, but not terrestrial.
Fungi seem to have colonized the soil at the same time as plants. This association
between an autotroph and a fungus probably favored the colonization and perma-
nence of eukaryotes in the terrestrial environment (Selosse & Le Tacon, 1998;
Heckman et al., 2001). One of the first associations that favored the colonization of
land by eukaryotes may have been the formation of lichens derived initially from a
fungus and a cyanobacterium. This association would have resulted in another type
of symbiosis between autotrophs and fungi, arbuscular mycorrhizae. Today, lichens
together with arbuscular mycorrhizae are the most common symbiotic associations
between autotrophs and fungi (see Sect. 6.4 on plant communication in this chap-
ter). In these associations, fungi assist in the uptake of nutrients, metabolites, and
water while benefiting from nutrients provided by the autotroph (Plackett & Coates,
2016; Audesirk et al., 2008). The early colonization of the terrestrial environment
by plants and fungi likely contributed to the rise in atmospheric oxygen concentra-
tion, promoting the Cambrian explosion of animals (Heckman et al., 2001; Plackett
& Coates, 2016). This point directly relates to the previously mentioned “energetic
expansions” in the planet’s history.
The colonization of the earth by plants was preceded in the early Cambrian by
invertebrate animals. According to the fossil record, the first was Apankura, an
Euthycarcinoid arthropod found in Argentina (Vaccari et al., 2004). This organism
is thought to be the precursor of terrestrial mandibulates, and traces of this animal
found in Canadian deposits also confirm its presence on land (Sánchez Alvarado,
2006). Arthropods were well adapted to life on land because they had an almost
impermeable shell, presumably used for protection (Waters, 2003; Mayhew, 2007;
Pisani et al., 2004). In addition to fungi, the evolution of plants is always closely
related to arthropods, mainly insects. During the early phase of land colonization,
arthropods were wingless, a condition known as “apterous.” This characteristic did
not significantly impact their interactions with plants since, at that time, plants were
generally short in height (Sánchez Alvarado, 2006).
An important evolutionary event associated with the first steps of vertebrates
onto land was the transformation of fins into limbs, thus moving from swimming to
walking and initiating the enormous radiation of terrestrial vertebrates. If we were
to view this event from an approach similar to that of Blumberg (2009), these were
changes that, if they occurred in a stable marine environment, could well be viewed
250 6 Focusing on Dynamics: When an Exception Becomes a Rule

as simple teratologies. In contrast, this is not the case if that change, as we know,
was linked to the colonization of a new environment where the adaptive value is
evident.
On the other hand, the evolution of limbs was preceded by a significant change
in sensory abilities (Nilsson, 2017). During the finned fish to early amphibious tet-
rapod transition, there was an increase in eye size and a shift in position toward the
top of the head. The authors explain this change in the visual system as an adapta-
tion to have better vision in the air (Nilsson et al., 2012; MacIver et al., 2017;
Nilsson, 2017). Again, the reflection on how a series of changes can be, to a greater
or lesser extent, considered teratological versus adaptive will depend on the context
in which it occurs. However, in a time and space context, sometimes the boundaries
could be more precise, as they will depend on the medium- and long-term fitness of
the organism that presents that change.
At this point, it is interesting to slow down and discuss a particularity in the con-
text of rules and exceptions. This refers to the fact that land invasion by plants is
considered to have been a “single event” in the history of life. At the same time,
animal groups colonized the land at different times during their evolution. Land
plants form a monophyletic group that evolved as an adaptive response to migrating
from a subaerial freshwater habitat to a terrestrial environment. Phylogenetic analy-
sis of extant plants suggests that green algae are related to land plants, i.e., land
plants likely evolved from a multicellular freshwater green alga (Wellman et al.,
2003; Pisani et al., 2004; Qiu et al., 2006; Rubinstein et al., 2010; Hanschen et al.,
2016). This monophyly strongly supports a single event of soil colonization by
plants (Plackett & Coates, 2016). Nonetheless, the intricate morphologies that
enabled animals to survive on land originally evolved in aquatic environments and
independently spread to land on multiple occasions. For instance, in the case of
arthropods, it is believed that at least four colonization events occurred, leading to
the independent terrestrial colonization of “myriapods” (centipedes, millipedes, and
related groups), insects, arachnids, and crustaceans (Pisani et al., 2004).
Thus, this unique event in the evolutionary history of plants represents, even
more, a great rarity, an exception, of that time. One so important that it later implied
crucial changes in ecosystems. For example, it facilitated the settlement of other
groups, such as herbivorous animals, as they were already present as the raw food
material (Benton, 2010). In other words, the invasion of animals was presented as
recurrent, multiple patterns, while in plants, everything was born from a single
situation.
In these early stages of colonization, those individuals with rapid growth and
short life spans could have been the ones that were initially successful in coloniza-
tion (Connell & Slatyer, 1977). At this time, these traits, perhaps not common in
the ancestral core population but common in the marginal population, could have
been later replaced by other species with a long life cycle and slower growth.
Here, the rare thing at that early stage of invasion would have been the latter (a
stage that could have lasted thousands of years or more—Connell & Slatyer,
1977). Again, we can always see what was familiar and rare at “x time,” “x space,”
and “x taxonomic group.” Indeed, whether we are discussing rules and
6.2 E-R Changes by Nature’s Action 251

exceptions—not solely based on our perspective of what “should be,” but on the
actual occurrences in nature—or patterns and rarities, the initial colonization of
the Earth encompassed a multitude of situations where this duality was evident, as
we have explored in this section.

Changes Associated with Ecological Succession Mechanisms Among Land

Colonizers

Initial colonization by a given group, e.g., plants, will then impact successive colo-
nizers of other groups, various animals, and so on. In this sense, three models have
been proposed to try to explain the mechanisms that determine the sequence of spe-
cies: facilitation, tolerance, and inhibition (Connell & Slatyer, 1977; Finegan, 1984;
Huston & Smith, 1987; Pickett et al., 1987), something central when we think of a
passage from exception to rule in the framework of colonization processes of new
environments. In the “facilitation model,” early successional species have specific
characteristics that allow them to colonize first, such as the ability to produce a large
number of propagules (Marks, 1974) and improve the conditions of the environment
(food, shelter, soil, and microclimate, for example) to make them more suitable for
later colonization by other species so that they can invade and grow to maturity
(Connell & Slatyer, 1977; Read et al., 2016; Koffel et al., 2018). For example,
among the roots of plants on aquatic margins, a microhabitat was created that was
conducive to many arthropods that were thus able to colonize the land as the first
animals on it (Ridley, 2004). Second, a “tolerance model” has been proposed, which
states that the modifications produced in the environment by the first species that
colonized do not increase or reduce the probability that new species can colonize
the site, nor do they affect the growth of the new species. Species that develop later
are simply those that arrive later. The sequence of species is determined solely by
their life history characteristics (Connell & Slatyer, 1977; Finegan, 1984; Huston &
Smith, 1987; Pickett et al., 1987). Finally, the third model, the “inhibition model,”
proposes that once the first colonizing species secures space and other resources,
they inhibit the invasion of later species or suppress the growth of those already
present. New species can invade only when the first species are damaged or have
died. In contrast to the first two models, here, the species replacing the previous one
need not be a different species adapted to conditions modified in a particular way by
the previous species (Connell & Slatyer, 1977; Finegan, 1984; Huston & Smith,
1987; Pickett et al., 1987). Newly settled species may well have defined the disap-
pearance or caused the disappearance of previously settled species, i.e., pioneers, to
become rarities. However, it is currently suggested that these three models are not
mutually exclusive and that one becomes more important than the other at different
stages of succession. What is certain is that what was initially rare on earth acted as
an indirect driving force for other groups that were also rare in their beginnings.
That is, they were exceptions that established scenarios as rules for those that would
come later. These rarities, whether still in their rarity state or gradually turning into
patterns, influenced what others could or could not do to a certain extent, regardless
252 6 Focusing on Dynamics: When an Exception Becomes a Rule

of whether they belonged to the same clade (e.g., plants to plants) or not (e.g., fungi
such as mycorrhizae–plants; plants–animals; animals–animals).

6.2.2 Perspectives and Cases of when “Oddities” Become

the Pattern

6.2.2.1 Nonrepresentative Individuals Are Settlers

In population genetics, random events play a crucial role in the passing of genes
from one generation to the next. These events, often referred to as genetic drift, are
considered significant in evolution. For instance, in biological evolution, the exis-
tence and strength of random sampling events involving a small number of individu-
als as founders of a new population are well documented. This process presents
changes in the frequency of genes, including some of them associated with diseases.
Genetic drift encompasses processes such as the founder effect and bottleneck.
These processes occur when a new population is established from a small group of
randomly selected individuals (Templeton, 1980). The founder effect occurs when
a small number of individuals break away from the original population and colonize
new territory. These individuals may possess rare genes in the original population.
Thus, these rare genes in the population will now be more common among the
descendants, affecting the original genetic variation (Templeton, 1980; Clegg et al.,
2002; Peter & Slatkin, 2015). The full founder effect requires not only a founder
event but also that the founder individuals are not genetically representative of the
original population.
On the other hand, a bottleneck effect occurs when an environmental catastro-
phe, such as an earthquake or a tsunami, eliminates most of the population at ran-
dom, and only a few individuals survive regardless of the genes they have
(Templeton, 1980; Cornuet & Luikart, 1996; Peter & Slatkin, 2015). Human behav-
iors can also act and produce bottleneck effects. For example, a species that suffered
from bottleneck effects is the northern elephant seal (Mirounga angustirostris),
which was hunted to near extinction. When the population recovered, less genetic
variation was observed among individuals (Hoezel, 1999). It is interesting to note
that both processes produce variations in allele frequencies, resulting in a decrease
in the population’s genetic diversity (Hoezel, 1999). Some genes may be eliminated
from the population, while others that were rare now become more common in the
new population. The link between founder and bottleneck events is the randomness
with which individuals are selected.
Gene drift processes differ from natural selection in that gene drift eliminates
individuals randomly. For example, a pest can only kill individuals lacking a par-
ticular gene (Lande, 1976). The genes with the best survival qualities are passed
onto the next generation in natural selection. Thus, we could discuss whether the
choice of the founding individuals of a new population was random or actually by
natural selection, e.g., they are the strongest, better able to expand and travel to the
6.2 E-R Changes by Nature’s Action 253

new site, etc. The truth is that we have illustrative examples (mainly from the world
of flies) that show how few individuals can initiate a new population. This popula-
tion’s allele frequencies will differ from the ancestral allele frequencies due to the
founder effect and may or may not contribute to speciation processes. Such is the
case for Drosophila hawaiana (Carson & Johnson, 1975; Templeton, 1979a, 1980),
D. mercatorum (Templeton & Rankin, 1978; Templeton, 1979b), D. silvestris, and
D. heteroneura (Carson & Kaneshiro, 1976). In other cases, however, the effects
alone are not as decisive as those observed in other Drosophila species that have
undergone founding events without speciation. This is the case, for example, of
D. melanogaster itself (Powell, 1978; Templeton, 1979b, 1980). Additionally,
within vertebrates, in some island-colonizing birds, the genetic variability of popu-
lations did not show a significant decrease (Charlesworth & Charlesworth, 1987;
Moya et al., 1995; Clegg et al., 2002). Thus, only a minority of the processes linked
to genetic drift lead to speciation. It could depend on specific characteristics of the
original population, such as its original structure, genome, mating system, and
mutations (Templeton, 1980). For example, concerning the structure of the original
population, different ancestral population models have been described that can
influence the selection of founder individuals, including the panmictic population
model, Wrights Island model, and “Yanomama” model (Nei et al., 1975;
Templeton, 1980).
Interestingly, more clarity is needed as to whether the emergence of speciation
derived from gene drift events is expected. However, even so, it should not be under-
estimated since it does exist. In this regard, the words of Templeton (2008) stand
out: “Although rare, founder speciation can have a disproportionate importance in
adaptive innovation and radiation, and examples are given to show that ‘rare’ does
not mean ‘unimportant’ in evolution.” It is worth noting that the terms “rare” and
“exceptional,” as applied to speciation by founder events, do not diminish its signifi-
cance within an evolutionary framework.
On the other hand, the individuals who originate the new population often come
from a marginal (i.e., noncore) subpopulation of the species. This “sample” in itself
may not be representative of the genes of the ancestral population. Thus, individuals
colonizing previously uninhabited spaces are descendants of those living near the
“expansion front” of the original population (Hallatschek et al., 2007; Klopfstein
et al., 2006; Peter & Slatkin, 2015). In some populations, a phenomenon known as
the “spatial ordering of individuals” may occur. This happens when individuals with
traits that enhance dispersal tend to accumulate at distribution edges (Phillips et al.,
2010). This arrangement promotes the frequency of dispersal-promoting genotypes
to be higher in expanding ranges of populations (Phillips et al., 2010; Szűcs et al.,
2017a). Indeed, in this case, we encounter a situation that can be considered an
exception both quantitatively and qualitatively. These populations may carry rare
alleles that will become the most common after the foundational event concludes.
Thus, we see that while the genes would be mainly those of the ancestral popula-
tion, the allele frequency would not. We now have a significantly high frequency of
alleles that were originally rare in the average population but prevailed in the
“extreme” sample that eventually formed the foundation of the new population. The
254 6 Focusing on Dynamics: When an Exception Becomes a Rule

characteristics of that sample, which will be the ones that migrate and finally colo-
nize the new territory, will be crucial. Implicitly, if the sample of a few individuals
came from the middle, more representative population, we would not see such a
marked and evident “effect” of the founder. This effect is seen in cases where the
members of the founder sample present a disproportionate number of these “rare”
alleles.
It is worth mentioning that homozygosity as such could not be expected from a
founder effect but from restriction in allele frequency. Changes in allele frequency
can be very dramatic and can be modeled (Slatkin & Excoffier, 2012). What is cer-
tain is how critical the founder effect may have been for the expansion of popula-
tions (Peter & Slatkin, 2015). Range expansion refers to the expansion of a
population from a small region to a much larger region. These expansions are com-
mon in many species and occur on different time scales depending on the species
(Peter & Slatkin, 2015). For example, two theoretical population genetic models
refer to the range of population expansion. The first describes the change in allele
frequency over space due to differences in dispersal and fitness in a continuously
distributed population.
In contrast, the serial founder model assumes discrete locations that can be colo-
nized by the population and not so extreme differentiation (Ramachandran et al.,
2005; Slatkin & Excoffier, 2012; Peter & Slatkin, 2015). This links directly to the
concept of variability we discussed in the previous sections regarding the extremes
of expression of a trait and, thus, the individuals carrying that expression.
Furthermore, it is possible for founders to include either multiple individuals or a
single fertilized female [as per Mayr’s definition from Mayr (1963)]. In some cases,
these individuals may belong to an extreme quartile of the trait within the original
population (Nei et al., 1975; Cornuet & Luikart, 1996). It could, as we said, be even
stronger if it is already in a marginal distribution and, therefore, already exhibits a
previous state of “low genetic representativeness.” This founder could also possess
a novel character associated with an adaptive function per se (see next section). It
could even be an individual with a quasi/or fully heritable teratological trait and/or
a carrier of diseases, something seen, for example, in some human colonizations
(see Fix, 1997—on cline formation of gene frequencies produced by the effect of
the founder).
There are multiple examples of founder effects in biology. As well compiled by
Ridley (2004), a “natural laboratory” has been the colonization processes of humans,
where medical anomalies can be seen in cases of foundational processes by scarce
colonists, where the progenitors were carriers of those alleles. For example,
Huntington’s disease (a genetic disease with an abnormal dominant allele that dis-
rupts the function of its nerve cells) is more common in Venezuela and South Africa,
with Dutch ancestry, than in most other populations. This is because the gene carry-
ing this disease was widespread among the small group of original Dutch settlers
(Zeegers et al., 2003). Another example is the disease known as porphyria variegata
(where an autosomal dominant gene produces a defective form of the enzyme pro-
toporphyrinogen oxidase). Individuals carrying this gene suffer a severe reaction to
anesthetics. This disease is widespread among the white population of South Africa
6.2 E-R Changes by Nature’s Action 255

with Dutch ancestry (Dean, 1982). To these examples, we can add that of the
Pennsylvania Amish with German and Swiss ancestry, which was established in the
United States in the eighteenth century (Curtis et al., 2008). This group has a high
incidence of dwarfism and extremities with supernumerary fingers (polydactyly)
called Elis-van Creveld Syndrome (McKusick, 2000). By chance, the members who
migrated to the United States carried that rare recessive allele that, in homozygosis,
manifests the syndrome. The Amish are a very close group with a high rate of
inbreeding, which makes homozygosity prevalent. The incidence in the group is so
high that their numbers resemble those reported for the rest of the world (Curtis
et al., 2008). We will see other examples later when discussing disease incidences
and rare diseases in Chap. 8.
From the above, it is then clear how the rare could become common because of the
founder effect. However, implicitly (although it is not usually stated in the texts), we
have that the common can become rare or even disappear, as we will explain in the
next chapter. Following the example of allelic frequency, common alleles would
become rare now in the population once settled in the new place. Interestingly, the
spatial context is crucial here since it refers, even implicitly, to founders coming from
elsewhere (see above for range expansion). Founding individuals encounter a differ-
ent environment from where they originated. Therefore, it is crucial to understand the
processes that will determine the successful colonization of new environments (Szűcs
et al., 2017b). The number of individuals founding the new population appear to be a
determinant of colonization success in various taxa, as it affects demographic and
genetic processes (Colautti et al., 2006; Blackburn et al., 2015). Thus, whether the
founding individuals are genetically and phenotypically diverse increases the estab-
lishment success of the new population (Forsman, 2014; Szűcs et al., 2017b).
However, in the framework of random sampling, we could alternatively refer to
cases where the context of time, rather than space, would be the most gravitating
factor in the changes in allele frequencies (making the rare familiar and vice versa).
This is because the change can occur in situ in the same space but is progressively
more and more marked over time. We already mentioned this when a population
passes through a bottleneck. Indeed, when an initial population in a new territory or
even a perfectly established population suffers a significant reduction in the number
of individuals at random, those that survive will then expand their alleles in the
descendants (Nei et al., 1975; Cornuet & Luikart, 1996; Hoezel, 1999). For our
book, the common denominator is the dynamics between R and E. For example, we
would pass an R (an x allele) to be an E after the bottleneck and perhaps an E (z
allele) to R after the bottleneck. Then, by starting its expansion, we already have a
change from what was once a common genotypic-phenotypic manifestation, the
pattern, the norm, the rule, to an exception or perhaps disappearance.
Conversely, something that was rare will now become common, the rule.
Everything will depend on whether the survivors associated with the genetic drift
processes (founder effect and bottleneck) had alleles or allele frequency markedly
different from the predecline population mean. Thus, we saw how the founder and
bottleneck effects provide us with examples of something going from “rare” (in
fact, this is used for “rare alleles” Ridley, 2004—p 176) to common. Finally, we
256 6 Focusing on Dynamics: When an Exception Becomes a Rule

now see the connection with the ideas of evolution by contingency discussed in
Chap. 1, when specific evolutionary processes are initiated by contingency events
(understanding contingency effects as what may or may not happen) rather than
processes linked to natural selection (Fig. 6.1a, b).
What has been exposed in this section comes from something very classic in
evolutionary biology, where it is appreciated that rarities exist in variability and that
they can and have a great value for understanding what is later seen in derived popu-
lations. In the next section, we will analyze more about how trait rarities can be the
critical element in establishing, in populations and species, novelties within the
framework of phenotypic plasticity.

Fig. 6.1 Processes that can cause rare alleles to become common in the population. (a) Bottleneck
effect. (b) Founder effect. (c) Environmentally induced phenotypic changes. A genetically diverse
population undergoes a disturbance in the environment, where different genotypes differ in their
response to the new environment. Selection acts and favors the genotype that produces the pheno-
type that best adapts to the new environment (Modified from Levis et al., 2018)
6.2 E-R Changes by Nature’s Action 257

6.2.2.2 Minorities Channeled Via Phenotypic Plasticity

This extreme case of the appearance of a new trait, not linked to anything homolo-
gous to an ancestor, is a rarity in its initial stage. Both this situation and the previous
one (of a phenotypic trait within the distribution range of the trait and present in a
few individuals) connect to underlying genetic level variations. These variations
may be minor or hidden. This links directly to cryptic genetic variation (CGV), a
concept applied to the appearance of morphs within a species adapted to particular
environments. CGV is a “genetic variation that normally has little or no effect on
phenotypic variation except under atypical conditions” (Levis & Pfennig, 2016).
The conditions that induce these cryptic genetic variations are usually rare or absent
in population history. It limits the opportunities for selection to act on that variation
and allows it to accumulate. The CGV then provides a pool of permanent genetic
variation, facilitating adaptation when a rare condition becomes common (Paaby &
Rockman, 2014).
When a trait emerges solely due to environmental induction, the genetic varia-
tion linked to the appearance of this novel trait becomes evident when there are
changes in environmental conditions. In that context, the variation is manifested by
an increase in the heritability of the trait, which will then be evolutionarily select-
able (Queitsch et al., 2002; Ledón-Rettig et al., 2014). However, the way variability
is experienced is not uniform across all organisms. For instance, animals can adapt
to varying resource availability through their mobility, minimizing heterogeneity.
On the other hand, plants, being sessile, begin their life cycle under specific condi-
tions that may change over time, and they lack the ability to counteract these
changes. Thus, plant survival and reproduction depend on tolerance to environmen-
tal extremes, which may be made possible by plastic responses (Bradshaw, 1965).
For example, crucial adaptive variation in plants involves differences in leaf mor-
phological, anatomical, and physiological characteristics along environmental gra-
dients (light, water availability, etc.). These variations can be observed between
species, populations of the same species, and even between leaves produced by a
single plant. They can be maintained over time according to environmental charac-
teristics, allowing tolerance to change and maintaining that new trait as a common-
ality (Wells & Pigliucci, 2000).
Indeed, this hidden variation, which may have minimal or no impact on pheno-
typic variation under typical conditions, can play a crucial role in “atypical” cir-
cumstances, where it becomes evident and acts as a cornerstone for later refinement
of the novel trait through genetic accommodation. This refined expression of the
trait can then become adaptive in a specific context. This is what is proposed by
the “plasticity-first hypothesis”, a mechanism of adaptive evolution in which envi-
ronmental perturbation leads, through phenotypic plasticity, to developmental
reorganization (through, e.g., of altered gene expression) and uncovers “cryptic
genetic variation” to, and ultimately the production of, a novel developmental
variant that immediately undergoes “phenotypic accommodation” and is subse-
quently refined through “genetic accommodation” (Levis & Pfennig, 2016)
(Fig. 6.1c).
258 6 Focusing on Dynamics: When an Exception Becomes a Rule

Here, we see two curious elements in the framework of the present book. How
something that is “hidden” is not hidden under certain conditions, which could be
the tip of something novel, which in turn is initially a rarity. In addition, the concept
appeals to “atypical” conditions in which this could occur so that this GCS is dis-
covered. As we see, concepts of rare and atypical are again ingredients at play in the
beginnings of an adaptive process, from minor variations of atypical environmental
change (in a broad, external sense). The novel will have the potential to continue
polishing and adjusting to that new environment (i.e., have more sensitivity, adjust-
ment, fit, coupling, and bound to that environment). Darwin’s own words come to
mind (1859) when referring to the degree to which the organization tends to prog-
ress, which sounds in a certain way indirectly linked to this subject: “...the final
result is that every being tends to perfect itself more and more concerning the condi-
tions” (pp. 153). This “perfecting” to which he referred well is, in this framework,
given by that adjustment to the new environment (e.g., via genetic accommoda-
tion—Levis & Pfennig, 2016).
It is striking that plasticity will be the requirement to be less sensitive (i.e., less
adjusted, limited to a single environment) but may then lead to new traits that may
eventually become more sensitive, adjusted to that change that occurred. Moreover,
this new morphotype, also adapted to its primitive environment, will coexist or not
coexist with the ancestor if it is present. An example is the spadefoot toads, common
in southern Canada, USA, and Mexico, of the genus Spea, which presents a new
carnivorous morphotype (Spea multiplicata), something unusual in this group. This
trait is presumed to have arisen via plasticity-first evolution. Today, two morphs
coexist, an ancestral, omnivorous morph and a new, carnivorous morph. The dynam-
ics between them are interesting. The tadpoles of this species consume mostly plant
material. However, they can also be facultative carnivores, depending on the cir-
cumstances of the environment in which they grow, and can even eat smaller tad-
poles of their species. It ensures the growth and metamorphosis of at least part of the
offspring (Levis et al., 2015). Today, we cannot say that one is the rule and the other
the exception, but perhaps the minority is, in any case, the carnivore.
It is intriguing to observe that at the initial stages of the evolutionary process
leading to the emergence of this new morph, there was an inherent situation of
exceptionality. This is true unless one postulates that it was a massive generalized
explosion of the same cryptic genetic variation, manifested at the same time in the
majority of the population subjected to an atypical environment (i.e., the one that
led to the selection of some morphs). Following the line of Levis et al. (2015), this
seems unlikely, as in many or most cases in evolution. The exception, initial rarity,
in terms of frequency of distribution and abundance of that morph (i.e., individuals
possessing that new trait or expression of an already existing trait such as body
size), is in itself—from the statistical point of view—an exception. Thus, we quickly
connect the above with the chapter on exceptions.
Importantly, the examples mentioned regarding the role of phenotypic plasticity
in the emergence of new morphs refer to an intraspecific phenomenon. In other
words, this does not necessarily imply the formation of a new species or a process
of speciation; rather, it focuses on variations and adaptations within the same
6.2 E-R Changes by Nature’s Action 259

species. Nevertheless, it is evident that the appearance of new traits via phenotypic
plasticity will connect with speciation processes in the event of subsequent changes
in more extreme environments. Especially at the level of sexual preferences and
sexual recognition, in short, pre- or postzygotic barriers of isolation between the
new morph and the morph that gave rise to it (precedent, ancestor, as it is better to
say). It has been argued that adaptive phenotypic plasticity can promote diversifica-
tion and speciation through its effect on selection and gene flow (West-Eberhard,
2003; Wund, 2012). Populations with plastic phenotypes that arrive in a new envi-
ronment may be more likely to persist because they are more responsive to environ-
mental demands (West-Eberhard, 2005; Pfennig et al., 2010). When this plasticity
is adaptive, the plastic population will be closer to optimal fitness, which may result
in directional selection and consequently reduce gene flow and lead to speciation
(Ghalambor et al., 2007; Crispo, 2008).
In addition, other examples of plasticity can also be observed in nematodes,
where in some species, there is an evolution of food structures, promoting novel
traits (Susoy et al., 2015). In some crustaceans, such as Daphnia melanica, there is
a regulation of the melanin gene that allows for reduced pigmentation and adapta-
tion to environments with novel predators (Scoville & Pfrender, 2010). In reptiles,
for example, snake populations that frequently encounter large prey can accumulate
mutations that result in larger head sizes (developmental adaptive plasticity) (Aubret
et al., 2004). In birds, several species inhabiting noisy environments develop the
ability to show changes in spectral settings and higher frequency songs (Slabbekoorn,
2013). (see Levis & Pfennig, 2016 for details). On the other hand, phenotypic plas-
ticity can also be observed in plants, allowing some populations’ novel traits to
become pattern traits. In some acacias, resistance traits are induced and expressed
in response to herbivore attacks (see Sect. 6.4.2.3). However, in other Central
American species, which ants obligately inhabit, extrafloral nectar is secreted. This
nectar is an indirect resistance, attracting ants that defend the plants from herbi-
vores. The phylogeny of Acacia and other closely related genera indicates that
induced nectar production is the “original” state, while constitutive extrafloral nec-
tar flow is derived within the Acacia genus. A constitutive resistance trait has
evolved from an inducible trait in response to particular functional demands (Heil
et al., 2004). It is interesting to mention here one of the open questions left by these
authors to explore in the future: are there particular taxonomic groups and traits
more likely to undergo evolution by plasticity-first than others, and if so, why? This
question is common to other problems or situations in evolutionary biology and
connects to others posed earlier in this book, such as whether transitions from E to
R are more common in certain groups than others and, if so, why.
Furthermore, numerous instances of plasticity, whether behavioral or morpho-
logical at the trait level, in general can enhance adaptation to new environments.
Interestingly, these plastic responses can be further reinforced through hybridiza-
tion processes, which aid in rapid expansion and adaptation. It may involve species
exotic to that particular site (see below on introduced species) or range expansion in
an area where it was already present. The combination of several factors, such as
personality, communication, metabolism, hybridization, etc., means that the rapid
260 6 Focusing on Dynamics: When an Exception Becomes a Rule

evolution of multiple traits can occur during the range expansion processes of the
organism in question (see Canestrelli et al., 2016). Range expansion requires the
colonization of a new environment, which was previously inhabited by the focal
species. During this expansion phase, essential traits favoring dispersal are those
remaining at the dispersal front, being maintained in new generations and, in turn,
accelerating the establishment of populations in colonized areas (Travis & Dytham,
2002; Phillips et al., 2010; Shine et al., 2011).
Recent eco-evolutionary experiments on expanding populations support the pre-
diction that rapid evolution can accelerate the rate of population expansion (Williams
et al., 2019). Experiments conducted, for example, on red flour beetles (Tribolium
castaneum), demonstrated that the rapid evolution of existing traits increases the
speed of population expansion in individuals at the expanding edge (Weiss-Lehman
et al., 2017). Experimental populations moved faster where evolution was operating.
Several animal personality traits have a degree of plasticity that can vary between
individuals in response to factors related to both ontogeny and adulthood
(Dingemanse et al., 2010). It adds a level of greater complexity but also more sig-
nificant variation available during range expansion. On the other hand, phenotypic
changes appearing during the expansion phase could also strengthen species recog-
nition and increase divergence in selected traits, e.g., sexually, promoting selective
mating (Cardoso et al., 2014). It would contribute, for example, to the construction
of isolation barriers before mating.
In sexual selection, traits linked to choice must be preferred by the chosen sex
within a population. Additionally, these traits may change if the preference is altered
or changed. For example, traits that enhance dispersal will increase the frequency at
the expansion front (Shine et al., 2011), potentially increasing mating rates. Females
may become more flexible in their choice due to a shortage of potential mates.
Thus, the overall process is more complex (i.e., not so univariate in terms of fac-
tors). Indeed, something as rare as hybridization could be used to fuel the emer-
gence of more genetic diversity. It is crucial and widespread, for example, in plants
(e.g., Rieseberg et al., 2007) when adapting to a new environment, and even more
so if it is entirely exotic (e.g., see below cases of introductions in Australia). When
related species live in sympatry and hybridization occurs, genes from one species
are added to the genetic material of the other, or new hybrid gene combinations can
be established (Barton, 2001). However, regardless of the mechanism, if these new
combinations improve growth and the ability to compete in novel environments,
invasion success may increase (Ellstrand & Schierenbeck, 2000; Blumler, 2003).
However, increased invasiveness could be due to increased genetic variability and
the fixation of new gene combinations and phenotypes (Arnold, 1997).
To this scenario, we should add behavioral plasticity as something “key” so that
new morphological variants can finally become established. Body modifications are
not dissociated (West-Eberhard, 2003) but are linked to specific behaviors—for
example, using a new food resource, avoiding a new predator, or maintaining body
temperature (Zuk et al., 2014). In the case of flexibility in antipredator behavior, this
allows animals to respond quickly to changes in the predation environment (Lima &
Dill, 1990). Response behavior to new predation threats may lead to the establish-
ment of novel traits. It may allow populations to persist long enough for
6.2 E-R Changes by Nature’s Action 261

evolutionary adaptations to occur or expose them to new selection pressures.

Plasticity in this type of behavior has been observed, for example, in populations of
Sceloporus undulatus lizards, which perform body contractions and flee from attack
by invasive ants of the species Solenopsis invicta. These behaviors have not been
observed or are rare in these populations (Langkilde, 2009), but when present, they
cause them to increase survival, both by reducing encounters with these ants
(Freidenfelds et al., 2012) and by eliminating encounters if attacked by them
(Graham et al., 2012; Langkilde & Freidenfelds, 2010). In addition, lizards inhabit-
ing sites invaded by these ants have also evolved to have longer hind legs, which
allow for increased efficiency in behavior against these predators (Langkilde, 2009).
In essence, any trait that undergoes modifications at the somatic level should
also, by implication, be associated with ethological plasticity. This means that for a
newly expressed genetic variant to be effectively utilized and beneficial in an ani-
mal’s life, it needs to be appropriately coupled with plastic behavior. The alignment
between the genetically expressed trait and the corresponding plastic behavior is
crucial for successful adaptation to the new environment. If there is an incompatible
match or a lack of alignment between the two, it may lead to difficulties in long-­
term persistence or a challenging mismatch when attempting to adapt to the new
conditions. However, there may be certain limitations to innovation in terms of
behavior. Although some changes can be advantageous, too rapid a change can have
negative consequences (Berends et al., 2010). One example is the inconvenience of
making changes in the face of transient ecological circumstances. Innovation may
involve high costs. Therefore, a new solution may be equally beneficial as detrimen-
tal. It could justify limitations in accepting novel behavior (Brosnan & Hopper,
2014). Thus, innovative individuals do this primarily when their pattern behavior
(their rule) is no longer beneficial, and therefore, change would bring them a more
significant advantage. Brosnan & Hopper (2014) suggest that individuals only
explore alternative strategies when there is an obligation to go through unavoidable
circumstances. The interaction between the individual and the environment will
determine whether those new strategies are maintained.
In this way, if sufficiently substantial, changes in the environment could lead to
the emergence or expression of new traits, perhaps initially represented by a minor-
ity in populations. This implied a rarity, a rare trait. Indeed, these seemingly “rare”
traits can, in certain instances, serve as a means to counteract environmental changes
that might currently be unfavorable. Over time, these traits can acquire value and
become selectable or heritable, providing a mechanism for organisms to adapt and
thrive in their changing environment. It is how so-called minorities sometimes end
up becoming, over time and as a result of evolutionary processes, the rule or pattern
that allows populations to continue to exist, albeit in a different way.

6.2.2.3 Beginning of Coevolution Between Plants and Pollinators

As we started commenting in the previous chapter, the role of animal pollination is

a point today undisputed in the evolution of angiosperms, even considered a key
factor for the diversification of the group and specialization of many of its species
262 6 Focusing on Dynamics: When an Exception Becomes a Rule

(Kay & Sargent, 2009; Sadava et al., 2011; Willmer, 2011). The ecology and evolu-
tion of plant–pollinator interactions can be very complex, depending on the degree
of generalization versus specialization of the animals involved (Herrera, 1996;
Mitchell et al., 2009; Willmer, 2011). How this level of coevolution was reached is
somewhat controversial. The origin of such an interaction may be no different from
that of any animal–animal or plant–plant interaction. However, the importance of
animal-pollinator function, to the point of being the engine of plant evolution, is of
great magnitude. It can be argued that, like all origins, this interaction began as
a rarity.

A Little History

Initially, pollination by abiotic agents was the rule. In the Carboniferous, ferns and
related plants had dust-like spores dispersed by wind (anemophilous dispersal). The
heights of many of the tree ferns must have allowed them to use the wind very effi-
ciently. The first seed-bearing plants were the conifers and related groups (gymno-
sperms) that dominated alongside the dinosaurs at the end of the Paleozoic period.
Pollination was commonly wind-mediated without flowers but with seeds, and
today, that is still the norm for most. However, as early as the Paleozoic and pro-
jected in some species that survived to the present, we can see insect-mediated pol-
lination, particularly featuring some flies, beetles, and moths. The fossil record
shows that in the beginning, pollination was very much linked to predation by pol-
linating agents and that the process was poorly articulated at the time. Today, the
exceptions to anemophilous pollination within gymnosperms are Cycadales and
Gnetales. Gnetum, Ephedra, and Welwitschia stand out in a particular group of
gymnosperms. Cycadales and Gnetales are pollinated by dipterans, noctuid moths,
or beetles (Willmer, 2011; Fogden & Fogden, 2018). Flowering plants evolved rela-
tively recently in the Cretaceous. With them came numerous adaptations that
coevolved with pollinators, resulting in an explosion of diversity in both groups
(Sadava et al., 2011). Many novel nutritious foods have appeared, such as pollen,
nectar, fruits, and seeds (Fogden & Fogden, 2018). The first to interact and take
advantage of this new world of nutritional resources were insects, followed by ver-
tebrates, particularly mammals and birds. The truth is that this condition, still not so
common at the time, was expanding. Flowering plants directed the shift from
abiotic-­mediated pollination to biotic-mediated pollination. As an exception to this
rule, some groups became anemophilous again (Charlesworth, 1993; Schoonhoven
et al., 2005).
An exciting aspect arises when evaluating the planetary scale. The rule seems
that anemophilous species of flowering plants increase with latitude and elevation.
It is crucial because it is directly related to the precision of pollination between
abiotic and biotic factors. Pollination mediated by biotic factors is much more effec-
tive and accurate. Imagine that the wind is less intense in dense and humid forest
areas, so that this system could be more efficient in such places. The target is gener-
ally well localized, and the interacting structures are shaped by years of evolution
6.2 E-R Changes by Nature’s Action 263

(Schoonhoven et al., 2005). There will be a progressive tendency toward the

improvement of the plant to “take better advantage of its animal vector” to carry its
pollen to another flower, from the resident, or donor, to the recipient, located in the
same or different individual, depending on the type of reproduction (Graham
et al., 2006).
In this sense, the current rule in flowering plants is hermaphroditism (both sexes
in the same flower) (Renner & Ricklefs, 1995; Vamosi & Vamosi, 2004; Schoonhoven
et al., 2005; Jarne & Auld, 2006). While there are exceptions, with many groups
having separate sexes (in distinct monoecious flowers or distinct dioecious indi-
viduals, Graham et al., 2006), more than 80% of plants have flowers with both male
and female reproductive organs (Willmer, 2011). Common sense would say this is a
good strategy because they can self-fertilize (Jarne & Auld, 2006) and thus ensure
seed production (Schoonhoven et al., 2005). While it is vital to ensure fertilization,
it is more critical to ensure variation in the progeny in case of coping or a sudden
environmental change (Darwin, 1859; Futuyma, 2013). Thus, many flowering plant
species avoid self-fertilization with physiological, temporal, and spatial mecha-
nisms (Fogden & Fogden, 2018). For example, like many other plants, orchids avoid
self-fertilization (Darwin, 1869; Proctor et al., 1996). However, there are examples
of orchids pollinated by insects that may become facultatively self-pollinating in
areas where insects do not carry out pollination or are directly absent (Proctor et al.,
1996). Thus, the orchid turns to self-fertilization because seed production with little
genetic variability is much better for plant fitness than no seed.

The Flower and Its Rewards

The flower as a unit can be taken as a natural billboard. It provides much informa-
tion to pollinators with its structure, shape, colors, etc. (Graham et al., 2006). Fossil
evidence shows that primitive flowers present many reproductive structures and spi-
ral arrangements. This rule, which probably existed from the beginning of the
appearance of flowering plants (Angiosperms), has changed and is currently only
represented in basal groups such as the Magnoliaceae. The current rule is regular
radial symmetry and structures shaped according to the interaction with pollinators
(Willmer, 2011). There is a tendency toward three-dimensional flowers that favor
recognition by the pollinator, and the reproductive structures are better positioned to
interact with the pollinator (Schoonhoven et al., 2005). If we discuss evolutionary
primitives and take the example of Magnoliaceae, the culmination of evolutionary
change would be orchids. We will see how evolution can mold curious but effective
floral forms.
A significant milestone for the interaction success between pollinators and plants
is the appearance of rewards for the pollinator. It all started with pollen rewards for
the transfer of pollen itself. While one might think this would result in an enormous
production of pollen, compared to the production in wind-pollinated species, it is
considerably less. However, the evolutionary response to optimize the reward pro-
cess was to switch from pollen consumption to nectar consumption. This change
264 6 Focusing on Dynamics: When an Exception Becomes a Rule

resulted in a benefit for the plant since pollen is much more costly from an energetic
perspective than nectar. This is a nice strategy since nectar is sugary fluid and recall
that a plant to run short of carbohydrates would be an exception.
In rare cases, some plants produce repellent pollen or nectar (Adler, 2000;
Schoonhoven et al., 2005; Patiny, 2011; Stevenson, 2020). It could be posited as an
exception since rewards are a significant part of the pollinator-plant relationship. In
this context, it is difficult to explain why generating rewards that would be detri-
mental to the pollinator is an essential intermediary for plant reproduction. Several
authors agree that the modularity of the plant–animal interaction (pollinator or her-
bivore) could partly answer this question (Adler, 2000; Stevenson, 2020). Many
hypotheses claim benefits for the plant, such as favoring specialist pollinators, scar-
ing away nectar thieves or low-quality pollinators, and modifying pollinator behav-
ior, among others (Adler, 2000; Rivest & Forrest, 2020). It is also believed that toxic
pollen may result from past selective pressures that do not operate today. However,
the adaptive validity of this phenomenon has yet to be demonstrated experimentally
(Adler, 2000). Unfortunately, to date, the origin and function of toxic nectar have
yet to be fully understood.
Other rewards are comparatively more exceptional than pollen or nectar, such as
oils, resins, perfumes, and egg deposition sites (Patiny, 2011). These exceptional
rewards limit the diversity of pollinators ready to do the job. Within these examples
of exceptional rewards is the case of butterflies (Ithomiini) that use alkaloids from
the flowers of certain species of Boraginaceae and Asteraceae to produce phero-
mones. Males use these pheromones to attract females and generate receptivity-­
inhibitory compounds that are transferred after copulation (Fogden & Fogden, 2018).
One rule applicable to pollinators is redundancy (Willmer, 2011). This suggests
that a pollinator can pollinate more than one type of plant, and a plant can receive
more than one type of pollinator. Thus, if one of the two were to become extinct, the
remnant would not a priori be in danger. On the side of the exception to this phe-
nomenon are the cases of extreme codependency, where we can cite the iconic case
of wasps and the fig tree (Ficus spp.), and moths, and the cassava plant (Manihot
esculenta). The punctual case of wasps and fig trees is a classic example of 1:1
specificity and represents a firm rule in this interaction. However, this may be a
somewhat reductionist approach to the subject (Cook & Rasplus, 2003), and there
are papers suggesting exceptional cases of this rule (Rasplus, 1996; Michaloud
et al., 1996).

Mutualism and Deception

While the plant–pollinator interaction is considered mutualistic, there is an underly-

ing conflict: exceptionally, some plants cheat their pollinators (Dafni, 1983; Willson
& Ågren, 1989; Ellis & Johnson, 2010; Ackerman et al., 2011). An alternative to
this norm of reward production is the production of deception structures or sub-
stances, a situation where mutualistic equality is twisted to the side of the plant
(Proctor et al., 1996). Overall, deception in the plant–pollinator interaction is rare,
6.2 E-R Changes by Nature’s Action 265

but it is not as rare as one might expect. These resources bet on pollinators being
mistaken, but as a resource, they are less effective since these plants tend to receive
relatively few visits (Baker, 1976; Little, 1983). There are different levels of decep-
tion. Simple levels, where plants falsify the amount of pollen available (Proctor
et al., 1996; Shrestha et al., 2020), and more complex levels of deception, where
mates and egg deposition sites are simulated. It occurs, for example, with sapro-
phytic organisms and plants that simulate decaying matter or where the flower is
modified in the form of a prison where insects are trapped, loaded with pollen, and
then released (Urru et al., 2011). Finally, there are extreme levels of deception
where plants mimic so accurately that they can simulate, smell, and even look like
females of certain insect groups and even generate false copulations with young or
unsuspecting males (Gaskett et al., 2008).
Concrete examples of these “extreme” adaptations in the shape of the floral area
reached by the pollinator frequently appear among some species of orchids. Charles
Darwin (1862) devoted an entire book to studying orchids. He described with his
well-known fascination and thoroughness his observations and interpretations of
pollination processes in British species. In a second edition (Darwin, 1877), he
incorporated more tropical material based on observations that were not his own
(Micheneau et al., 2009). Darwin’s aim with these trials was to add evidence of the
importance of cross-fertilization in natural selection and to use orchids as a model
since they show complex morphologies that generally avoid self-fertilization and
favor pollination (Fay & Chase, 2009). Darwin’s optics produced a change of vision
in the study of plants, especially flowers, in the Victorian society of the time. Darwin
managed to “reinvent” plants, especially orchids, before public opinion by giving
them a more vibrant tone with strategies and means to achieve them (Endersby,
2016). From the point of view of this book, Darwin added evidence to demonstrate
that the rule was not that plants were static inanimate agents but that with their strat-
egies, they could achieve incredible things with a will often assigned to animals
(Endersby, 2016).
There are several morphologies of orchids. Some are simple with a more com-
mon “flower” appearance, such as Eriaxis rigida or Stenorrhynchos speciosum (see
photos in Fay & Chase, 2009), and others with much more complex aspects, such as
Caladenia longicauda. However, the climax of complexity and precision is found in
species such as Ophrys insectifera or O. apifera, where the entire floral structure
simulates an insect. These orchids use a tactic that is not the norm among flowering
plants but is very common among orchids: deception (Proctor et al., 1996; Jersáková
et al., 2006). These orchids of the genus Ophrys attract pollinators by simulating
sexual substances produced by females (Gaskett et al., 2008). In effect, the males of
certain insects, such as wasps, are the sexes deceived by the orchid. They are
attracted and driven to copulate with the flower that mimics odor and even shapes
their female, ending up loaded with pollen after the unfruitful mating. However, we
have different levels of deception among orchids (see Phillips et al., 2014 for a
detailed analysis of criteria for sexual deception in orchids). For example, some
orchids mimic only the odor of the sex pheromones of receptive female insects to
attract males (e.g., spider orchids, genus Caladenia). Additionally, as seen before,
266 6 Focusing on Dynamics: When an Exception Becomes a Rule

some species mimic a shape similar to the body of the female insect (e.g., warty
hammer orchids, one is Drakaea livida, the aforementioned O. insectifera, and
O. apifera) (Alcock, 2000; Gaskett et al., 2008; Fay & Chase, 2009; Bohman et al.,
2014). Other species, along with scent, trapping mechanisms are added to ensure
that the male insect carries pollen attached to his body (e.g., red-banded greenhood
orchid Pterostylis sanguinea) (Peakall, 1990; Lehnebach et al., 2005; Gaskett et al.,
2008; Phillips et al., 2014). Each example acts on males of a species or at least on
particular genera of wasps (the first two examples) or dipterans (in the last one).
It is thought that the rule is that with this strategy, the plant biases mutualism to
increase its fitness, and the deceived pollinator male gains nothing but loses nothing
either (Schiestl, 2005). However, many exceptions are found where this deception
leads to fitness costs for both males and females of the pollinator (Gaskett et al.,
2008). These costs are linked to the loss of copulations with genuine females and
especially to the loss of costly ejaculate due to pseudocopulation (Coleman, 1929;
Blanco & Barboza, 2005), as occurs, for example, in Cryptostylis erecta and
Cryptostylis leptochila and the male pollinator orchid wasp (Lissopimpla excelsa),
where there is a high rate of ejaculation (Gaskett et al., 2008; Brunton-Martin et al.,
2020). Thus, in orchids pollinated by pseudocopula, species pollinated by essence-­
collecting insects, and other groups that show an intense relationship with their
pollinators, the rule is the attraction of the pollinator through olfactory chemical
signals (essences) (Proctor et al., 1996). As we saw, this chemical attraction can be
accompanied by morphological and functional changes.
Many species of orchids are pollinated by insects, which are rewarded with nec-
tar, but the exceptions to this typical pattern in plants are, as we have seen, very
numerous among orchids (Proctor et al., 1996). Thus, in this framework, we can ask
ourselves how these deception strategies arose. We know that they involved adjust-
ments over time that were not minor, reinforced by the success of the novelty in its
beginnings on the part of the plant. While more experienced males may tend to
avoid them and not want to “copulate” with these deceptive orchids (Peakall, 1990;
Alcock, 2000; Wong & Schiestl, 2002; Schiestl, 2005), what is certain is that it has
worked and continues to do so.
Thus, an important question arises: how can a plant reach such a degree of com-
plexity or weave such a strategy? How can the plant be able to generate a prison,
mimic an oviposition site, or even mimic the shape and signals of the female of its
pollinator to attract it to pseudocopulation and benefit from the transfer of pollen?
The functional question is obvious, the “what for.” However, it is difficult to under-
stand, even with advances in pollinator–plant interactions, especially insect–plant
interactions, how to reach such perfection in the design of deception. The tip of the
iceberg encloses hundreds of options that characterize the linkage between plants
and their pollinators. From the perspective of our book, the example mentioned
above leads us to see how something that was indeed a rarity at the beginning, per-
haps something subtle, gradual, from a natural selection approach, became in cer-
tain groups of plants the common, the norm.
Moreover, if we have not learned this modification’s value or adaptive function
to date, we could consider it a clear teratology. Having insect-like flowers would
6.2 E-R Changes by Nature’s Action 267

have no meaning per se for the plant. Thus, if we look closely, we see how the func-
tionally adaptive loses strength, and we can easily mislabel something.
For our analysis, it is interesting to note that from the intraspecific point of view,
these cases began as rarities and ceased to be so. They emerged as novelties, rarities
in the occurrence frequency, or the trait’s conspicuousness. They may have involved
an even subtle level of preadaptation in color, shape, or a type of “bouquet” (odor),
as noted by Vereecken et al. (2012) in their comprehensive comparative study in
orchids of the genus Ophrys. In that work, the authors even overturn the “Cope’s
rule of the unspecialized,” that very specialized groups cannot “reverse” in the evo-
lution toward more generalist forms; in this case, transitions in both directions
between generalists (shelter mimicry) and specialists (sexual deception).
The “duality according to the perspective of the analysis” is that, at the level of
the supraspecific group, these groups of plants are species, genera rare for the clade
to which they belong (i.e., the deception of these types is not a “rule” or pattern
widespread among plants). Moreover, many insects are also somewhat different
from their relatives. Thus, from the intraspecific view, these exceptional cases of
evolution are fantastic examples of the passage from rarity to a pattern (i.e., depend-
ing on the clarification, it may be rather supra-familial). They are still rarities since
they are restricted to a delimited group. Whether we call a phenomenon a rule or an
exception depends very much on the level of analysis we are carrying out.

6.2.3 A More Bidirectional E-R Dynamic in the Short Term:

Facultative Organisms

When we have mentioned examples of the passage from exception to rule, whether
we refer to a pattern (e.g., form, behavior, etc.), process (its causes and mecha-
nisms), or both, it does not imply that this is necessarily unidirectional. It is expected
that in many circumstances, this will have an apparent bidirectional character, i.e.,
that the passage from exception to rule may occur in reverse. It is not only evolu-
tionary time, as would be a regression or change in a trait that will not always be
equal to the ancestral one, but where the “spatial” context (i.e., environment, sur-
rounding environment, geography, territory) is the trigger for that change from E to
R or from R to E, even during the life of the organism.
Where then, can we easily see this relatively fluid dynamic in one direction or the
other? For this purpose, we can use so-called “facultative organisms.” This concept
refers to organisms (animals, plants, bacteria, etc.) that exhibit different behaviors
or traits in response to varying environmental conditions. In one spatial context
(x1), they may display specific characteristics, while in another spatial frame (x2),
they might exhibit entirely different traits. This modality of change means that what
is a rule, even implicit, in one setting is not so in another; therefore, this feature is
different in greater or lesser magnitude. This trait may be morphological, physiolog-
ical, behavioral, or a combination. It is worth remembering that “optional” is defined
268 6 Focusing on Dynamics: When an Exception Becomes a Rule

as something that can be done or not done; that can develop or function but is not
obligatory (The American Heritage® Dictionary of the English Language, 2003).
Concerning living things, that term is pointedly applied to an organism that mani-
fests its genotype under defined environmental or biological conditions, for exam-
ple, a greater or lesser degree of parasitism or the ability to reproduce sexually or
vegetatively (Burke & Bonduriansky, 2017). Many bacteria illustrate the above
(Table 6.2), as in some cases, they can survive both in the presence of oxygen and
in anaerobic systems or environments.
When we discussed the origin of life and how the evolution of the first organ-
isms that existed on earth occurred, we said that the rule in that first context was
to be anaerobic, and when some molecular oxygen arose in the atmosphere, it
came directly from the photolysis of water or other means. However, it was still

Table 6.2 Some examples of facultative organisms where the rule operates according to the
environmental context in which the species develops are highlighted
Facultative
Organism characteristic Context 1 Context 2 References
Escherichia Respiratory Anaerobic Aerobic Stanier &
coli metabolism Villanueva (1996)
Salmonella Respiratory Anaerobic Aerobic Stanier &
metabolism Villanueva (1996)
Vibrio Respiratory Anaerobic Aerobic Stanier &
cholerae metabolism Villanueva (1996);
Fernandez &
Alonso (2009)
Klebsiella sp. Metabolism Nitrogen fixation Aerobic Bagley (1985)
Hamiltonella Endosymbiosis Presence: Ausence Castaneda et al.
defensa with aphids Resistance to (2010)
natural enemies,
increased thermal
tolerance
Bombus sp. Mutualism Legitimate Nectar robbing Inouye & Ogilvie
Bumblebee (pollination) pollination (2001);
Lichtenberg et al.
(2018)
Hypericum Reproduction Apomixis Sexual Pank et al. (2003)
perforatum reproduction
St. John’s
wort
Salmo salar Life in fresh or Lives in the ocean Reproduction in McCormick et al.
Atlantic saltwater for most of its life freshwater (1998)
salmon
Anemonia Mutualism Solitaries Symbiosis with Calado et al.
sulcata decapods (2007)
Sea anemone
Aphids Reproduction Sexual reproduction Parthenogenesis in Simon et al.
in times of low times of high (2010)
resources resources
6.2 E-R Changes by Nature’s Action 269

too little to have a relevant role in microbial evolution. Indeed, in early evolution,
one could disregard oxygen and consider that it was the age of anaerobes (Martin
& Sousa, 2016). Then, as oxygen increased notably in the atmosphere, organisms
began to adapt to metabolize it. However, some maintained the ability to perform
different types of metabolism depending on the context of the presence or absence
of oxygen (Curtis et al., 2008). These bacteria are the so-called facultative anaer-
obes (or also facultative aerobes). They develop an aerobic respiratory metabo-
lism when they use oxygen in the environment or a fermentative metabolism in
the case of its absence (Stanier & Villanueva, 1996). Thus, facultatively anaerobic
bacteria can obtain energy through both types of metabolism, depending on envi-
ronmental conditions. One of the main groups of this type of bacteria is
Proteobacteria, which include some important pathogens, such as Escherichia
coli, Salmonella, Vibrio, and Helicobacter. There are also free-living bacteria
with facultative metabolism, such as those represented by nitrogen-fixing bacte-
ria. This mechanism allows them to adapt to the environment, and the passage
from exception to rule would occur in a bidirectional manner to meet the meta-
bolic needs of the organism (Unden et al., 1994; Unden et al., 1995; Murashko &
Lin-Chao, 2017).
From an ecological perspective, concerning bacteria, there are cases of organ-
isms that can live with different patterns according to the environment in which they
are found. Facultative endosymbionts constitute one case. These are common
among arthropods (Duron et al., 2008; Henry et al., 2015), and they can provide,
among other things, a defense against natural enemies, such as parasitoids or fungi
(Burke et al., 2009). The functions of these symbionts can range from an obligate
nutritional role to an optional role in protecting their hosts against environmental
stress. For example, almost all aphids are infected with the obligate nutritional sym-
biont Buchnera aphidicola, which they generally need for survival (Shigenobu
et al., 2000). However, many aphids also possess additional symbionts that are fac-
ultative from the host’s perspective (Moran et al., 2005). This means that although
they are not necessary for the aphid to survive, they give it an advantage in defend-
ing itself. These bacteria can be transmitted from mother to offspring. There may
even be several types of bacteria in a host associated with the aphid’s host plant,
geographical area, and climatic characteristics, which influence the evolutionary
biology of aphids (Barrenchea-Mellado et al., 2015).
Other species exhibit a form of facultative mutualism, i.e., they benefit from a
symbiotic relationship with another species but can live without it. Myrmecophilous
plants, such as some species of Passiflora, whose living tissues are occupied by
ants, are an example of this type of mutualism (Apple & Feener, 2001). Facultative
myrmecophiles have a more significant number of ant species associated with them
than obligates, as they do not require ants for survival but would be expected to
associate opportunistically with numerous species (Glasier et al., 2018). The oppor-
tunistic nature of these associations implies that there must be chance encounters of
symbionts interacting with a host (Rodrigues et al., 2010). The ability of hosts to
interact with more ant species would increase the likelihood of symbiosis and thus
benefit facultative myrmecophiles (Glasier et al., 2018).
270 6 Focusing on Dynamics: When an Exception Becomes a Rule

Similarly, facultative mutualism is observed in some insects and birds pollinating

certain plants, depending on the environment (Ollerton, 2006). Sometimes, as a
flexible rule, facultative mutualists may behave cooperatively or in a host-­
exploitative manner. This is the case, for example, in individuals of the yucca moth,
which sometimes skip behaviors used to pollinate flowers (Tyre & Addicott, 1993).
These behaviors exist in numerous pollinators, which may use flower-pollinating
tactics to consume nectar or make holes in their base instead of “legitimately” visit-
ing flowers (Inouye, 1980). Nectar “stealing” is widespread, exhibited by insects,
birds, and mammals, and is seen in most flowers with a tubular corolla or nectar
spur (Irwin et al., 2010). Whether an individual visits a flower legitimately or steals
depends on the costs needed to access nectar with each tactic and the amount of
nectar it can extract. The most efficient flower management tactic under a set of
ecological conditions would be the prevailing tactic or, in this framework, the pre-
vailing rule (Lichtenberg et al., 2018).
Another example of a facultative organism is epiphytic plants, which live perched
on other plants but do not have metabolic contact with them (Benzing, 1990).
However, they establish interactions and intervene in the nutrient cycle of the host,
in addition to being necessary for the functioning of the ecosystem (Ceja et al.,
2008). Some epiphytes are also facultative and can indistinctly inhabit both the
canopy and the ground (Sartí, 2012). This means that they can use different strate-
gies according to their needs in the environment they are in. These include hemi-
parasitic plants. These plants generally live attached to the xylem of a host plant and
can be facultative or obligate, depending on their degree of dependence. Obligate
parasites depend on the host throughout their life, while facultative parasites may
live part of their life independently (Westwood et al., 2010).
Facultative hemiparasites can complete their life cycle without host plants
because they are photosynthetic, but when they encounter the root of a host, they
form connections called haustorial. Thus, they extract water and minerals directly
(Press et al., 1990). Some examples are found within the families of Scrophulariaceae,
Santalaceae, Oleaceae, etc. Even in some species, seedlings can be independent of
the host for up to one year, as in Atkinsonia or Rhinanthus (Sosa & Tressens, 2002).
Therefore, in all these cases and others, we cannot speak of exceptions to the rule
but rather that the rule is very flexible in an optional context. As we have seen,
sometimes the obligate was initially the rule, as in the example of anaerobic organ-
isms. In the same way, evolution can be observed in parasitic organisms that come
from free-living organisms. The potential transition in this evolution can be seen in
facultative parasites, which, according to environmental conditions, can behave in
one way or another (Luong & Mathot, 2019). Facultative parasites can complete the
life cycle without a host but exploit them under certain conditions. For example, in
facultative parasitic nematodes, parasitic juveniles form under stressful conditions
(high density, low food availability, high temperature), but under favorable condi-
tions, they can complete their life cycle without a host (Viney, 1996; Stasiuk et al.,
2012). In mites, for example, the reproductive state of the host, its availability, and
the parasite’s state are necessary conditions that dictate whether organisms will
behave parasitically or not (Luong et al., 2017). These context conditions, in all
cases, make it the rule to be free-living, as was the pattern in the beginning, or to
parasitize a host when this way of life represents an advantage to them.
6.3 E-R Changes Due to Human Activity on Nature 271

At the reproductive level, there are also cases of some organisms that follow
specific guidelines according to the best strategy. That is to say. They cannot be
pigeonholed as “always” following this principle or pattern in reproduction mode.
In botany, for example, there is facultative apomixis, through which individuals can
reproduce asexually, but without leaving aside sexual reproduction, in a balanced
system. Facultative apomixis is widespread in the Rosaceae family (Richards,
1997). For animals, facultative parthenogenesis is common, and we have already
discussed that it appears, among other groups, in many insects, such as bees, ants,
or aphids. In the latter, reproduction by parthenogenesis occurs when the environ-
ment presents favorable conditions and abundant food. Otherwise, they produce
males and females who reproduce sexually (Lanteri et al., 2010).
The “facultative” component may be discovered late in many organisms and may
even have been considered a mere rarity initially. This could occur due to the bias of
studying only a restricted space or group of species in a clade. Cases of these late
discoveries are other groups to those already mentioned where cases of partheno-
genesis are also still found, which were previously totally unknown or taken as mere
exceptions. For example, in the reproduction of the spiny leaf stick insect Extatosoma
tiaratum, it was observed that females could reproduce asexually when sexual
reproduction represented high costs (Burke et al., 2015). Another example is the
case of eastern copperhead snakes (Agkistrodon contortrix) and their venomous cot-
tonmouth cousins (A. piscivorus), which until relatively recently were thought to
reproduce asexually only under captive conditions. However, it was discovered that
some litters of wild snakes had also been born by parthenogenesis and that females
could reproduce in this way when males were absent, when the population was low,
or when migrating to new habitats (Booth et al., 2012). A couple of years ago, the
case of asexual reproduction was observed for the first time in an endangered saw-
fish species (Pristis pectinata), documenting the birth of seven asexually conceived
offspring. This behavior, as in those snakes, has been observed only in captive indi-
viduals (Fields et al., 2015). Therefore, all these “late” discoveries indicate that
there could be many more cases of groups of animals and plants that follow more
than one strategy. It would make them facultative organisms in that part of their
biology. In conclusion, this bias mentioned above may mean that some of these
cases remain outside our knowledge, but far from being exceptions, they may be
evidence of the existence of patterns that differentially show themselves according
to needs throughout the life cycle.

6.3 E-R Changes Due to Human Activity on Nature

6.3.1 Exotic Groups that Become Local Pests

6.3.1.1 Introduced Animals

Most biological introductions, which may later become invasions, appear as a direct
result of human activity (Sakai et al., 2001). Plants and animals have long been
mobilized to different places around the globe, and invasive species have caused a
272 6 Focusing on Dynamics: When an Exception Becomes a Rule

great deal of change worldwide, often harming native communities (Simberloff,

2001). In the framework of this book, we could say that native species, in any place,
would represent the rule, the common, and adapted group to their environment.
Moreover, when a new and exotic species is introduced, it would represent an excep-
tion. The problem arises when exotic species present a great competitive ability and
capacity to spread. With these characteristics, it can become an invasive species,
with the capacity to exclude and displace native species, even leading to extinction
(Gurevitch & Padilla, 2004; Bøhn et al., 2008). Here, we would have a change in the
pattern, where now the alien species could become the ruler.
Biological invasions have become a significant threat to biodiversity, with main
mechanisms such as competition and niche substitution, which can make invaders
dominant in their new ecosystem (Cheng et al., 2009). The introduction of species
into new ecosystems was generally intentional and human-facilitated. Many times,
species in captivity manage to escape, and they can become established in the new
environment, competing with native species. One of the main motives for intention-
ally introducing species is economic gain. There are numerous examples of species
introduced for agricultural or livestock purposes. Indeed, the most numerous and
abundant introduced species are agricultural plants and animals. Cattle, sheep,
goats, horses, and chickens are examples of introduced animals in many regions.
The domestic bee (Apis mellifera) is another example of a highly adaptable species
that can naturalize in a wide variety of environments. On the other hand, other spe-
cies have been introduced for recreational purposes, such as hunting and fishing,
such as boards, salmon, and trout.
One crazy example is the introduction of hippopotamuses to the shores of the
Magdalena River in Colombia (Buriticá, 2014). This story relates to drug traffick-
ing, as the infamous Colombian drug trafficker Pablo Escobar was obsessed with
exotic animals and set up a private zoo in one of his mansions. He brought in a
couple of young hippopotamuses, among many other rare wild animals (he loved
birds). After his death, his entire empire collapsed, and many animals were released
into the wild. It is how a megaherbivore and important ecosystem engineer was
introduced into a place far from its original environment. Hippos have a relatively
high reproduction rate and no major predator or disease in the area. These charac-
teristics will lead to a significant increase in individuals by 2050, with a projected
population of 1,500 hippos. It is currently the largest herd outside Africa. Thus,
hippos are not only invasive species that compete for resources, alter ecosystem
processes, and shape the landscape but also, due to their high aggressiveness, endan-
ger human settlements that share their new area of distribution (Monsalve, 2014).
The Colombian government is currently implementing strategies to limit the growth
and expansion of the hippo population to mitigate future social and ecological
implications.
In South America, particularly in southern Chile and Argentina, the wild boar
(Sus scrofa) is considered one of the most noxious invasive ungulates (Jaksic et al.,
2002; Novillo & Ojeda, 2008; Ballari et al., 2015). Wild boars are native to Eurasia
and North Africa and have invaded almost the entire world (Wehr, 2021). It is a suc-
cessful invader because it has a high reproductive rate and remarkable plasticity of
6.3 E-R Changes Due to Human Activity on Nature 273

adaptation to a wide range of habitats, climates, and food (Coblentz & Baber, 1987;
Podgórski et al., 2013; Ballari & Barrios-García, 2014). As an invasive species, it
damages animal and plant communities and modifies ecosystem processes and hab-
itats. For example, it favors the dispersal of invasive plant species, which generates
a double disturbance in the invaded local ecosystem (Ballari et al., 2015). The wild
boar was introduced into Argentina from Europe early in the last century for sport
hunting. As often happens with this practice, some individuals escaped from con-
finement and spread throughout the territory (Navas, 1987). It is currently exploited
as an economic and cultural resource in several provinces, but this makes it a sus-
tainable activity far from controlling and eradicating this invasive species (Ballari
et al., 2015).
Australia is the perfect case of an isolated geographical area in the world that has
suffered the introduction of exotic animals in large numbers that displaced many
unique local representatives. There are many examples of cases ranging from insects
to mammals and plants, some of them for more than 100 years. Perhaps the worst of
the invasive species in Australia and many parts of the world is the European rabbit
(Oryctolagus cuniculus), which, both for its ability to proliferate and its adverse
effects, is included in the 100 lists of the world’s most harmful invasive alien species
(Lowe et al., 2000). It was introduced as a game but adapted very well to the new
conditions and without the danger of natural predators. The rabbit accelerated the
process of erosion and desertification in Australia by consuming natural vegetation.
In addition, this lack of food affected many native animals and livestock. In addi-
tion, introducing a natural enemy, the red fox, was a disaster, as it preferred to attack
birds or marsupials. A solution for this invasive species was the introduction of
some viruses, such as myxomatosis and later hemorrhagic disease, which managed
to stabilize populations (Coman, 2010).
An important aspect to highlight in this scenario is the rapid expansion of some
of the introduced species. Hybridization processes have favored it with locals in
some cases, as well as a great capacity to adapt to new environments. We have as
examples the “invasive cane toads” or cane toads (Rhinella marina) (satirized in the
comic strip The Simpsons) and the invasion of fruit flies in eastern Australia
(Canestrelli et al., 2016). The cane toad was introduced to Queensland from Hawaii
in 1935 and spread rapidly across Australia. After that, the cane toad has become a
plague and a threat to native species because of its ability to reproduce and its venom
(Tyler, 1994). In addition, during expansion, toad populations underwent significant
morphological changes that promoted the dispersal of the invasion front, such as
longer legs, as well as behavioral changes, such as straighter dispersal trajectories.
On the other hand, invasion front toads could reduce parasite load and positively
regulate enzymes involved in energy metabolism and response to oxidative stress
(Brown et al., 2015; Hudson et al., 2015). All this allowed this exotic species to
become highly invasive and to spread rapidly, competing with native species.
The other example mentioned above is the fruit fly (D. melanogaster), intro-
duced in northern Australia approximately 100 years ago. Researchers observed
that this species underwent several morphological changes during its dispersal.
These changes included alterations in wing size and shape, as well as modifications
274 6 Focusing on Dynamics: When an Exception Becomes a Rule

in life history traits, stress tolerance, and metabolic enzymes (Frentiu & Chenoweth,
2010; Ray et al., 2016). All these changes allowed rapid adaptation to new environ-
mental conditions and enhanced dispersal and reproduction.
In the framework of this book, we could state that these species, due to their
particular characteristics, whether accidentally or voluntarily introduced to new
environments, have become the rule, competing with and even displacing native
species in Australia, as is the case in many other places. Many of the competing
native species still persist but have changed the rate of appearance. They are now
becoming the exceptions or the rare species that these new invaders displaced.

6.3.1.2 Introduced Plants

As with animals, invasive plants can compete with native vegetation and displace or
drive native species to extinction. In addition, one effect of invasive plants that
become established in a new ecosystem is that they can significantly affect soils and
their fertility, water availability, erosion, etc. (Giorgis et al., 2006). All these modi-
fications caused by invasive plants can affect the ecosystem’s biodiversity and have
negative economic consequences (Pimentel et al., 2005). A typical example is
Mimosa pigra, native to neotropical regions but which can become a significant
invader. This species was introduced into Australia more than 100 years ago and has
spread remarkably throughout northern Australia. Although it allows some endan-
gered species to find refuge in its canopy, it is generally harmful to Australian wild-
life, as their diet is still based on native plants, which are displaced by the rapid
growth of the Mimosa (Miller & Lonsdale, 1987; Lonsdale et al., 1995). The same
is true of the fig cactus belonging to the Opuntia genus (Opuntia ficus-indica) that
is native to Mexico but has spread to the United States and Argentina. From the
United States, it reached Australia to be used in gardening and then naturalized and
spread, adapting to the climate. It was also introduced in Europe and from there to
North Africa. If the conditions are right, this plant quickly spreads because it can
reproduce asexually by fragmentation and grow extremely fast, making it easy to
become a pest (Cañas, 2017).
The success of introduced species has many hypotheses that postulate the need
for unique ecological characteristics to explain their dispersal. However, recent evi-
dence suggests that native and introduced species have similar successional trajec-
tories (Meiners, 2007), as do other characteristics, such as defenses (Lind & Parker,
2010), enemy release (Schultheis et al., 2015), and grouping mechanisms (Lemoine
et al., 2016). This suggests that introduced and native species thrive for very similar
reasons. Interestingly, the latter authors state: “we show that native and introduced
species appear to follow the same ‘rules’ for becoming abundant.” In other words,
introduced species are not so different from their native counterparts, at least regard-
ing ecological behavior. An invasive species is more successful than a native species
in competing with it and displacing it to become the new ruler of the ecosystem.
6.3 E-R Changes Due to Human Activity on Nature 275

This may be due to particular characteristics, such as rapid growth or dispersal

inherent to the plant, and not to the geographical origin or the ecosystem’s
characteristics.

Other Witness Cases in Different Regions of the World

In addition to the cases mentioned above, invasive species exist in all regions of the
globe, and in the same way, they can be distributed and become pests. The important
thing about these ecological explosions is that they can sometimes have severe
effects, even affecting human life. An example mentioned in the valuable and inter-
esting book “The Ecology of Invasions by Animals and Plants” (Elton, 2020) is that
of the Anopheles gambiae mosquito, the carrier of malaria. In 1929, some mosqui-
toes accidentally arrived in northeastern Brazil and were probably transported from
Dakar, Senegal. Although not much attention was initially paid to them, the insects
spread silently along the coastal region. It caused one of the worst malaria epidem-
ics in Brazil due to its rapid reproduction in open ponds. Fortunately, control of the
species was possible, and Anopheles gambiae was exterminated from the South
American continent.
The same is true for many other species in different parts of the world, intro-
duced as a source of food, the fur industry, the timber industry, and other economic
or recreational purposes such as hunting and fishing. The increase in the speed of
transportation in recent years has maintained and intensified this bombardment of
foreign species in all countries, brought accidentally or intentionally from places
that used to be isolated. Although not all plants and animals carried worldwide suc-
ceed in becoming established, they can somehow change the balance of native spe-
cies. This process is gradually changing the distribution of species around the globe.
In this list, we can cite the case of the Burmese python (Python bivittatus), a snake
species native to India, Pakistan, and Indochina (Uetz et al., 2019), introduced in
Florida, United States to be marketed as a pet. Subsequently, many of these snakes
were released into the Everglades, generating a problem by impacting the ecosys-
tem through heavy predation on mammals, including some endangered species,
resulting in a considerable decline in previously common species (Reichert et al.,
2017; Sovie et al., 2016). Another species threatening the local species in the United
States is the tiger salamander Ambystoma tigrinum, which was introduced for use in
fisheries as bait and then dispersed, competing with the locally endemic Californian
species A. californiense (Naylor et al., 2001; Riley et al., 2003). Exotic species were
also introduced to the rest of the world for use in various industries, such as red
foxes from Europe to the United States and Australia for the fur industry and recre-
ational hunting. The European red fox is probably responsible for the decline of
some small canids and ground-nesting birds in North America and numerous small
and medium-sized rodents and marsupials in Australia (Global Invasive Species
Database, 2021 (http://www.issg.org/database).
276 6 Focusing on Dynamics: When an Exception Becomes a Rule

Witness Cases from the South of the World

Most of the invasive species in South America come from Europe. This is com-
monly observed, for example, in places such as Argentina related to the arrival of
European immigrants in the late nineteenth and early twentieth centuries (Speziale
et al., 2012). In general, exotic species in Argentina were introduced for ornamental
reasons (Rejmánek & Richardson, 2013) but are also related to the timber industry,
forestry functions, and erosion control (Giorgis & Tecco, 2014). Each region has
some characteristic exotic species. The occurrence of exotic species greatly depends
on the proximity to urban centers and human presence (Viano, 2014). There are
many cases cited for Argentina, and although most of them were introduced for
commercial purposes, their dispersal and reproduction characteristics, among oth-
ers, made them established in the country.

An Edible Fruit Whose Thorny Plant Displaces Not Only Plants: The Case
of the Blackberry
The blackberry (Rubus ulmifolius) is an exotic species in the province of Córdoba,
Argentina belonging to the family Rosaceae. Due to its rapid growth and the fact
that it reproduces successfully through its seeds and stems (Giorgis et al., 2006), it
has been a severe problem in the province for several years. Although it is very com-
monly used for the construction of fences or the consumption of its fruits, it forms
thorny thickets, causing the landscape and habitat structure to change drastically
(Comparatore & Mazzolari, 2009). Despite the invasiveness of this species, its abil-
ity to rapidly produce fruit and the possibility of asexual reproduction have made it
valuable for consumption and exploitation. Its fruit is used for gastronomy and is
part of the group of red fruits. However, it also has interesting properties due to its
high content of tannins, sugars, and other organic compounds. Therefore, in addi-
tion to being used for food preparations, it also has medicinal purposes (Ortiz,
2007). Despite this, wild varieties of the species have spread rapidly in some regions
of the country. Therefore, measures have had to be taken to eradicate it through the
interdisciplinary work of biologists, agronomists, and foresters to reverse the dete-
rioration of the natural environment caused by this plant (Comparatore & Mazzolari,
2009) (Fig. 6.2a, b).

A Colorful Tree for the Landscape However, Harmful to Native Species:

The Crataegus (Pyracantha angustifolia)
It is a shrub native to Africa, with long thorns and white flowers, whose fruits enable
the species’ rapid dispersal and invasion. These are fleshy fruits eaten by birds,
which then disperse their seeds. Crataegus was introduced to different regions of
Argentina for its ornamental value. Because of its rapid growth and reproduction, it
is one of the main invasive species in many ecosystems today (Giorgis et al., 2006).
Its dense foliage generates much shade, an attraction for ungulates such as goats,
horses, or sheep, which also disperse its seeds. Crataegus also helps the growth of
6.3 E-R Changes Due to Human Activity on Nature 277

Fig. 6.2 Invasive blackberry

in mountain environments of a
Argentina. The blackberry
(Rubus ulmifolius) invades
various mountainous regions,
including high altitudes such
as Los Gigantes, Córdoba,
Argentina. It competes with
high-­altitude grasslands at
1800 m and progressively
fills the canyons and
temporary watercourses
inhabited by native species,
displacing them.
Credit: Gabriel
Laufer; Javier martin
(a) Rubus ulmifolius.
License: Public domain.
https://www.inaturalist.org/ b
observations/61610193.
(b) Rubus ulmifolius fruit.
License: Public domain,
via Wikimedia Commons.
https://commons.wikimedia.
org/wiki/File:Rubus_ulmifo-
lius_Fruits_23August2009_
SierraMadrona.jpg

another invasive exotic species, the broad-leaf privet (Ligustrum lucidum), which
grows more densely under its foliage and replaces native trees (Giorgis et al., 2006;
Viano, 2008). Other species that also represent major invasions in Córdoba are
sweet briar and dog rose (Rosa rubiginosa and R. canina), cotoneaster (Cotoneaster
franchetii), pine (Pinus sp.), thistle (Carduus sp.), etc. All of these factors are
already established, which makes their eradication much more costly.

Some Examples of Exotic Animals

Among the invasive animals, we already cited the case of the wild board. However,
one of the most important invasive species that can be cited for Argentina is the
European hare (Lepus europaeus), which can inhabit different environments, colo-
nizing quickly due to its high number of offspring in each gestation. Trout and
salmon have also been introduced, especially for recreational sport fishing activi-
ties, and have affected several native species in Patagonia by competing for the
same resources (Giorgis et al., 2006). The abundance and quantity of exotic species
278 6 Focusing on Dynamics: When an Exception Becomes a Rule

are constantly increasing. Those introduced as “rare” species can slowly take the
place of native species if the necessary measures are not taken, knowing each par-
ticular species in each region where they have become established.
In conclusion, this pool of examples and witness cases mentioned from various
parts of the planet, as well as hundreds of others that exist of the exact nature (which
would require a book for that purpose), serve to illustrate how the concept of excep-
tion was initially present for the introduced species. Moreover, from a frequency of
occurrence perspective, it gradually or drastically became the most abundant, the
new rule for the region in question. In contrast, native species may become rare spe-
cies, representing new exceptions, which, unfortunately, in many cases, represent
the “previous step” to their extinction.

6.3.2 A Look at the Disease Cycle and the Role of Man

6.3.2.1 General Epidemiological Context

As a rule, humans have been dealing with diseases since the beginning. Diseases
have a relatively basic development cycle within the host body. However, they can
also have a cycle more related to the general population with sudden and abrupt
changes in onset and incidence. At the end of this chapter, it will be apparent that
both diseases and more global processes such as pandemics start as an exception
that, with time, and helped mainly by the constant changes in human habits and
relationships, can become the rule in a specific time and space.
We must first turn to epidemiology to rescue some concepts that will help better
understand these cycles and patterns shown by diseases (Bonita et al., 2006;
Rothman, 2012; Gordis, 2013). For an infectious disease to occur, three components
should interact: the infectious agent or pathogen, the host, and the environment that
makes these two components coincide. On the other hand, noninfectious diseases
are multifactorial, so this simple model can be made more complex (Rothman,
1976). Infectious diseases have a cycle called natural history. It shows the develop-
ment of the disease at the individual level, over time and without treatment. As a
rule, the cycle begins with a susceptible host exposed to an infectious agent or con-
ditions that initiate the process in the case of noninfectious diseases such as cancer.
After exposure, there is an asymptomatic incubation or latency period of the dis-
ease, which can vary widely depending on the agent. At this stage, some pathologi-
cal changes may be detected in the patient. When symptoms appear, the clinical
stage of the disease is reached. Finally, the disease ends, and the host may recover,
but the disease may also leave sequelae or disability, or in the worst case, death. In
addition, disease cycles can be analyzed from a macrohealth point of view and not
so much from an individual point of view as described above. As a rule, diseases
have levels of presence in the community. The base level is the endemic level, which
may be zero or not, and the incidence of the disease may be rare or very common
but within a range considered normal. Thus, there are diseases whose base level is
6.3 E-R Changes Due to Human Activity on Nature 279

rare, and a single case sets off health alarms (e.g., rabies, poliomyelitis). In other
cases where diseases are common, people wait for an abrupt change in the norm
before becoming alarmed (e.g., influenza).
On this basis, we have different denominations according to the behavior and
rarity of the disease. Sporadic diseases are rare and irregular. Endemic diseases are
common in the population in a geographical area. When the incidence level of a
disease suddenly increases above the expected baseline level, it is called an epi-
demic. When the epidemic spreads to other geographical areas, such as countries or
continents, and affects many people generating community circulation, we are deal-
ing with a pandemic. The emergence of an epidemic may be related to changes in
exceptions to rules. For example, an agent may increase its virulence, which is the
proportion of severe or fatal cases. Additionally, the agent may be rare or absent in
one place and may be introduced. It can change the mode of transmission by making
it more infective. It can also change the susceptibility of the host to be more likely
to respond to the agent. However, these cycles also end naturally due to a compro-
mise between host resistance and parasite virulence, artificially due to technological
developments or a better understanding of the causes of infection or the develop-
ment of sanitary measures.
It should be noted that the progressive eradication of the pathogen (or its decrease
and/or disappearance due to seasonality) generates the reverse step, i.e., that a dis-
ease that is a rule becomes an exception. Thus, developing a vaccine for an agent
that has become more virulent may cause the disease to become rarer, chronic, or
disappear. Although terms such as epidemic were intended for infectious agents,
they are now applied to noninfectious diseases such as obesity and diabetes (Centers
for Disease Control and Prevention, 2004; Mitchell et al., 2011). McNeill (1998)
strongly emphasizes that the human being can be seen as a disease and, to some
degree, an epidemic for other organisms, which may engage in less virulent forms
of behavior but constantly generate a disturbance to the system. This view was
brought to the cinema by the 1999 film The Matrix. Thus, the human being was an
exception when it was in harmony with the environment and became, as a rule, the
predominant organism on the planet, becoming a “macroparasite” (McNeill, 1998).
Diseases are also seen as a means of population control since, for example, in
Africa, many parasites and microorganisms do not trigger the formation of immune
reactions. As density increases, infection increases, and the system escalates into an
epidemic that returns to equilibrium once people die or are unable to generate
resources due to levels of disability (McNeill, 1998).

6.3.2.2 Historical Review and Some Emblematic Cases

Historically, disease cycles followed humanity as civilization progressed. Human

actions such as trade routes, social groupings, dietary modifications, improved
health practices, and armed conflicts influence the appearance and disappearance of
diseases (Bollet & Jay, 2004). In the beginning, the rule was that humans were scat-
tered in small groups of hunter-gatherers separated from each other. Epidemics and
280 6 Focusing on Dynamics: When an Exception Becomes a Rule

significant pandemics (human plagues) were rare, if not nonexistent, since the para-
site or infectious agent could not easily find a host to perpetuate the ailment (Kenny,
2021). Paleontological analyses suggest that humans who reached adulthood had an
average level of health (Bollet & Jay, 2004). Additionally, parasites are at risk of
eventually killing their host before being transmitted (McNeill, 1998), which is evo-
lutionarily not suitable for the pathogen and is generally an exception in an efficient
parasite (McNeill, 1998; Méthot, 2012). However, this is not to say that humans did
not get sick. Indeed, many diseases affected primates, from which we evolved but
also common diseases that we know, such as herpes, hepatitis, or yellow fever, and
bacterial diseases linked to hunting and consumption of wild animals, such as
anthrax and brucellosis (Aberth, 2011).
Moreover, in these times, human diseases were the rule in tropical areas because
that is where the ancestors of human beings came from. We can give as an example
sleeping sickness produced by a unicellular organism (Trypanosoma brucei). This
parasite is found as a rule in antelopes and is transmitted by tsetse flies. It is harm-
less to the antelope and the fly but not to the human host. It generates extreme weak-
ness and can be lethal. It is a case where the parasite is, as a rule, in equilibrium with
the vector and the wild animal host but, as an exception, generates severe disease in
humans, perhaps because it has not yet had time to reach a mutualistic equilibrium
with them (McNeill, 1998). However, as humans spread throughout the world, they
left these tropical latitudes to reach more temperate or colder zones and brought
many diseases. They also escaped from others that afflicted their predecessors
(McNeill, 1998; Kenny, 2021). The ability to create shelters, use clothing, and cook
food contributed to avoiding many diseases, resulting in improved health, increased
vigor, and population growth (Birdsell, 1957, 1958; McNeill, 1998). Cultural evolu-
tion generated a significant change in the environment and nature, and the relation-
ship with diseases also changed considerably (McNeill, 1998; Pagani-Balletti, 2020).
During the first great human revolution, the agricultural revolution, humans went
from hunter-gatherers to more stable groups where agriculture was practiced. This
change drastically favored the spread of diseases that, until then, were considered
rare in humans or absent. It favored the emergence of “crowd diseases” (Bollet &
Jay, 2004). It was also a period of domestication of wild animals, which favored the
appearance of common diseases in animals that were rare in humans (zoonoses). It
is possible to identify common diseases that are associated with illnesses observed
in domestic animals. For example, mumps is related to rinderpest, canine distemper,
smallpox to cowpox, and of course, influenza is shared by humans, pigs, and poultry
(McNeill, 1998). Examples of diseases common in wild animals and, therefore, rare
at first in humans are bubonic plague (burrowing rodents), yellow fever (monkeys),
and rabies (bats). Furthermore, as humans continue to invade wild places or come
into contact with wild creatures, the occurrence of such diseases becomes more
common. For instance, the hypothesis of exotic species displayed in Asian markets
has been linked to the appearance of diseases such as COVID-19.
Thus, settlement in cities, population increase, interaction with other individuals
(people and animals), increased waste and pollution, and trade routes were the trig-
gers that favored the appearance of significant plagues and epidemics (Aberth,
6.3 E-R Changes Due to Human Activity on Nature 281

2011; Pagani-Balletti, 2020; Kenny, 2021). Ancient texts, from Mesopotamia and
Far Eastern texts to Egyptian papyri and the Bible, speak of many diseases. However,
the descriptions are not detailed enough, and plagues are often attributed to superior
forces (Aberth, 2011). Trade and conquest routes, together with armed conflicts, led
to the appearance of great pandemics that wiped out a large part of the world’s
population (McNeill, 1998; Pagani-Balletti, 2020). Thus, places where diseases
developed a normal cycle of epidemics or local circulation were connected and
allowed diseases to affect a wider geographical range, similar to what has happened
recently with the COVID-19 pandemic. Examples include the Justinian plague
(camel route), the bubonic plague that was brought from the East, or the plague of
Amwâs and probably the plague of Athens, which are related to armed conflicts
since fighting troops were the first to be infected (Dols, 1974; Conrad, 1998).

Some Witness Cases

The Black Plague

Brought from southern Russia, the disease is spread by rats. These rats are infested
with fleas, which in turn are infected with a bacterium (Yersinia pestis). Once the
rats die, the fleas parasitize other animals and humans, thus spreading the disease
(McNeill, 1998; Pagani-Balletti, 2020). It can also be transmitted from human to
human when it causes pneumonia, but this way of spreading the disease is rarer
(Bollet & Jay, 2004). Geographically, travel and trade routes spread the disease
throughout much of the known world at that time (McNeill, 1998; Bollet & Jay,
2004; Aberth, 2011). The term bubonic comes from the buboes or swollen lymph
nodes it produces, and the term black derives from the gangrenous patches that
severely ill people show in some regions of their body (Bollet & Jay, 2004).
Many of the epidemics of antiquity are attributed to the bubonic plague. However,
many accounts are vague, and historians often do not agree with epidemiologists in
identifying diseases, such as the plague of Athens (typhus) (Pagani-Balletti, 2020)
and the Antonine plague in Rome (smallpox, typhus). The Justinian plague is very
likely to have been bubonic plague. The Black Death was the most famous plague
epidemic in history (fourteenth century). Here is a good model explaining how
human activities (such as travel and trade) spread a disease. It is thought to originate
from the hunting of marmots, which is believed to be the natural reservoir for
infected fleas. The fur trade extended from Crimea to the Mediterranean. Many sick
or dead animals were easily captured, and their skin was contaminated with hungry
fleas. In addition, the Crimean port was used by Genoese and Venetian merchants
who allied with rival Mongol tribes. One of these tribes attacked the Genoese and
allies and forced them to retreat to Kaffa. Here, history documents one of the first
examples of biological warfare, as the Mongols catapulted bodies of Black Death
victims over the city walls. Although the bodies themselves could not contaminate
people directly, it is believed that the rats in the city, along with the infected fleas
that infested the bodies, played a significant role in spreading the disease. This led
282 6 Focusing on Dynamics: When an Exception Becomes a Rule

to the downfall of the city besieged by the Mongols. Thus, the survivors returned to
their origin cities, and on the way, they spread the plague throughout the
Mediterranean, helped in turn by the rats they carried as stowaways on their ships.
Then, the maritime routes between infected cities caused the plague to spread
throughout most of the known world. Often, the ships arrived at ports with many of
the crew dead. An example of a practice introduced at that time that became the rule,
especially in ports, is the establishment of quarantine. Beyond religious beliefs, it
was said that in 40 days, a disease had time to appear and manifest itself. Quarantine
centers were thus created. One of the best options was quarantines inside the ship
since, on land, people complied with the quarantine, but rats and fleas did not.
Therefore, we can see how something restricted, endemic to Crimea (exception),
which would have killed comparatively a handful of people, was transformed into a
killing machine, unstoppable (The rule in medieval Europe). This was due to the
convergence of various specific conditions, such as hunting and selling wild animal
skins, the proliferation of rats in cities and ships, and trade routes that favored the
spread and proliferation of the disease. It is estimated that the Black Death wiped
out approximately 1/3 of the population of Europe and the Middle East. Because
almost 7 out of 10 infected individuals died, many agricultural areas were deserted.
The lack of labor generated famines and malnutrition that opened the door to other
diseases, such as smallpox and typhus. Then, several epidemics of the Black Death
occurred in Europe. It became endemic in England from the fourteenth to seven-
teenth century. At this time, there was a change in the social paradigm, and hygienic
norms were established in the population, leading in the next century to the con-
struction of sewers and drains to avoid massive contagions (Pagani-Balletti, 2020).
It is also thought that the pathogen in question, Yersinia pestis, has become less
virulent, the hosts have become more resistant and there is a possibility that infec-
tion with another related strain, Y. pseudotuberculosis, could generate cross-­
resistance with Y. pestis. This is in line with the previously mentioned idea that
pathogens evolve to be less virulent and can coexist with the host without killing it
(Smith, 1934). The dynamics between the host and parasite are complex. Although
a rat extermination program would favor a decrease in the frequency of the disease,
in the short term, the incidence would increase. Hungry fleas desperately seek
another host, and humans would be one of the safest options. Historically, during
many of the bubonic plague epidemics, when large numbers of dead rats were
found, it was a harbinger of an increase, an outbreak in human cases of the Black
Death. However, many suggest that the extraordinary appearance of rats in European
cities was due to the great slaughter of cats related to witchcraft and the devil (Pigna,
2020). There are currently some outbreaks of bubonic plague, suggesting that it can
be maintained in natural reservoirs until it infects people and is reintroduced to new
areas (Keeling & Gilligan, 2000; Stenseth et al., 2008; Gascuel et al., 2013).
As we saw, trade routes were vehicles for large-scale pests capable of wiping out
entire people. We have a clear example of the colonization of the American territory
and how many groups were decimated by rare or absent diseases in those popula-
tions. On the other hand, for European conquerors, these diseases were common,
and their bodies already produced the immunity that Native Americans lacked
6.3 E-R Changes Due to Human Activity on Nature 283

(Pagani-Balletti, 2020). It is another case of biological warfare that some of the

most renowned conquerors used. Examples of this are the great Aztec and Inca civi-
lizations that perished mainly with the introduction of smallpox (McNeill, 1998).
Inevitably, the industrial revolution also led to the spread of diseases due to poor
hygienic conditions and overcrowding at that time. In addition, high industrial pol-
lution levels appeared and continued to increase exponentially. Here, the dynamics
of diseases became chronic.

HIV and the Aids Pandemic

One of the most compelling cases in recent times of something that began as an
absolute rarity, an exception from the human perspective for man and his health,
concerns the emergence of HIV and its consequent production of AIDS. Indeed, the
origin of HIV and its two types have been the subject of much debate. Both have
been considered to be the result of multiple cross-species transfers of primate
immunodeficiency viruses (SIVs) that naturally affect African primates (Holmes,
2001; Sharp & Hahn, 2010, 2011; Peeters et al., 2013). HIV can be categorized as a
rarity because of the number of exceptional characteristics it possesses. It belongs
to the retrovirus family. These viruses are exceptional because they can reverse the
current standard order of cell biology we saw in the origin of life chapter (transcrip-
tion of DNA into RNA) (Weiss, 1996). Retroviruses generally do not break the cell
membrane to release their copies (Aberth, 2011). In addition, retroviral DNA can
remain dormant within the cell for years and suddenly become activated. Within
retroviruses, HIV is particular in that it can specifically target crucial cells of the
immune system that present the CD4 receptor to which the virus interacts (Aberth,
2011). Compared to other viruses that wage battles with the immune system to see
who prevails, HIV takes it hostage by using its cells to replicate. It also belongs to
the subclass of retroviruses that cause a slow infection (Lentivirus) (Haase, 1986).
Patients, in general, can go a long time being asymptomatic, which gives the virus
an advantage from the point of view of propagation. Finally, patients are prone to
other diseases, as AIDS is not the one that kills but leaves the way open for the body
with no immune system to perish under the action of other diseases, which would
otherwise be contained (Aberth, 2011). Something that was initially restricted to
monkeys, then passed to apes and from them to man, generating a pandemic pro-
cess. Considering the more than 26 species of nonhuman primates involved, hypoth-
eses on the nonspecific transmission of viruses, their mutations, and consequent
transformations between species, it has been discussed whether the appearance of
AIDS then constituted a zoonosis (see debates between Hahn et al., 2000 & Marx
et al., 2004).
The truth is that today, in terms of epidemiology, incidence, and prevalence of
HIV, it can be stated that this is a disease that can no longer be pigeonholed into a
social group as it was done in the early 1980s. Today, the incidence of the virus is
related to culture and the level of awareness of people belonging to different groups.
For example, today, in first-world countries, the disease affects mainly white hetero-
sexuals and women. However, the virus continues to have an incidence within the
284 6 Focusing on Dynamics: When an Exception Becomes a Rule

homosexual community. The myth that this was a disease only associated with
homosexuals is now a thing of the past. On the other hand, in Africa, there is a
higher incidence in people of color and heterosexuals, with a high incidence in
women. Beliefs and rituals have a lot to do with this. On a global scale, AIDS cases
have decreased, and patients now live with the disease chronically, without it being
a death sentence. These individuals have a life expectancy that is close to the aver-
age (Becerra et al., 2016). Unfortunately, due to the complexity of the virus, devel-
oping an effective vaccine is difficult, but the effects of antiviral therapy allow the
disease to be controlled.
The AIDS pandemic serves as a clear example of a transition from something
rare and confined to something widespread. Initially, specific groups such as homo-
sexuals, sex workers, hemophiliacs, or Haitian immigrants were disproportionately
affected and were at the forefront of detected cases (Aberth, 2011). However, as
time progressed, the perception and understanding of the disease evolved, and the
social taboo surrounding the subject began to diminish. Like other pandemics,
human beings initially discriminated against those with the disease. It was only with
the realization that anyone could be exposed and at risk that the collective perspec-
tive gradually changed. This shift in perspective has led to a broader and more
empathetic approach to addressing the AIDS pandemic.

Influenza and Covid-19

Influenza viruses are classified according to their host and the subtype of surface
proteins that allow them to interact with the host cell they infect. These proteins are
highly variable due to the high rate of mutations and/or recombinations. Thus, the
nomenclature of the virus has the letters A, B, and C according to the host and then
H (Hemagglutinin) N (Neuraminidase) with a subscript indicating what type of pro-
tein it is (e.g., AH1N1 is influenza that infects humans and animals and has the
subtypes 1 of membrane proteins). The natural reservoirs are animals such as birds,
pigs, and bats. Some strains share one of the receptors between both species, which
makes the infection less effective in humans, but recombination may make the
infection more specific in humans (Webster, 2002; Rodríguez Lozano, 2009; Ozawa
& Kawaoka, 2013).
Different types of influenza have caused many epidemics and pandemics.
Perhaps the worst influenza pandemic known to date is the misnamed “Spanish flu”
(Spain was the neutral nation in World War I, which was the first to report its occur-
rence) (Flecknoe et al., 2018). The virus is believed to have appeared explosively in
Kansas, USA, at a military camp. The US military carried it to Europe in World War
I (Patterson & Pyle, 1991; Oxford et al., 2005; Foss, 2020). It is estimated to have
killed 27% of the world’s population. The second wave is said to have been more
deadly and coincided with the end of WWI. It was an exceptional moment in human
history where the devastation of war, the mutation and increased virulence of the
virus, and the relaxation of social measures combined, a cocktail that proved deadly.
There were other influenza epidemics, some of which were classified as potentially
pandemic pathogens (PPPs) according to the WHO. Several different viruses cause
6.3 E-R Changes Due to Human Activity on Nature 285

seasonal influenza. It is a chronic seasonal disease and is controlled by the vaccina-

tion of people at risk.
At the end of 2019, a respiratory syndrome generating pneumonia appeared in
the Chinese city of Wuhan. It was detected as a coronavirus that was named SARS
CoV-2, and the disease was named COVID-19 (Lango, 2020; Singhal, 2020;
Al-Qahtani, 2020). It was thought that the outbreak could be controlled locally, and
no immediate action was taken, allowing the progressive spread of the epidemic to
become a global pandemic. Air routes and ease of travel for much of the world’s
population facilitated the rapid spread of the disease. Additionally, ignorance about
the pathogen and poor political, social, and sanitary decisions made it difficult to
control the disease in many countries.
As a rule, quarantine and lockdown systems were implemented globally. Many
countries did not adequately comply with the primary control and prevention mea-
sures and served as a substrate for virus mutation and the emergence of new strains.
By the mid-2020s, vaccines began to be applied, and they helped to control the
spread of the disease, thus establishing a new “normality” thus far. This description
is real-time, and there is still much to learn because it is fully developed and cannot
be compared with the other pandemics we have analyzed (Pigna, 2020).
We see it very easy to relate the disease cycle to human activities (McNeill, 1998;
Aberth, 2011). Many diseases common in the past are becoming rare today thanks
to health policies, changes in people’s habits, and global vaccination campaigns
(Cockburn, 1963; McNeill, 1998).

Change in the Incidence of “Civilization Diseases”

Some diseases or conditions are entirely related to the development of modern civi-
lization, especially Western civilization, mainly with its current diet and lifestyle
(Carrera-Bastos et al., 2011; Kopp, 2019). Thus, these conditions were rare or non-
existent in ancient times but changed the status to frequent or common diseases
(Bollet & Jay, 2004) and are called “Civilization diseases” (Carrera-Bastos et al.,
2011; Kopp, 2019). Here, there is a clear shift between what was the rule and what
was the exception. Until the late twentieth century, most deaths were due to infec-
tious diseases. That was the rule. Today, many deaths are from noninfectious and
degenerative diseases. It is even more common and notorious in Western civilized
societies and infrequent in places where more primitive systems, such as hunting
and gathering, and less westernized societies, are followed.
We will take as an example obesity, which is currently considered a pandemic
with many health implications (Roth et al., 2004; James, 2008; Kopp, 2019). What
is striking is the change of conception about this condition, which went from merely
an esthetic and monocausal norm to being cataloged as a chronic, dangerous disease
with multiple causes. What used to be seen as a rarity has now become common-
place. Its causes have much to do with the change from exception to rule in human
habits. For example, the poor quality of sleep and/or lack of sleep causes circadian
rhythms and metabolism to be altered. As a result, the individual spends more time
awake and eats more outside regular eating schedules. Throughout history, we went
286 6 Focusing on Dynamics: When an Exception Becomes a Rule

from eating a few times a week or a few times a day to eating at all hours. Another
cause is related to our stable environment, where physical activity is not the same as
our ancestors did. Again, a change from exception to the implicit rule, where now
the intake in portion size is much higher but commonly nutritionally poor (Kaidar-­
Person et al., 2008; Khanna et al., 2012; Lieskovská & Megyesiová, 2015; Bitar,
2018). In addition, another linked change is that houses are temperature condi-
tioned, which results, for example, in the body not expending energy trying to con-
serve heat (Kotradyová et al., 2013). The type of food in modern societies has
undergone significant changes at a much faster pace than human beings have been
able to adapt to. As a general trend, we have moved away from a Paleolithic type of
nutrition, where protein and fat were predominant over carbohydrates, and refined
sugars and dairy products were absent (Kopp, 2019). Let us remember that our
metabolism and genetics are still adapted to that nutrition. The deviation from this
ancestral diet to modern dietary habits can contribute to nutritional issues and health
problems in contemporary times (Rendel, 1970).
Fat has a particular behavior in obese people. It represents a tissue that usually
fulfills the function of energy storage. However, adipocytes (cells that form fat tis-
sue) also have a secretory function and can release hormones and fatty acids that
impact metabolism and interact with other tissues (Roth et al., 2004; Berggren et al.,
2005). When this tissue grows too much, it invades other tissues, causing fatty
organs, coronary problems, diabetes, and inflammation. It is an exciting paradigm
shift that changes how obesity is currently perceived and treated. Obesity is directly
associated with two other common civilization diseases, coronary heart disease, and
diabetes (Rana et al., 2007). Obesity is prone to the occurrence of these two condi-
tions that were not as common in ancient times. In addition, the change in lifestyle
that we cited for obesity predisposes individuals to the appearance of these and
other associated diseases (Betlejewski, 2007). Obesity is a complex and challenging
disease that requires a comprehensive approach to treatment. It is not just about
relearning eating habits and incorporating exercise but also addressing psychologi-
cal and emotional factors. A holistic approach that encompasses mental well-being
and emotional support is crucial for successful management.
Regarding modern campaigns that promote obesity acceptance, there is a fine
line between body acceptance and normalizing a serious health condition. While
promoting body acceptance and self-love is essential, it is equally important to
address the health risks associated with obesity. Sending messages that trivialize or
normalize obesity can be dangerous, as it may undermine efforts to combat this
health issue and compromise the overall well-being of individuals affected by it.
Balancing body acceptance with the recognition of the importance of maintaining a
healthy weight is essential to promote both physical and mental health.
Additionally, stress deserves a separate paragraph. Stress is a beneficial mecha-
nism for survival. It keeps us alert and triggers the flight or fight reflex (Chrousos,
2009) that has served us so well from an evolutionary point of view. However, a
mechanism that did not evolve as a disease today is an intermediary that generates
many deaths worldwide or has undesirable consequences. The passage from excep-
tion to rule is apparent here.
6.3 E-R Changes Due to Human Activity on Nature 287

Alzheimer’s: Rare in Young People, Common in the Elderly?

Alzheimer’s syndrome is a neurodegenerative disease that became prominent at the
beginning of the twentieth century (Petsko, 2006). The disease was probably not
new but very rare and had a very low incidence before this date (Mahandra, 1984).
It is a rare disease in other species and predominantly in humans (Gunn-Moore
et al., 2018). Historical analysis agrees that it had a low prevalence prior to the
twentieth century (Bondi et al., 2017). Many think it was due to low life expectancy.
It is a common perception that the rule in ancient times was to live to age 40.
However, it is recognized that people have reached average ages similar to today
without problems (Griffin, 2008). The rule in those times was that the adult survival
rate was low (Robson & Kaplan, 2003; Burger et al., 2012; Kua et al., 2014).
Therefore, it is not rare for humans to live more than 60 years. However, it was
perhaps rare because they did not survive birth or infancy (Montagu, 1994). In addi-
tion, they had to endure wars and killings, severe famines, or, as we said before,
plagues or diseases that some are today easily curable as superficial bacterial infec-
tion that today is treated with antibiotics but that in the nineteenth century was the
most frequent cause of death (Zaffiri et al., 2012). Likewise, it is not ruled out, as
with other syndromes, that it was not accurately diagnosed in ancient times, and its
low incidence is partly due to this phenomenon (see Chap. 8).
This age-related view is associated with the low incidence of Alzheimer’s dis-
ease in young people and its prevalence in older adults (Petsko, 2006). However,
some studies associate the disease’s spread with substantial physical activity
declines. Imagine our hunter-gatherer ancestors, the rule was to spend a lot of time
wandering and hunting, with all the physical exertion that entails. They performed
an average of four times more physical activity than people do today. Currently,
despite the growing fitness trend, the overall level of physical exercise in modern
society has decreased significantly compared to that in the past.
People who perform moderate to high physical activity lower the probability of
developing the disease by 30%. Therefore, whether it is because of the increase in
human longevity or the decrease in physical activity, it is clear that Alzheimer’s is a
disease that has gone from being rare to very common and with a high incidence
among adults.

Anecdotal Case in History

A rare and curious historical case was the dancing epidemic that ravaged Strasbourg,
France, in the sixteenth century (Pigna, 2020). Infected people danced uncontrol-
lably and died of exhaustion. It could have been an outbreak of collective psychosis,
or it could have been associated with a rare genetic disease with a high prevalence
rate due to the high consanguinity of the region. There is also talk of massive intoxi-
cation with hallucinogenic substances with precursors of LSD (Matossian, 1989;
Waller, 2008, 2009; Pigna, 2020).
In conclusion, the passage from the exception to the rule has been given mainly
by the change in the human population’s lifestyle. Thus, the change in relationships,
288 6 Focusing on Dynamics: When an Exception Becomes a Rule

economy, science, technology, and food has impacted human life from the health
point of view, opening doors to new diseases and conditions that, from being
restricted or absent, have become part of people’s daily lives. Some, such as conta-
gious diseases, may be relatively easy to attack. However, others, such as diseases
related to contemporary Western civilization, are much more challenging to combat
and will again require a significant change from rule to an exception in human
activities and customs. Just as we saw that we are responsible for their emergence,
we are also responsible for their combat and eradication. In Chap. 8, we will con-
tinue to discuss rules and exceptions in medicine, giving a general overview of the
subject’s current state and the horizons we can expect.

6.3.3 Influence of Environmental Pollution

and Climate Change

Humans have dramatically modified the environment without ceasing to be part

of it. However, many human activities generate drastic modifications of the
environment that tend to break the dynamic equilibrium between the two (see
the analogy between humans and viruses in the previous section). A term has
been coined to describe a new geological era known as the Anthropocene that
began in 1950 with the appearance of general-purpose plastic and became a key
indicator of human activity (Zalasiewicz et al., 2016; Geyer, 2020). While many
may talk about many animals changing the environment drastically, such as
beavers building dams, few animals have reached the level of change that
humans have generated. One of the environmental concerns caused by human
interference is environmental pollution.
Environmental pollution is the phenomenon by which harmful substances of
various kinds are introduced into the environment, damaging the entire system,
including the living organisms that inhabit it (Merriam-Webster, 2010). This pollu-
tion can be natural or artificial (Farmer, 2002). Thus, planet Earth has seen many
similar instances in which harmful substances were produced that harmed or even
changed the environment during its long life. We have already mentioned the origin
of life and oxygen production, which may have been considered harmful at the time
but was later used beneficially by organisms adapted for that purpose. Additionally,
significant catastrophes that produced massive extinctions can be considered events
that pollute the planet, harming many living organisms. It occurred in the Permian
(Benton & Twitchett, 2003) and in the Cretaceous–Tertiary boundary, an event that
ended with dinosaurs (Officer & Drake, 1983; Shaw, 2018). Certainly, in these
cases, the primary causes were volcanoes, abrupt climate changes (Crowley &
North, 1988), and/or space asteroids (Alvarez et al., 1980). However, it is rare for a
living organism to modify its environment to jeopardize its own existence. While
certain examples of species modifying the environment exist in nature, these species
generate modifications while maintaining a sustainable balance between their popu-
lation and the surrounding environment (Wright et al., 2002).
6.3 E-R Changes Due to Human Activity on Nature 289

Like any other animal, human activities have historically produced manageable
amounts of waste and residues without introducing or generating elements that were
not naturally present in the environment. As humanity moved away from wilderness
and clustered in cities, environmental change increased, as did water and land pol-
lution (See Markham, 2019). The industrial revolution is one of the critical points in
humanity that could be taken as a point of no return. While it sparked numerous
advances that ultimately benefited society, the environment has endured and contin-
ues to endure significant suffering as a consequence. Air pollution levels escalated
exponentially (e.g., Klimont et al., 2013). The levels peaked in the 1970s and
dropped slightly until our time. This modification of the air brought with it prob-
lems with the ozone layer related to greenhouse gases. These gases concentrate in
the atmosphere and generate a layer that does not allow heat dissipation, producing
the famous greenhouse anomaly linked to climate disruption (Kweku et al., 2018).
This phenomenon contributes to a larger-scale issue known as global warming.
Despite attempts by various conspiracy theories and unfounded claims to divert
attention and cast doubt on the reality of global warming, its validity is evident and
undeniable to anyone who examines the evidence.
As with pollution, climate change is not a rare phenomenon on the planet
(Crowley & North, 1988; Huber et al., 2000). There have been many periods of
abrupt climate change (Crowley & North, 1988). For example, in The Middle Ages
(mid-fourteenth to mid-nineteenth centuries), humanity witnessed “The Little Ice
Age” in which the European climate was impacted, resulting in glacial expansions
and altered climatic conditions (Mann, 2002; Matthews & Briffa, 2005). However,
this was not a global-scale phenomenon but was confined to the northern hemi-
sphere (Bradley & Jonest, 1993; Mann et al., 1999; Mann, 2002). However, none of
these climate changes had a human component or even resulted from any other
organism on the planet and are considered regular climate cycles.
Thus, we see that although environmental pollution and climate change may
have a purely natural component, they are processes that have been greatly acceler-
ated in recent decades by human action. Many patterns and processes they trigger
were rare before and are very common now. We will cite a few examples to illustrate
this idea.

6.3.3.1 Water and Air Pollution

Contamination of water, air, and soil has been extensively studied. For example,
water can be contaminated with organic matter, mainly phosphorus and nitrogen,
derived from nutrients from high loads of wastewater and fertilizers from agricul-
tural activities. It results in cultural (human) eutrophication, which generates the
pollution of marine coasts, estuaries, and rivers (Seitzinger et al., 2002 Glibert et al.,
2005; Burkholder et al., 2007). It is one of the most significant pollution problems
worldwide (Howarth et al., 2002; Glibert et al., 2005). Although eutrophication can
occur naturally (e.g., upwelling) (Richardson & Jørgensen, 1996), it occurs in a
more controlled manner compared to human-generated eutrophication, mainly
290 6 Focusing on Dynamics: When an Exception Becomes a Rule

because of the magnitude of the impact. Eutrophication, in turn, leads to uncon-

trolled growth of certain species of toxic harmful algal bloom species (Smayda,
1990; Anderson et al., 2002; Glibert et al., 2005), oxygen deficits, and death of vari-
ous organisms (Bricker et al., 1999; Burkholder, 2001; Burkholder et al., 2007).
There is a dynamic balance between light, nutrient availability, and temperature in
nature. These are the factors that may limit plant biomass production. When nutri-
ents condition biomass increase, their exogenous incorporation via eutrophication
can affect the biomass in the ecosystem (Richardson & Jørgensen, 1996). Thus,
naturally, this eutrophication phenomenon is infrequent, so the effects on algal and
plankton populations are rare. At the same time, their influence on other organisms
is rare when there is an uncontrolled increase in biomass (blooms), generating
hypoxia and even changing the diversity and abundance of species. This behavior
may be natural in the organism, but the magnitude of population growth and the
exacerbated action on other individuals is often the exception in nature. Studies
report that blooms are more significant, toxic, and prolonged than they used to be
(e.g., Anderson et al., 2002) and that the presence of soot and smog in large cities is
not normal. An interesting case of microevolution and the influence of the industrial
revolution on air pollution and its impact on organisms is reflected in a species of
butterfly associated with trees in the industrial regions of England. Peppered moths
(Biston betularia) are nocturnal Lepidoptera that can have two morphs (insularia
[light] and carbonaria [dark]) (Cook et al., 1986).
The light morph (insularia) mimics very well with the tree trunk, which was also
light and contained lichens. Increased pollution and soot deposition resulted in the
darkening of the tree trunk and elimination of lichens, making light butterflies
highly visible and favoring the camouflage of dark butterflies (Majerus, 2009; Curtis
et al., 2008). Although this phenomenon occurred in real time while Darwin was
developing the theory of evolution, he did not explore it (Kettlewell, 1959). Here,
we see how a phenotype that was considered rare changed its status to standard as a
result of environmental change due directly to artificial air pollution. Furthermore,
we know that, in general, with the exception of rare natural cases such as volcanoes
or giant meteorite impacts, the air should be pure and easy to breathe. Unfortunately,
this is currently the exception in certain megacities worldwide, whose pollution and
toxicity make it difficult to breathe such air (Meteosim, 2021).

6.3.3.2 Spill

Natural disasters related to oil were also uncommon, especially when it spilled into
the sea. As with other pollutants, oil spills exist naturally. They are cited in the bible
and are common in places where oil is produced naturally (Nelson-Smith, 1971).
The pollution we are referring to, which was exceptional until the middle of the
nineteenth century, is marine or coastal pollution linked to the transport of crude oil
or the use of gasoline by ships, pollution directly linked to human activity (Blumer,
1971). From the biological point of view, it is a disaster of enormous magnitude,
affecting the ecosystem permanently for an extended period. Organisms are not
6.3 E-R Changes Due to Human Activity on Nature 291

accustomed to or adapted to this type of contamination, which causes many to per-

ish, a situation that would be uncommon in systems without such contamination.

6.3.3.3 Soil

When we refer to the soil, the most abrupt change that man has made is the change
in land management and the production of large arable areas (Power & Follett,
1987). Humans have modified the landscape and produced extensive monocultures
that deviate from the natural patterns found in nature. The norm is that different
plant species are combined (Hooper et al., 2012). Monoculture brings about signifi-
cant pest challenges from insects (Altieri et al., 1984), fungi (Fisher et al., 2012),
and rodents (Howard, 2018), necessitating the use of pesticides for their control and
fertilizers to enhance crop production (Epstein, 1997). All of these examples are
exceptions and exaggerations of what happens naturally.

6.3.3.4 Nuclear Energy

Concerning nuclear energy, both the war tests and the accidents related to nuclear
power plants generated evident changes from exception to rule. Take, for example,
the Chernobyl nuclear disaster (Haynes & Bojcun, 1988). It is evident that this event
led to a disproportionate rise in diseases and malformations associated with elevated
levels of artificial radiation (Lendon & Martin, 2007; Völkle, 2015), a trend that
persists even today (Nesterenko & Yablokov, 2009). Additionally, animals had to
adapt to that radioactive environment. Imagine the changes that must occur in nature
and the adaptations that organisms must develop (Mousseau, 2021). Although many
studies are controversial mainly due to the hermeticism of the former Soviet regime,
some works clarify that species fall in abundance and biodiversity in these contami-
nated areas (Mousseau & Møller, 2012). Thus, the change from exception to rule is
seen in the current presence of many radioactive substances or derivatives that are
not commonly found in the environment (Kholosha et al., 2008). In addition, there
are other cases where spider communities, for example, grow proportionally to the
level of contamination, probably due to the disappearance of other predators of their
food or the malformation and incapacity of prey (Møller et al., 2012).

6.3.3.5 Micro and Nanoplastics

Plastics are generally synthetic polymers. Polymers are not a rarity in nature. They
appear in many natural materials that we have studied in biology. Basic examples
are DNA, spider silk, plant cellulose, hair, and muscle fibers (Geyer, 2020). World
War II triggered the production and use of plastics worldwide. Although plastics
have been around for approximately 100 years, their production and use were rare
prior to WWII (Geyer, 2020). Different types of plastics with different
292 6 Focusing on Dynamics: When an Exception Becomes a Rule

conformations are directly related to their recycling ability. In a gradient from the
easiest to recycle to the most difficult, we would find thermoplastics such as PVC or
PET capable of being melted and, therefore, potentially recyclable. Thermosets that
are more complex in their molecular structure, such as plastic resins or melamine,
are more difficult to recycle. Finally, the combination of thermosets with fibers
makes fiberglass or carbon fiber-reinforced polymers even more difficult to recycle
but resistant. The biodegradation of these materials is a complex mechanism involv-
ing microbes that breakdown the material into its essential components. It is a pro-
cess that takes different rates that can range from weeks to decades.
Plastic became an indicator of human activity on a geological scale. Before 1950,
it was absent from sediments, but it was present from that time onward (Zalasiewicz
et al., 2016). We see how the very presence of the material went from being a rarity
in nature to being a conspicuous constituent in nature. We will now look at the mag-
nitude and impact of the occurrence of this material in the environment.
Plastic produces pollution on different scales. This material generates waste dur-
ing production and disposal of the article after it has been used. Subsequently, recy-
cling produces gas emissions into the atmosphere, as does disposal by burning. Both
are emblematic cases of plastic impact mitigation that generate even more impact.
The only use of waste that does not generate impact, at least for a time, is the reuse
of the product (e.g., reusing plastic containers, bottles, or cups). However, at some
point, the plastic product inevitably ends up being recycled, thermally destroyed, or,
in the worst case, discarded. Due to improper disposal or negligence, plastic enters
marine habitats at a dizzying rate (Steer & Thompson, 2020). Various analyses show
that plastics of various sizes (5 mm and over to less than 0.1 mm) are now the rule
in nature, appearing in freshwater, marine, and terrestrial environments as a poten-
tially hazardous pollutant (Besseling et al., 2017; Li et al., 2019). The most preva-
lent forms of waste are micro and nanoplastics. An intriguing phenomenon is the
formation of a 1.6 million km2 synthetic “island” entirely made of waste known as
“The Great Pacific Garbage Patch” (Kaiser, 2010; Gabrys, 2017; Lebreton et al.,
2018). This immense patch, predominantly composed of plastics, floats through the
Pacific Ocean. The rule was thus far that islands were generated by geological pro-
cesses such as volcanic islands or biological processes such as coral islands.
However, with their waste, humans have become agents that can generate some-
thing similar. Plastics can also interact with marine biota and bioaccumulate in liv-
ing organisms in the ocean (Toussaint et al., 2019; Wang et al., 2021) or become
entangled in them, causing disability or even death (Steer & Thompson, 2020).
As we have seen throughout this section, the examples are many and varied and
work at different scales. What must be clear from this section is that man has become
a potent agent of environmental change, even competing with critical geological
processes that have shaped the planet in ancient times. By shifting the environmen-
tal balance, he produces many changes from exceptions to rules. Although the earth
is suffering at the moment, in the long run, it is used to these cycles of contingency
or stress (e.g., catastrophes and extinctions), and we have seen that it takes time, but
it knows how to recover well. The one whose days may be numbered if it continues
on the current path, is the human species. Humans may eventually join other large
6.3 E-R Changes Due to Human Activity on Nature 293

groups, such as dinosaurs, in the annals of species that succeeded and were able to
transcend but ended up dying out abruptly. The rule is that no matter how long it
takes, the Earth always recovers and is the species that goes extinct. If we do not
change course, we will not be the exception. In the next chapter, we will discuss
how processes linked to human-induced climate change impact species diversity, in
particular, changes from rules to exceptions, the reverse order to the one just
discussed.

6.3.4 Manipulating Organisms to a Destination

6.3.4.1 Artificial Selection: Turning Exceptions into Rules

By understanding the principles of natural selection, we can apply them to enhance

the breeds and varieties of plants and animals. It is already known since Darwin
himself (in fact, he devoted chapters on this) that artificial selection was initiated by
man long before he had any knowledge of the existence of natural selection. The
knowledge of natural selection has further refined these artificial processes, allow-
ing for a more detailed consideration of rarities and exceptions in their entirety. This
optimization enables more efficient and ethical applications in various fields, such
as biomedicine, agronomy, and animal production. In this context, it is interesting
to note that artificial selection is restricted to what is deliberately done by man, for
example, for the domestication of animals or plants for agricultural or ornamental
purposes. Clearly, its definition points exclusively to it: “a process in the breeding
of animals and in the cultivation of plants by which the breeder chooses to perpetu-
ate only those forms having certain desirable inheritable characteristics” (Collins
English Dictionary, 2003). In other words, artificial selection is a method by which
humans intervene in the reproduction of animals and plants to favor the develop-
ment of selected traits, whether for productivity, resistance, docility, esthetics, or
other purposes. In addition to these techniques based on sexual reproduction, genetic
engineering techniques are also used, such as the creation of transgenic and other
genetically modified organisms (Hill & Caballero, 1992; Conner, 2003).
Indeed, the definitions of artificial selection often overlook unguided human
actions, which can have a similar impact on nature. These “involuntary” actions can
also significantly influence and shape natural processes. In other words, we are
referring to artificial selection that is not conscious, not directed to an objective, but
that invariably acts at a selective level on certain organisms. Thus, depending on the
type of planning, two types of artificial selection can be considered: conscious,
when there is an objective, a determined selection plan, and unconscious or invol-
untary, when there is no previously determined objective.
In addition, conscious artificial selection can be differentiated between stabiliz-
ing type selection when those selected are individuals with intermediate character-
istics, where genetic variance is expected to be reduced (Bulmer, 1971), or disruptive
type selection when those selected are individuals with extreme characteristics and
294 6 Focusing on Dynamics: When an Exception Becomes a Rule

genetic variance is expected to increase (Hill & Caballero, 1992). Numerous exam-
ples can be included in involuntary artificial selection, and they occur when animals
face an anthropic environment that we impose. They change to better adjust to it.
Some classic illustrative cases are as follows: (1) due to the effect of the urban envi-
ronment, for example, swallows in United States highways. Now short-winged indi-
viduals are more abundant because they are the ones that better maneuver to avoid
being run over by trucks or cars, and this is reflected in less and less mortality
(Brown & Brown, 2013); (2) due to hunting and fishing. For example, Chesapeake
turtles are evolving to a larger size, as the smaller ones can enter the traps fishermen
use for crabs (Santos et al., 2018); (3) because of environmental pollution, as some
aquatic organisms survive or overcome challenges imposed by us. For example, fish
and invertebrates adapted to PVC spilled throughout rivers and lakes (Lusher et al.,
2020; Hammer et al., 2012); (4) due to the effect of the introduction of exotic spe-
cies (either for productive purposes or to control some local pest) that finally force
certain native organisms to adapt. A clear example appears in an already mentioned
invasive species, the cane toad introduced in Australia (Sect. 6.3.1). Their influence
reduced the head size of the native snakes, as the smaller snakes ate smaller, less
toxic toads and were the surviving individuals (Phillips et al., 2003; Phillips &
Shine, 2006); (5) due to the effect of organisms that are released into habitats other
than their natural habitat and must adapt to survive. For example, on Pod Mrcaru
Island in the Adriatic Sea, a population of lizards of the species Podarcis sicula was
released. The lizards came from an island abundant in insects, so their diet was
practically insectivorous. However, on the newly colonized island, the abundance of
insects was much lower, and plants were more abundant. This species of lizard
changed the basis of their diet and adapted to eating leaves. Among other adaptive
characteristics, they developed a larger head to give a better bite, and their legs
became shorter as there was no need to run to hunt (Herrel et al., 2008).
All these cases are ultimately events of natural selection in the broad sense.
However, in a narrower sense, they represent examples of artificial selection since
they involve modified scenarios and conditions imposed directly (with an objective)
or indirectly (unconsciously) by man. These clarifications are important, as they
expand the concept of artificial selection beyond its strict definition as deliberately
oriented by humans. Whether we are aware of it or not, in all these cases, we start
with exceptions that potentially lie at the extremes of the trait distribution, which is
often continuous. For example, short wings in the US highway swallows, extralarge
body size in the turtles mentioned above, and the small head in the snakes of north-
ern Australia (Fig. 6.3a, c). In short, something analogous to natural selection on
extreme variants is done, mainly by directional selection.
Indeed, the birth of agriculture serves as a compelling example of conscious
artificial selection. During this transformative period, humans made a significant
decision to choose wheat spikes in which the seeds (grains) would not naturally fall
and disperse to the ground, as was the “rule” in the species. By deliberately select-
ing these monodispersing spikes, humans altered the natural mechanism of seed
dispersal, which allowed for better control over the crop and facilitated cultivation.
This act of conscious artificial selection marked a pivotal moment in human history
6.3 E-R Changes Due to Human Activity on Nature 295

Fig. 6.3 Species under

involuntary artificial a
selection. (a) Petrochelidon
pyrrhonota, American cliff
swallow (Credits: Channel
City Camera Club from
Santa Barbara). (b)
Malaclemys terrapin,
diamondback terrapin. (c)
Acanthophis praelongus,
northern death adder.
(Credits: Valentin Moser)
(a) Petrochelidon
pyrrhonota. License: CC b
BY 2.0 <https://
creativecommons.org/
licenses/by/2.0>, via
Wikimedia Commons.
https://commons.
wikimedia.org/wiki/
File:Cliff_Swallow_
(51120316295).jpg. (b)
Malaclemys terrapin.
License: Public domain,
via Wikimedia Commons.
No machine-readable
author provided. Ltshears
assumed (based on
copyright claims). https://
commons.wikimedia.org/
wiki/File:Diamondback_
Terrapin.jpg. (c)
Acanthophis praelongus. c
License: CC BY 4.0
<https://creativecommons.
org/licenses/by/4.0>.
https://www.inaturalist.org/
photos/29424801

and laid the foundation for modern agriculture. These seeds were sown. If the trait
was inheritable and not merely ontogenetically acquired, a proportion of the off-
spring replicated that trait, which was in itself an exception. That is, something even
teratological, since that characteristic of “not opening” of the spike was an attempt
against the reproduction of the species. By using this to domesticate the plant, it is
considered man-initiated agriculture. Different wheat species are used for different
purposes. For example, the flour we use today also results from an artificial selec-
tion process. Triticum monococcum and Aegilops speltoides were crossed and
296 6 Focusing on Dynamics: When an Exception Becomes a Rule

resulted in T. dicoccum, and when crossed with A. squarrosa, they resulted in T. aes-
tivum, known as common wheat, from which many products for human consump-
tion are made (Gregory, 2009). Another notable example, because of its importance
in human consumption, is maize. Almost all maize harvested in the world today is
“hybrid maize,” i.e., a product of artificial selection. We will discuss this in the fol-
lowing chapters. Improvement after domestication has led to changes in morphol-
ogy, yield, plant habit, and biochemical composition (Gregory, 2009; Wright et al.,
2005; Gage et al., 2017). Among other examples that increased their productivity
thanks to artificial selection, we can name them rice (Izawa, 2007) and rye (Cooper,
1960; Robertson, 1961). The creation of different species of cabbage plants
(Brassica oleracea) to obtain a greater variety of vegetables has given rise to differ-
ent varieties grouped in cultivar groups, such as brussels sprouts, cauliflower, and
broccoli (Gregory, 2009). The example of bananas (Musa paradisiaca) is an excep-
tional case of conscious artificial selection and how an exception becomes a rule.
The domestic banana, whose fruit is consumed worldwide, is characterized by being
fleshy and small-seeded and has the right length and thickness to fit in hand. This
fruit descends from hybridization and selection between species of the Musaceae
family, native to Indonesia. The fruit of this wild plant is small and oval, not so
fleshy, and its seeds are enormous compared to those of its artificial descendants (Li
& Ge, 2017). On the other hand, varieties of stunning beauty in ornamental plants
have also developed through artificial selection for desired characteristics that, in
most cases, were simple exceptions in ancestral populations (Zhang & Liu, 1998).
For example, of conscious artificial selection involving animals, we can mention
a few among a large number. For example, the domestic dog (Canis lupus familia-
ris) originated from populations of the gray wolf (C. lupus); all current varieties of
domestic dogs are the product of artificial selection. Current dog varieties are task-­
oriented, such as guarding, companionship, and esthetic purposes, or species that
humans consider “cute,” e.g., breeds such as poodles and bulldogs (Frank, 1980;
Hedrick, 2015).
Today’s dairy cows are the result of many years of selective breeding, where
those individuals who produced more milk, the exceptions that differed from the
average, were selected, and these were the ones that, in turn, were made to breed
(Flori et al., 2009; Hedrick, 2015). In addition, excellent varieties have been created,
such as the “Patagonian Dynasty,” transgenic cows capable of producing insulin in
their milk (Linares & Maciel, 2017). Other examples, such as farm animals for
higher body weight and greater body fat thickness, have also been under artificial
selection for higher productivity and profitability (Hetzer & Harvey, 1967; Verghese
& Nordskog, 1968). Racehorses are bred under artificial selection to create a higher
probability of producing faster and stronger horses in subsequent generations,
which generates a business with significant economic benefits (Hanot et al., 2018).
In the laboratory, mice, for example, have been selected to be able to run at a much
faster speed than mice from control lines. These mice have body adaptations that
give them higher levels of endurance (Swallow et al., 1998). Additionally, species
such as guppies (Poecilia reticulata), freshwater fish native to Central America, are
under artificial selection processes where those with the most attractive colors are
6.3 E-R Changes Due to Human Activity on Nature 297

selected to reproduce in search of the most “beautiful” ones (Endler, 1980; Kotrschal
et al., 2014).
Indeed, these examples are repeated with some similarity in the process in many
other examples of agriculture, forestry, fish farming, livestock, ornamentation, and
biomedicine, among others. Every innovation arises from the deliberate selection of
an unusual variety, either in its entirety or specifically with a unique trait “x.” This
trait may be rare and unremarkable in the organism’s natural environment, but due
to some desirable quality, it becomes the ideal choice for a particular human inter-
est. That variety can indeed be a single specimen or two before the beginning of the
process of artificial selection. Therefore, this context resembles the teratological
from a realistic perspective of the species. Just think of the extravagant dog breeds
from an adaptive point of view; there are teratologies everywhere.
An interesting point to mention is that many times it has been demonstrated how
to go back from something that by artificial selection became the rule to the ances-
tral pattern. Let us think of cases where more than 10,000 years ago man “chose” an
exception of interest in a certain organism and transformed it into a rule, perhaps
having completely transformed what the initial rule was for that species. It should
be noted that variants often appear in artificially selected organisms that a breeder
may see as teratologies but which in reality are nothing more than ancestral traits
that refuse to disappear. There are plans that seek to vindicate ancestral and/or lost
traits. In this scenario prevails the quest for exceptions in the genes, phenotypes of
some specimens, or dispersed breeds. It is aimed to “put it all together” to go toward
that lost ancestral rule. In other words, to recover the appearance, the morphology
of the original organism. The results of this selection can then be placed in nature to
test the aptitude of these “new” (original?) variants (Conner, 2003). In this regard,
we use two examples. The first is that of the Aurochs (Bos primigenius). This spe-
cies of animal, similar to bulls and bison, existed thousands of years ago in Europe.
Humans began to domesticate them and select various genetic traits to make them
increasingly docile and tame, creating several different species of cattle. A group of
researchers set out to “resurrect” the original aurochs. By crossing different species
of cattle, they have achieved the original genetic characteristics of the aurochs and
have managed to obtain 80% of the original genome (Kyselý, 2008). The second
example conveys the common pigeon (Columba livia), where wild phenotype
reconstruction could now occur (Sol, 2008).
It will be interesting to see in these projects if the current rule (traits that have
already been artificially selected) remains as mere exceptions in these future
“retro”—artificial secondary organisms, returning to the old version of the organism
via reversion. This connects with an additional idea, implicit but worth emphasiz-
ing, which is that the varieties we have created by artificial selection are abnormali-
ties for the species itself. This is clearly seen, as we exposed above, in some
examples, in breeds of dogs, fish, cattle, and plants, with exacerbated traits of size,
length, height, body color, appendages, or others. If these traits appeared in the
original population, it would not be simply an extreme value of natural variability
but true teratologies. Indeed, this would even imply a break in the continuum of trait
distribution, something even more discrete and strikingly different. In other words,
298 6 Focusing on Dynamics: When an Exception Becomes a Rule

humans “create teratologies” for our benefit. This is a not insignificant point, which
involves us directly in the dynamics between rules and exceptions with living
beings, as no other organism on Earth has ever done before. Many varieties of plants
and breeds of animals are “beautiful” from our point of view or even appear so to us
because of their bizarre characters (this is what we are attracted to show). However,
from the natural perspective of the species, they may be “monsters.” Indeed, in some
species, artificial selection has gone too far, favoring traits with which the species
would not have been able to survive in nature for different reasons, for example,
difficulty in feeding, moving, or reproducing, among others. In other words, this
exception would hardly have become the rule. There are many illustrative cases in
this respect of birds (e.g., Mitchell, 2014). For example, the common pigeon
(Columba livia), which has almost no beak, bulging eyes, and a tiny skull, is one of
the pigeon breeds we consider “beautiful” (Parrott-Holden, 1987); the Gibber itali-
cus (Serinus canaria) domestic canary, which has been selectively bred for a few
hundred years and where breeders can control everything from skeletal formation,
the number of feathers, to the length and style of the bird’s song (Bartels, 2003);
chickens bred to develop larger breasts, the giant Junglefowl (Gallus gallus) have
great difficulty moving and hearts that have not been adapted to support the addi-
tional mass (Paxton et al., 2010).
Among the fish, bubble eye goldfish (Carassius auratus) is a species that has
been created through artificial selection, especially for the delight of the human
observer, resulting in an incredible variety of shapes and sizes. This fish grows large
fluid-filled sacs under the eyes and has malformed, upturned eyes, a curved spine,
and no dorsal fin (Komiyama et al., 2009). The Rhodesian Ridgeback dog breed was
bred for hunting and is large, fast, solid, and has excellent eyesight. However, it may
possess a hole toward the end of the spine that leaves nerve tissue exposed to bacte-
ria (Hedrick, 2015). Something similar occurs with the German Shepherd (Deutscher
Schäferhund), a beautiful, intelligent, and protective dog with cinnamon and black
fur widely used by security forces and the military. Among other diseases, it is com-
mon for large specimens to suffer from hip dysplasia, which causes deformities and
problems in the posterior area and much pain (Hedhammar et al., 1979; Rossi, 2018).
On the other hand, it should be noted that most plant and animal species domes-
ticated through artificial selection suffer a similar effect to the bottleneck (see Sect.
6.2.2.1) as their genetic diversity decreases concerning their wild ancestor (Wright
et al., 2005). This results in increased vulnerability to disease and an increased inci-
dence of morphological problems that would otherwise be minimized or eliminated
by natural selection (Robertson, 1961; Conner, 2003). In addition, it can shorten the
life span of selected organisms, create new mutations that it is not known how they
will be routed later, and cause sterility (see the iconic example of sterility in bananas,
Pearce, 2003, 2008).
All we have mentioned and exemplified in the present section provide clear evi-
dence of the artificial selection of dynamics between exception and rule. If we as
humans become more aware of this, it would allow us to be more responsible for the
impact of creating breeds, “quasi” teratological variants, which could bring to a
directional limit the genetics and phenotype of a given species (e.g., to the detriment
6.3 E-R Changes Due to Human Activity on Nature 299

of its ancestral genotype and morphotype). Most importantly, we must be more

responsible for clearly foreseeing the direct and indirect effects of such manipula-
tion and this “new organism” on other species and ecosystems. Time will tell how
this will affect nature worldwide in a much more generalized way and what our role
will be in this challenging scenario.

6.3.4.2 “Artificial” Cloning, the Transition from Exceptions to Rules?

On the subject of artificial cloning, it is necessary first to be clear about what clon-
ing is in a natural context. In this sense, cloning obtains a biological entity (gene,
chromosome, cell, or organism) genetically identical to another by asexual repro-
duction mechanisms where only one parent is involved (Chuaire et al., 2004).
Cloning appeared at the early stages of the evolutionary process, when microorgan-
isms began to produce copies of themselves by mitosis. Thus, a somatic cell repli-
cates, and the genetic material of the daughter cells is identical to that of the mother
cell. We could consider mitosis a type of “natural” cloning (Chuaire et al., 2004). In
nature, asexual reproduction or clonal reproduction is widespread in “lower” organ-
isms, such as bacteria, protists, and other unicellular organisms (Logares et al.,
2009), as well as in multicellular animals, such as sponges, coelenterates, flatworms,
annelids, and echinoderms (Ereskovsky & Tokina, 2007; Kostyuchenko et al., 2016;
Rubilar et al., 2005). Asexual reproduction only occurs in organisms whose cells
retain the property of embryonic totipotency (the ability to multiply and differenti-
ate into different cell types). Indeed, cloning is an intrinsic element of perpetuation
in the offspring of more organisms than we initially imagined. Thus, although the
primary form of reproduction of eukaryotic organisms is sexual reproduction, many
groups also use asexual reproduction as a mechanism for producing offspring. Most
fungi can reproduce sexually and asexually (Elliott & Maheshwari, 1994; Taylor
et al., 2015). Yeasts, for example, reproduce asexually by budding, and other fungi
can reproduce by spore production. Examples of asexual reproduction are also
observed in plants, which occurs when a plant part divides and develops separately
into a new plant (Cook, 1979; Bengtsson & Ceplitis, 2000). Among the most com-
mon forms is the production of propagules and apomixis, among others. Examples
are northern highbush blueberry (Vaccinium corymbosum), common hazel (Corylus
avellana), and quaking aspen (Populus tremuloides).
Let us look at cloning from a macroevolutionary perspective, i.e., considering the
whole tree of life. We could say that in terms of the number of species and branches
derived in the evolution of living beings (e.g., toward newer animals and plants), it
went from being a rule as such (i.e., reproduction only or mainly by cloning) to an
exception (i.e., reproduction only by sexual means). However, if we focus on the
microevolutionary level, we see that there is a dual dynamic with sexual reproduc-
tion in many groups. For example, some insect species can switch their reproductive
mode between sexual and asexual reproduction, depending on seasonal changes in
temperature and day length (Razmjou et al., 2010; Peng et al., 2017; Kokko, 2020).
These two reproductive patterns in one species have been observed in aphids (Le
300 6 Focusing on Dynamics: When an Exception Becomes a Rule

Trionnaire et al., 2008; Ollivier et al., 2012; Shuo et al., 2020), termites (Matsuura
et al., 2009; Yashiro & Matsuura, 2014), ants (Pearcy et al., 2004; Fournier et al.,
2005), bees (Beekman et al., 2011), beetles (Perotti et al., 2016), and locusts
(Hamilton, 1953). Another example where this occurs is flatworms (Ramm, 2017).
Among vertebrates, we can name whiptail lizards (Cnemidophorus sp.), a species of
Teidae where asexual reproduction is favored in the peripheral zones of the distribu-
tion (Wright & Lowe, 1968).
In contrast to natural cloning, artificial cloning techniques require a manipula-
tion process to obtain copies of the mother cell. Within artificial cloning, we can
mention reproductive cloning, which aims to duplicate complete living beings (the
embryo is transferred to a uterus for implantation in the endometrium, and thus a
new organism develops) (Hochedlinger & Jaenisch, 2003; Rideout et al., 2002). On
the other hand, there is therapeutic cloning, which aims to become an alternative for
the treatment of some diseases and the replacement of injured tissues or organs
(here, the embryo is transferred to a culture medium and will give rise to embryonic
stem cells with the potential to differentiate into different cell types) (Keller &
Snodgrass, 1999; Cibelli et al., 2001). Several methods have been developed for
artificial cloning, including somatic cell nuclear transfer (SCNT) cloning (Pardo,
1997; Keefer, 2015). In this technique, two types of cells are used: somatic and
female sex cells. In the procedure, genetic material is extracted from both cell types,
and the nucleus of the somatic cell to be cloned (donor) is injected into the female
sex cell (recipient) (Gurdon & Byrne, 2003; Li et al., 2003; Hochedlinger &
Jaenisch, 2003).
Artificial cloning has been applied without much discussion in plants, which,
possibly, being “phenotypically alien” to a human, did not produce ethical and
moral controversy. Artificial cloning in plants is highly relevant (Giacometti, 1990).
Initially, focused on cultivating flowers, most studies on artificial cloning in plants
are currently focused on species with desirable agronomic characteristics, for exam-
ple, to increase their production. With the application of the latest plant cloning
techniques, it is possible to regenerate an entire plant from a single plant cell, tissue,
or organ (González Jiménez, 1998; Torres et al., 2000).
The panorama of artificial cloning changes drastically when talking about ani-
mals, where numerous preliminary tests, and failed experiments, to others close to
its realization, such as the pioneering work of J. Gurdon in the early 1960s when he
successfully cloned the frog Xenopus laevis (Elsdale et al., 1960; Gurdon, 1996;
Gurdon, 2006). We then have the iconic example of “Dolly” the sheep, which rep-
resented the first cloned mammal; more precisely, in July 1996, it was a sheep of the
Finn Dorsert breed, with many previous failed attempts (a rarity in a pool of 278
attempts in total 1/277) (Campbell et al., 1996). Other examples of artificial cloning
in vertebrates exist in monkeys of the genus Macaca (Meng et al., 1997; Liu et al.,
2018), domestic cats (Shin et al., 2002; Gómez et al., 2008), and different species of
goats, sheep, and cattle (to improve their productivity) (Smith et al., 2000; Kühhölzer
et al., 2001; De Sousa et al., 2002). The artificial cloning of equines also has a tre-
mendous economic impact since these animals are used for sports such as horse-
back riding and polo.
6.3 E-R Changes Due to Human Activity on Nature 301

There are many advantages to be gained from artificial cloning, such as the clon-
ing of endangered animal species, animals with important livestock characteristics
(e.g., more productive cows), or genetic manipulation to produce transgenic animals
that produce substances used in the pharmacological and sanitary fields. However,
despite the advantages of artificial cloning, there are also ethical objections. The
main ones refer to the fact that it could endanger the biodiversity of the animal
world and the ecological balance itself since it could lead to a decrease in the genetic
variability of species, with irreversible consequences for the ecosystem (Tsunoda &
Kato, 2002; Wells, 2005). In addition, many cloned embryos die after implantation
(Rideout III et al., 2001; Hochedlinger & Jaenisch, 2002), and if they survive, they
show more significant than average body size (Hill et al., 2000; Humpherys et al.,
2001; Rideout III et al., 2001), obesity (Tamashiro et al., 2003), and defects in the
kidneys, heart, liver, lungs, and brain (Cibelli et al., 2002). As already mentioned,
the cloning of the famous Dolly sheep (Campbell et al., 1996) resulted in an appar-
ently healthy individual. However, one of the most significant concerns raised was
that Dolly seemed to age at a faster rate compared to a typical sheep. Additionally,
the cloning process needed a total of 277 unsuccessful embryo attempts before
achieving a successful single birth.
Furthermore, artificial cloning has triggered numerous discussions as the poten-
tial for its future application in humans became evident. Ian Wilmut, the leader of
the team that created Dolly, suggested that this scientific advance could serve as a
foundation for combating diseases, marking a potential starting point in the pursuit
of disease eradication. As previously mentioned, therapeutic cloning offers the
potential for creating tissues or organs that can be used for transplantation, present-
ing an efficient alternative for treating specific pathologies. One significant advan-
tage of this technique is the avoidance of immunological rejection (Pardo, 1997;
Singec et al., 2007; Brown, 2009). We will return to this subject in Chap. 8 of this
book. The researcher also highlighted the usefulness of dealing with infertility prob-
lems (e.g., through reproductive cloning, which is the most questioned), something
that was a rarity, an impossibility, at the time and is now a feasible option.
Undoubtedly, the prospects for nuclear transfer involving the artificial cloning pro-
cess are manifold, and the potential is yet to be exploited (Colman & Kind, 2000;
Dinnyes & Szmolenszky, 2005).
In this context, the possibility of cloning human beings has given rise to an
intense ethical and political debate on handling reproductive cloning. It is argued
that cloned individuals will not benefit from possessing a unique and unrepeatable
identity (Bellver, 2002). Legislation varies widely among countries and tends to
distinguish embryo cloning for therapeutic purposes from reproductive cloning,
which aims to create complete human beings. The latter is legally prohibited in
many countries. The Catholic Church has also spoken out against human artificial
cloning techniques, arguing that a few individuals would appropriate the right to
create other individuals by manipulating their biological identity (Nabavizadeh
et al., 2016). In recent years, a misconception about artificial cloning has been gain-
ing popularity, fueled by the media and cinema. This misconception suggests that a
302 6 Focusing on Dynamics: When an Exception Becomes a Rule

clone is an exact replica of another individual. However, clones defined in such a

way do not exist, as an individual’s phenotype is influenced not only by their geno-
type but also by epigenetic and developmental mechanisms involving other factors.
Consequently, much of the societal rejection of artificial cloning lacks a solid fun-
damental basis (Kahn, 1997; Shapiro, 1997; Gracía, 1999).
From all of the above and within the framework of our book, it is clear that artificial
cloning was a total “rarity” in its beginnings, something even unthinkable but which
has been progressively advancing toward the transition from exception to rule. Are we
in an “intermediate zone” from rarity to the pattern? In reality, it will continue to be
considered a rarity or a pattern depending on what it is compared against. Generally,
seeing artificial cloning as a rarity is already quite outdated. The applications of genet-
ics in various fields, as already mentioned, invite us once again to reflect on the fact
that everything rare can become a pattern or at least an “intermediate” but essential
option and that it has both beneficial and harmful consequences that still need to be
evaluated in depth. In this transition, it is expected that the techniques will improve
over time and that the success rate will be increasingly higher, allowing artificial clon-
ing processes to become more frequent and safer. In conclusion, artificial cloning is a
highly illustrative case of the change from exception to rule by human action, and
where advances in science and technology clearly show us that reality will surpass (or
has already surpassed?) what seemed pure fiction until a couple of years ago.

6.3.4.3 Synthetic Biology: On the Way to Becoming Something Common?

Connected to artificial selection and cloning, we can also incorporate the field of
synthetic biology into the framework of artificial exception-to-rule dynamism.
Synthetic biology is defined as the application of science, technology, and engineer-
ing to the chemical synthesis of biological components and the design and use of
those synthetic components as interchangeable parts to produce new organisms
designed to perform specific functions (O’Malley et al., 2008; El Karoui et al.,
2019). As a rule, synthetic biology uses artificially constructed parts such as amino
acids, ribosomes, synthetic DNA sequences, artificial cells, or biological systems
that are entirely alternative to those found in nature (Arkin, 2008; Cameron et al.,
2014). Thus, by adding or deleting specific genes, synthetic biology produces genet-
ically modified organisms (Keasling, 2007; O’Malley et al., 2008; Cameron et al.,
2014). The basis of synthetic biology are biobricks, synthetic DNA fragments that
code for a biological characteristic and can be combined to form complex circuits.
Biobricks form the basic standard and modular unit that performs a simple function
and allows a cell’s behavior to be modified (Endy et al., 2010; de Lorenzo &
Schmidt, 2017). In this context, the focus is on creating, modifying, or evolving
biological systems with the purpose of controlling and utilizing them for direct
biotechnological applications to meet human needs (Endy, 2005; Ruiz Mirazo &
Moreno Bergareche, 2012).
6.3 E-R Changes Due to Human Activity on Nature 303

Fig. 6.4 Different

approaches from molecular
a
biology (a) and synthetic
biology (b) (Modified from
Lorenzo, 2014)

If we pause for a moment, we see that comparing synthetic and traditional biol-
ogy may be interesting. As we said in Chap. 1 (Sect. 1.2.1), traditional biology
(here, we will call it traditional to differentiate it without confusion from synthetic
biology) has three fundamental laws, laws that undoubtedly must be fulfilled and
that do not accept exceptions. These are the laws of thermodynamics (laws of phys-
ics and chemistry), systems defined by membranes, and living beings subject to a
constant process of biological evolution. In this sense, although synthetic biology is
a discipline that does not focus on the study of living beings but, as we have already
said, has as its objective the study of systems that do not exist in nature, we can find
similarities and differences between them. Thus, synthetic biology transcends
manipulation and brings to the table some of the laws of traditional biology since
processes of reproduction and evolution are also involved in biological systems.
However, this evolution may take different paths from those that nature would take.
Thus, a distinguishing feature of synthetic biology from traditional biology is its
ability to alter the basic organizational structure and processes inherent to life (Ruiz
Mirazo & Moreno Bergareche, 2012).
From a synthetic biology perspective, two main aspects come into play. The first
aspect involves design, which is accomplished through layers of increasing com-
plexity, encompassing the construction of parts, devices, modules, and systems
(Endy, 2005; de Lorenzo & Schmidt, 2017). The second aspect is the flow of infor-
mation where one of the principal dogmas of molecular biology, in which informa-
tion flows from DNA to RNA, proteins, and then different specific functions, is now
replaced by the compositional and quantitative principle of synthetic biology in
which biological parts give rise to devices and these to modules and systems
(Fig. 6.4a, b) (de Lorenzo, 2014; de Lorenzo & Schmidt, 2017; de Lorenzo, 2020).
In synthetic biology, a fundamental premise is to standardize biological compo-
nents in a manner that separates them from their natural context (de Lorenzo, 2020).
The behavior of these components becomes a crucial requirement for engineering
new devices, regardless of the environment in which they operate. This is due to the
intrinsic ability of biological functions to evolve together as a whole and thus behave
in a highly context-dependent manner (de Lorenzo & Danchin, 2008; de Lorenzo,
304 6 Focusing on Dynamics: When an Exception Becomes a Rule

2020). Furthermore, by way of rules, synthetic biological systems must meet par-
ticular characteristics to be considered as such, for example: (a) be computationally
predictable, (b) measurable, (c) controllable, and (d) transformable (add and regu-
late previous functions) (Lee et al., 2013; Li et al., 2015; Muñoz-Miranda et al.,
2019). Additionally, three stages are proposed for the construction of a synthetic
biological system: (1) decoding and analysis of the genomes of biological systems,
(2) synthesis of the parts that make up the genome and their assembly, and (3) the
use of genome editing tools such as CRISPR–Cas9, which has been key to synthetic
biology (Lee et al., 2013; Doudna & Charpentier, 2014). Other techniques used by
synthetic biology include genetic code expansion, minimal genome, sequence
assembly, and synthetic messenger RNA, among others (Lammoglia et al., 2016;
Adli, 2018; Charlesworth et al., 2019).
The origin of this discipline dates back to the 1970s. Throughout its history,
synthetic biology has gone through three stages. Therefore, its character of total
rarity can be appreciated in its beginnings and then gradually assimilated as an
increasingly predominant field. The first stage was the era of genetic engineering or
biotechnology, which modified the genome of microorganisms (for example, the
genome of Escherichia coli was altered to produce insulin). The second was the
elaboration and development of synthetic genomics associated with producing
drugs, biofuels, and genetically modified foods. Moreover, the third phase, which
we are currently in, aims to achieve the complete synthesis of genomes (Alonso,
2013; Garro, 2016). In 2010, Venter and collaborators developed a new bacterium
to self-replicate. This was the first time a cell’s genetic material was replaced
entirely by synthetic genes. This synthetic genome dictated the instructions for the
bacterial cell’s activity, growth, and division. With this new field of research, two
different implementation strategies are proposed. From a more extreme perspective,
synthetic biology aims to control and direct life, redesigning it without further con-
templation (Endy, 2005; Endy et al., 2010). On the other hand, a more subtle imple-
mentation is proposed, taking advantage in some way of the properties that we
recognize as inherent to living beings (Chen et al., 2004; Mansy et al., 2008).
We now focus on the applications that synthetic biology has or may have in the
not-so-distant future. In that case, human society demands many products and
resources to satisfy needs. These are constantly increasing due to the growing
human population. It is then that synthetic biology could have a prominent role
(Serrano, 2007; Muñoz-Miranda et al., 2019).

Some Fields where Synthetic Biology Could Become Very Common

Let us start by listing the fields and areas where synthetic biology can have signifi-
cant participation and stop being a mere curiosity, a rarity. Medicine will be one
of the fields that will benefit the most from advances in synthetic biology, where
different projects are being developed in numerous areas, and even others are
already being implemented. For example, (1) creating artificial cells called CARs
(CAR T cells). Such cells can be detected through biosynthetic sensors, activate
6.3 E-R Changes Due to Human Activity on Nature 305

or inhibit themselves, and attack cancer cells without attacking healthy cells and
thus decrease, at least in part, the adverse effects that current techniques have on
patients (June et al., 2018; Chandran & Klebanoff, 2019; Ventura González et al.,
2020). (2) Tissue repair is based on the design of molecular systems that can rec-
ognize tissue damage. (3) Cellular reprogramming, where stem cells are altered to
have new characteristics. This therapy could significantly impact the immune sys-
tem (Satoshi et al., 2018; El Karoui et al., 2019). (4) 3D bioprinting of organs and
tissues. This method will address the significant lack of organ donors and better
understand certain diseases. Tests and prototypes of different organs, such as
heart, kidney, liver, corneas (to prevent blindness), and ovaries (against infertil-
ity), among others, have already begun (Murphy & Atala, 2014; Zhang & Zhang,
2015; Mandrycky et al., 2016). Amazingly, researchers in Germany have suc-
ceeded in creating transparent organs, making them possible to study. The
SHANEL technique, described in the journal Cell, makes organs transparent and
makes it possible to identify the different cell types to map them within a 3D rep-
resentation of the organ (Zhao et al., 2020). Technology is significant in studying
diseases since it allows a better understanding of their anatomy. (5) In addition,
optimizing the production of antibodies or vaccines, to be able to reduce the cost
and increase the speed of production, and give greater ease of application and
distribution. (6) Genetic engineering of pigs to be resistant to viruses and have
immune profiles similar to humans to allow the development of xenotransplanta-
tion (transplantation of cells, tissues or organs from one species to another, it is
sought that the species are close to avoid rejection) and thus cover the significant
lack of organs for transplantation (Burkard et al., 2018). (7) Synthetic constructs
can also be designed to limit the spread of infections by attacking the vectors of
certain viruses as in the case of mosquitoes (Ruder et al., 2011).
Another field that could benefit significantly from synthetic biology is drug pro-
duction, where it will be possible to develop specific drugs. In this way, it will no
longer be a rarity, an exception, for drugs to be tailored to each patient’s specific,
finely personalized needs (see also Chap. 8). For example, synthetic antimalarial
drugs and malaria vaccines are under development (Vennerstrom et al., 2004;
Keasling, 2007). The food industry is another field where great benefits could be
obtained by implementing synthetic biology. This is a field in which an increasing
number of innovations and methods are being sought through which the processes
of obtaining different foods can be optimized, both in quantity and quality (Tyagi
et al., 2014; Jullesson et al., 2015). On the other hand, synthetic biology offers the
opportunity to create responsive materials that could be particularly useful for
improving building materials (Le Feuvre & Scrutton, 2018).
Finally, bioremediation uses bacteria and fungi to remove toxic or noxious
compounds from the environment. For example, molecular techniques targeting
specific genes involved in key metabolic processes have been employed to study
methanotrophs, which are microorganisms crucial in reducing methane emissions
(a greenhouse-­effect gas) from soil and sediment (Strong et al., 2015). These
approaches have successfully revealed novel methanotrophs capable of actively
degrading methane under environmental conditions. Additionally, methanotrophs
306 6 Focusing on Dynamics: When an Exception Becomes a Rule

possess the ability to cometabolize trichloroethylene (TCE), a common ground-

water contaminant (Guo et al., 2001). Methane injection is often used to stimulate
the TCE-degrading activity of indigenous methanotrophs in TCE
bioremediation.
In other studies, in marine petroleum degradation, molecular ecological
approaches have been utilized to study bacterial populations in petroleum-­
contaminated marine environments (Shi et al., 2019). Research has demon-
strated that specific bacterial groups, such as those associated with
α-Proteobacteria and γ-Proteobacteria, are frequently present in oil-­contaminated
marine environments and likely play a significant role in the bioremediation of
spilled oil (Chang et al., 2000). Moreover, studies have highlighted the acceler-
ated growth of bacterial populations belonging to the genus Alcanivorax when
seawater is supplemented with petroleum and inorganic fertilizers. These find-
ings suggest that certain bacterial populations hold potential for effective biore-
mediation of oil spills in marine environments. Indeed, numerous relevant
examples (Watanabe, 2001; He et al., 2016) highlight the significance of these
microorganisms, which are expected to play a crucial role in the biological bio-
remediation of our planet.

Synthetic Biodiversity Conservation

Despite decades of conservation effort, current indicators show that it has not
been possible to reduce the rate of biodiversity loss (Butchart et al., 2010; Tittensor
et al., 2014; Corlett, 2017; Piaggio et al., 2017), even with the increase in terres-
trial and marine protected areas (Butchart et al., 2010; Butchart et al., 2015).
Furthermore, several factors contribute to this decline: the negative impact of
invasive species spreading deleterious genes within their populations (Webber
et al., 2015; Faber et al., 2021), the prevalence of infectious diseases, the effects
of climate change, and pollution (Redford et al., 2021; Hoegh-Guldberg et al.,
2008), all collectively contributing to this troubling decrease. As a result, it is
becoming increasingly apparent—an idea that was once inconceivable—that the
field of conservation requires close collaboration between conservation biologists
and synthetic biologists. This joint effort is essential to apply new techniques
aimed at preventing biodiversity decline (Piaggio et al., 2017; Redford et al.,
2013; Johnson et al., 2016). On another note, certain aspects related to reintroduc-
ing nearly extinct species (Seddon et al., 2014; Keefer, 2015; Saragusty et al.,
2016) and utilizing gene editing to enhance resistance against diseases and the
effects of climate change, such as higher temperatures or droughts, hold potential
for safeguarding endangered plant and animal species. The implementation of
synthetic biology techniques (Hoegh-Guldberg et al., 2008; Corlett, 2017) could
enable these advancements to become more prevalent in the near future, possibly
becoming standard practices.
6.4 E-R Changes Due to Modifications in Scientific Interpretations 307

Ethical Aspects

Because of the relevance of the multiple elements mentioned above that make up syn-
thetic biology, it is important to highlight other disciplines that involve ethical, legal,
philosophical, and economic aspects (Sandler, 2020). Synthetic biology is the subject of
great debate worldwide due to the impact of its different applications. Its principles are
too challenging for our conception of what is or is not the norm. Synthetic biology is an
example of dual-use technology that promises numerous beneficial applications but can
also generate significant detriments (El Karoui et al., 2019). Therefore, it is perceived
both positively and negatively in society, which is naturally expected when faced with
something unknown, and these new techniques being developed are no exception. The
concepts of nature, life, and biodiversity can be significantly affected by genetic modifi-
cation of individuals and the exploitation of genetic resources. Without ensuring fair
sharing of benefits, this could exacerbate inequality in resource access, among other
potential consequences. However, it is undeniable that genetic modification holds great
potential, particularly in the field of medicine, where it may encounter less resistance
(Sha et al., 2017; Muñoz-­Miranda et al., 2019).
In this sense, there is an exponential annual increase in projects and patents
linked to synthetic biology. When observed by area of application, the primary pat-
ents are for the medical, energy, and industrial sectors (Van Doren et al., 2013;
Carlson, 2016). The countries that are leading patent applicants are the United
States and Japan. Synthetic biology is a tool with high expectations and socioeco-
nomic potential. Its field of action will likely grow exponentially in the next decade
based on the new developments, patents, and industries being created and developed
(Muñoz-Miranda et al., 2019).
In conclusion, synthetic biology has evolved into an essentially interdisciplinary
science, which already has its principles and guidelines, under which it studies the
interactions of multiple components, and which promises to be of great help in various
fields where the main objective is to increase or improve human needs (Liu et al.,
2013). Although for the moment, humanity still sees synthetic biology as a rarity or
curiosity compared to traditional biology, it is unquestionable that it is advancing at an
incredible speed and that it is progressively being used more frequently in various
fields, where the application of its innovative techniques can provide more significant
benefits. It is not venturesome to foresee then that, on a par with traditional biology (or
perhaps above it in some cases?), synthetic biology will become something regular,
even indispensable, in our daily lives. All the applications we have mentioned were
unthinkable or barely dreamed in the past. They were, in any case, rarities for tradi-
tional biology but also for synthetic biology itself in its beginnings. However, we have
observed that synthetic biology holds immense potential for change, and the term
“rare or exceptional” no longer carries the same connotation as it does in traditional
biology. In other words, because of its dynamism, almost anything seems possible for
synthetic biology (if it cannot/is not now, it can/will be sooner or later). Definitely,
weirdness as a synonym for “watertight” does not seem to be in their lexicon.
308 6 Focusing on Dynamics: When an Exception Becomes a Rule

6.4 E-R Changes Due to Modifications

in Scientific Interpretations

The history of science is an essential field where changes from exception to rule
have continuously occurred and continue to do so. That is, how our perceptions of
the surrounding world have been changing according to changes in the knowledge
of biodiversity and technological advances applied to research. Our vision of the
biological sciences is dynamic, which is the basis for permanently modifying what
we consider a rarity or a pattern. Depending on the area of biology, what we now
consider a rule, the typical pattern differs from what was considered a hundred years
ago or even just a couple of years ago. Technological advances and the models of
organisms used, new statistical and analytical models or newly acquired data can
generate a bias in the observations and results, and above all, generalizations must
be cautious.

6.4.1 Key Factors Associated with Change

These changes in the history of biology respond to different factors that generally
work in combination. We could highlight the following:

6.4.1.1 Scientific and Sociocultural School Biases

Scientific trends have always been closely linked to the prevailing sociocultural
context. Perhaps the most recognized case is how the social context and the
nineteenth-­century market and competition theories from Malthus served as inspira-
tion for the concepts of competition and struggle for survival in Darwin’s Theory of
Natural Selection (Malthus, 1969; Herbert, 1971; Bowler, 1976). Among other
aspects, in this context, sociocultural conditioning factors likely hindered the con-
sideration of learning capacity and the presence of intelligence and emotions in
“lower animals.” Moreover, it has been much more challenging to consider plants
beyond their decorative or complementary roles in an ecosystem. Instead of seeing
them merely as simple primary producers, a more comprehensive and enriched per-
spective is needed. Additionally, the female role in sexual selection processes and
mechanisms was accepted only a couple of decades ago (Smith, 1991; Andersson &
Iwasa, 1996; Jennions & Kokko, 2010; Hosken & House, 2011; Ah-king, 2023). In
short, a mixture of anthropocentrism and sociocultural bias has prevailed. It has
prevented us from admitting that living beings exhibit characteristics previously
limited to the human species and, even more, from relegating the female role as an
evolutionary engine.
Moreover, science has tended to be reductionist in some arguments. For exam-
ple, there has been a predominant tendency toward a unidirectional vision of
6.4 E-R Changes Due to Modifications in Scientific Interpretations 309

phenomena as a linear cause–effect when many processes can feed back and mul-
tiple variables and factors can participate. We have an example of how epigenetics
modified the unidirectional view of the mechanism of genome functioning (see
below). Another case is the discovery of “flexibility” at the hormonal level, which is
connected with flexibility at the level of animal behavior and, thus, the ability to be
adaptable to new environments. In other words, according to Taff and Vitousek’s
(2016) review, flexibility at the endocrine level in a world that is dynamic. Thus,
such a unidirectional view of nature becomes obsolete.

6.4.1.2 Knowledge of Diversity and Evolutionary Framework

Within the context of changes due to modifications in scientific visions or percep-

tions, the knowledge of biodiversity and its understanding within an evolutionary
framework has undoubtedly played a preponderant role. The discovery over the
centuries of organisms, the understanding of how they function, and the existence of
an evolutionary theory to unite them were crucial for changes in what was consid-
ered as rules at the time. The iconic case of considering some invertebrates, such as
Porifera and cnidarians, as plants in the early days of biological sciences, particu-
larly during the Aristotelian era, can be attributed to a lack of scientific knowledge
at that time (Ruppert & Barnes, 1996; Bavestrello & Sarà, 2009). The prevailing
“rule” defining “being an animal” was movement, leading to the misconception that
organisms with somewhat greenish colors and fixed to the substrate could only be
plants. Furthermore, it is worth noting that before the theory of natural and sexual
selection emerged, understanding apparent aspects such as the sexual dimorphism
of traits, as well as many morphophysiological adaptations of organisms to their
environment, was not possible. Prior to the advent of Darwin’s ideas, in many cases
when the sexes were highly dimorphic due to differential pressures of sexual selec-
tion, scientists proceeded, as we saw previously, to classify them as two distinct
species (Kelley, 1988; Delph, 1999; Mori et al., 2017). During those periods in the
history of biology, a significant mixture of scientific (or “proto-scientific”) interpre-
tations with obscurantism and religious interpretations played a crucial role, hinder-
ing scientific progress (Barbour, 1990; Evans & Evans, 2008; Rowbury, 2009).

6.4.1.3 Related to Current Equipment and Methodologies

Few data, insufficient technology, and a strong influence of a paradigm may lead to
the omission of elements that could indicate that observed patterns do not represent
rare phenomena. These factors also apply to the inverse situation (shift “from excep-
tion to rule”). Indeed, before the invention of key instruments that significantly
advanced scientific knowledge and underwent further improvements, such as the
telescope (from the initial eyepiece to the current sophisticated versions) and the
microscope (starting from optical and then advancing to electronic ones), what was
once considered the norm or standard quickly gave way to what could be perceived
310 6 Focusing on Dynamics: When an Exception Becomes a Rule

as an exception in its early stages. From the change in the view of the universe, our
solar system in particular, to the understanding of microscopic life and its compo-
nents, everything implied, explicitly or implicitly, constant changes in what was or
was not “the rare vs. the common.” In this context, there are also improvements in
histochemical techniques in biochemistry, including DNA and RNA in particular.
We also have an improvement in behavioral filming techniques and techniques for
ecological and climatic studies. Undoubtedly, behind every technology, no matter
how small it may seem, there was a part of the history of biological sciences linked
to its progress. Mario Bunge’s phrase summarizes this scenario very well: “Whereas
science elicits changes in order to know, technology knows in order to elicit changes”
(Bunge, 1979). As far as our book is concerned, we do not intend to bombard you
with an exhaustive analysis of all the cases where this occurred; we leave that for a
treatise on the history of science from its origins. Within this context, it is essential
to emphasize recent examples of modifications. This serves as a reminder that cur-
rent scientific interpretations will inevitably undergo changes in many cases. Being
aware of these shifts helps us realize that our present understanding may evolve
over time.

6.4.2 Some Case Histories of E - R Change by Scientific Vision

6.4.2.1 Learning and Animal Personality

Among the various topics where our interpretations have changed drastically in
recent years, we can mention the field of study of animal learning and personality,
both in general and, more specifically, concerning groups that were underestimated
in the past, such as invertebrates. Let us first analyze what refers to learning, review-
ing some concepts we will use later in the examples.

Animal Learning

Today, we know that the ability to learn is not a process exclusive to humans, and at
this point, a paradigm shift occurred, which we will refer to throughout this section.
Learning itself is an adaptive process. It is acquired through subtle and incremental
changes (Moreno, 1994). Learning allows animals to adjust their behaviors accord-
ing to the changes they detect in nature, a clear example being flight response in the
face of the sudden appearance of a predator. In this sense, the learning of individuals
must be plastic. By this, we mean that it must allow individuals to modify and adapt
their behaviors and skills to changing conditions, i.e., the original learning must be
adapted to the new conditions to which the individuals are exposed. The types of
learning of a species can range from very elementary to very complex processes
(Aguado-Aguilar, 2001). This variation in the complexity of learning processes will
depend to a great extent on the development of the nervous system of organisms,
6.4 E-R Changes Due to Modifications in Scientific Interpretations 311

and here, it was essential to have a better knowledge of the existing biodiversity
since it allowed us to understand the variation in the development and complexity of
the nervous system on an evolutionary scale.
Learning has been classified into nonassociative and associative. Nonassociative
learning is considered the simplest and refers to changes in the response of individu-
als to repeated exposure to the same stimulus (Perry et al., 2013). Nonassociative
learning comprises habituation and sensitization. Habituation involves a decrease in
response to repeated stimuli that are not associated with a reward, while sensitiza-
tion involves an increase in response to repeated stimuli (Moreno, 1994; Perry
et al., 2013).
On the other hand, in associative learning, the individual learns that the response
to a stimulus is associated with a given event (Perry et al., 2013). Here, it is critical
to highlight the influential contribution of Ivan Pavlov through what was called clas-
sical conditioning (Pavlov, 1927; Perry et al., 2013). Pavlov was a great revolution-
ary in formulating the theory of the conditioned reflex, or classical conditioning, a
significant step in understanding animal learning. In his experiments, he discovered
that dogs’ salivary and gastric secretions could be stimulated not only by food but
also by images and sounds regularly presented to them before feeding as a result of
associative learning (Castro & Wasserman, 2010). Another researcher who brought
about a change in our conception of the learning capacity of animals was Edward
Thorndike. He recorded the time it took for an animal to escape from a box and used
dogs and cats as experimental models. Thorndike found that the time it took the
animals to get out of the box decreased as a function of the repeated times they were
subjected to this experience (Castro & Wasserman, 2010; Dorey, 2020).
Based on these experiments, the Law of Effect was developed, where if a positive
outcome follows a behavior, then it is more likely to occur; however, if a negative
response follows a behavior, then it is less likely to occur again (Castro & Wasserman,
2010; Dorey, 2020). To be sure, discoveries of this type in the sociocultural context
of the time were revolutionary since it was rare to demonstrate with clear evidence
that animals could learn and respond to certain stimuli for their benefit. A central
point to highlight is that when in the past, reference was made to learning processes,
it was common to think only of humans and animals such as rats (Santín et al., 2000;
Vicens et al., 2003; Honey et al., 2014), monkeys (Waelti et al., 2001), and dogs
(Dorey, 2020), where learning processes are fundamental for behaviors associated,
for example, with foraging, reproductive behaviors, offspring care or escape
(Kessels et al., 2001; Vicens et al., 2003). However, we did not even consider the
idea that animals, wrongly called “inferior,” could learn. Here, a paradigm shift
occurred, accepting that animals with a less developed nervous system could
also learn.
The implementation of new technologies was significant in this paradigm shift.
Until not so long ago, descriptions of the behavior of individuals, associated with
learning as with many other processes, were qualitative descriptions, in many cases
with great detail, by the way. However, implementing new technologies and new
forms of analysis allowed the study of behaviors to be a quantitative process, i.e., in
a much more “strict” way. Regarding new technologies for behavior evaluation, the
312 6 Focusing on Dynamics: When an Exception Becomes a Rule

use of cameras and high-speed video cameras has proven valuable. They enable us
to observe behaviors in slow motion, facilitating the detection of actions that occur
at high speeds, which are not easily detectable by the naked eye (Dell et al., 2014;
Egnor & Branson, 2016); development of computerized programs for the analysis
of behaviors, which allow us to detail not only which behaviors individuals show in
a given situation but also their frequency, duration, chronology with respect to other
behaviors, making diagrams of relationship between behaviors, among others
(Kyzar et al., 2012; Jones et al., 2016); technologies for bioacoustic studies, such as
the use of microphones to analyze the behaviors of certain species remotely
(Liedvogel et al., 2013); microclimatic sensors to estimate temperature and humid-
ity; the use of radiofrequency techniques to monitor certain species such as pollina-
tors (Barlow & O’Neill, 2020); and simple or very sophisticated statistical analyses
depending on the need for the data obtained. These are just a few examples of the
new technologies that have been implemented in recent years and have greatly ben-
efited countless investigations, making it possible to change our interpretations and
thus consider that numerous processes, such as learning and personality in inverte-
brates, are no longer rarities but on the contrary processes present in numerous
species.
We will now present examples to illustrate that species of “lower” animals are no
longer only exceptions where some form of learning has been demonstrated to exist.
Indeed, both associative and nonassociative learning have been demonstrated in
many invertebrates (Perry et al., 2013). Although they have simpler nervous systems
than vertebrates, they possess a great variety in complexity, ranging from simple
nervous networks to more complex cephalized systems (Giurfa, 2013; Perry et al.,
2013). For several years, specific invertebrate models, with insects historically
being prominent, have become crucial for studying learning. These models offer
easier experimental conditions, making them valuable in research (Giurfa & Sandoz,
2012). The great use of insect species in studies on learning and memory is based
on linking associative learning processes to specific neural circuits (Giurfa, 2015).
In the insect world, K. Takeda pioneered the study of learning ability, using the
common honeybee, Apis mellifera, as a model. He developed a specific guideline
called the olfactory conditioning protocol for the proboscis extension response
(PER) (Takeda, 1961; Bitterman et al., 1983). With this protocol, he proposed evalu-
ating learning and memory in studying olfactory discrimination at different levels of
analysis ranging from molecular to behavioral (Takeda, 1961; Menzel, 1999). Thus,
the foundations were laid for what would later become one of the most widely used
tools for studying learning and memory in invertebrates (Bitterman et al., 1983;
Giurfa & Sandoz, 2012). The original protocol proposed that the bees were first
given an odor stimulus in the conditioning tests. After a few seconds, the antennae
were allowed to touch a sugar solution, which caused the proboscis to extend, and
the bee could lick the solution. This protocol was intended to demonstrate that bees
learned to associate the olfactory stimulus with feeding (Takeda, 1961; Bitterman
et al., 1983; Menzel, 1999).
Most behavioral biologists have historically underestimated the learning ability
of arthropods, except for a few cases (e.g., Thorpe, 1943; Monteith, 1963). However,
6.4 E-R Changes Due to Modifications in Scientific Interpretations 313

several studies have shown that crustaceans, spiders, and insects can modify their
behavior based on previous experiences (e.g., Reaka, 1980; Dukas, 1998, 2008).
The influence of experience is not limited to simple tasks but also involves complex
behaviors, such as patterns of elaborate predatory and sexual behavior (e.g., Cronin
et al., 2006; Dukas et al., 2006; Jakob et al., 2011). Species of ants, butterflies, and
spiders have shown learning based on associations between colors and food pres-
ence (Perry et al., 2013). Drosophila melanogaster can be visually conditioned to
modify its flight behavior in a simulator to avoid heat shock (Brembs & Heisenberg,
2000; Giurfa & Sandoz, 2012; Perry et al., 2013).
The common honeybee was also used as a model for the study of classical con-
ditioning (Hammer, 1997; Menzel, 2001; Giurfa, 2007), whereas already men-
tioned, proboscis extension behavior is a function of olfactory conditioning
(Bitterman et al., 1983; Giurfa & Sandoz, 2012). There are also analyses, with a
focus on associative learning, to determine how bees learn different floral odors
(Wright & Schiestl, 2009; Reinhard et al., 2010; Giurfa & Sandoz, 2012) and learn-
ing behaviors where bees show an association between thermal stimuli and feeding
(Menzel et al., 2001; Hammer et al., 2009).
In addition, the classical conditioning process of the proboscis extension
response was also applied to blowfly species, flies, and bumblebees (McGuire,
1984; Fresquet, 1999; Laloi et al., 1999). Another example is crayfish; when
threatened, they produce flexions of the abdomen to move away from danger, and
it can be said that they are under a habituation-type learning process since the
probability of escape decreases with repeated stimulation (Krasne & Wine, 1987;
Krasne & Teshiba, 1994).
Learning about invertebrates is not limited to the arthropod world. Perry et al.
(2013) show a wide variety of different types of learning in nonarthropod inverte-
brates and protists. For example, among the primitive organisms where the exis-
tence of learning has been experimentally proven, we can name the amoeba
Physarum polycephalum. They found here that after successive exposures, this spe-
cies of amoeba stops avoiding certain substances it has repeatedly encountered; this
is linked to the habituation type of learning (Pershin et al., 2009). This amoeba also
overcame movement tests associated with changes in temperature and humidity
(Pershin et al., 2009). On the other hand, rotifers, microscopic invertebrates con-
taining only approximately 200 neurons, showed that their contractile capacity
decreases in the face of repeated tactile stimuli over time (Applewhite, 1968).
Ascidian larvae that possess only approximately 100 neurons (Meinertzhagen &
Okamura, 2001) also show forms of nonassociative learning. Larvae modify their
swimming behavior according to repeated light exposures. The behaviors showed
habituation or sensitization depending on the light intensity to which they were
subjected (Perry et al., 2013). Studies in flatworms and cnidarians, groups contain-
ing elementary nervous systems, have also demonstrated the existence of a type of
classical conditioning. For example, flatworms contract the body upon exposure to
light (Thompson & McConnell, 1955), and cnidarians can respond to olfactory and
touch stimuli (Perry et al., 2013). In nematodes, it was shown within a now-famous
model, Caenorhabditis elegans, that it can learn and remember stimuli it encounters
314 6 Focusing on Dynamics: When an Exception Becomes a Rule

around it (Rankin, 2004). It has also been shown that this nematode can learn based
on mechanosensory (Rose & Rankin, 2001) and thermosensory stimuli (Mori, 1999).
One invertebrate group to highlight in learning is the cephalopods, which include
octopuses, cuttlefish, and squid. These specialized mollusks form a fascinating
group in which a significant development of cognitive capacity has been observed,
including processes such as learning and memory (Schnell et al., 2021). Cephalopods
show different forms of learning, mainly associative (Darmaillacq et al., 2004,
2014; Cole & Adamo, 2005). For example, the octopus Octopus cyanea can learn to
associate a neutral stimulus, such as a sound, with a reward, such as obtaining food
(Papini & Bitterman, 1991). The octopus Amphioctopus marginatus surrounds itself
for protection, with coconut shells as a shield, a behavior that individuals are thought
to associate with a reduced risk of predation (Finn et al., 2009). In addition, cepha-
lopods possess spatial learning, such as exploratory learning (Karson et al., 2003;
Jozet-Alves et al., 2008). On the other hand, in cognitive processes linked to mem-
ory, studies show that cephalopods have short- and long-term memory (Jozet-Alves
et al., 2013; Zepeda et al., 2017). Cuttlefish, for example, can remember what they
ate and where they consumed it. These processes allow them to undoubtedly opti-
mize foraging behavior (Jozet-Alves et al., 2013; Schnell et al., 2021). In recent
years, it has been suggested that various evolutionary pressures, such as predation,
foraging, and mating competition, have significantly influenced the development of
cephalopod cognitive processes that facilitate behavioral flexibility (Schnell &
Clayton, 2019; Amodio et al., 2019). Undoubtedly, the most salient and recognized
example is the behavioral flexibility of cephalopods in predation avoidance behav-
iors, where they can change their body coloration in mere seconds. This behavior
has been associated with associative learning based on the individual’s previous
experience (Hough et al., 2016; Schnell et al., 2021).

Animal Personality

Linked to learning processes, we can refer to animal personality (Sih et al., 2004a,
2004b; Schuett et al., 2010), which is currently not considered a pattern, a rule, but
no longer appears as just exceptions in the literature. The concept of personality
refers to the fact that individuals in a population may show differences in behavior
that are maintained over time and in different situations (Réale et al., 2007).
Although psychologists have paid particular attention to the study of personality in
both humans and animals for many years (Wilson, 1994; Gosling, 2001), it is only
recently that animal personality has been included as a topic of study by ecologists
and evolutionary biologists (Sih et al., 2004a, 2004b; Dall et al., 2004). We now
have a large body of evidence that certain personality traits can affect essential pro-
cesses such as dispersal, colonization, and reproduction, among others (Réale et al.,
2007; Dingemanse et al., 2010; Stamps et al., 2012; Keiser et al., 2018). Personality
in animals involves different traits that have been classified into shyness-boldness
(reaction of individuals to nonnew risk situations), exploration (reaction of an indi-
vidual to a new situation), activity (general level of activity of an individual),
6.4 E-R Changes Due to Modifications in Scientific Interpretations 315

sociability (reaction to the presence or absence of conspecifics), and aggressiveness

(agonistic reaction to conspecifics) (Réale et al., 2007).
When we estimate the repetitiveness of a trait, we consider that the environment
is kept constant. This is to avoid any new variable influencing the analysis of the
repetitiveness of the behavior we are evaluating. However, even if we achieve this,
learning processes inherent to each individual, such as habituation or sensitization
of the ones we talked about before, could affect the performance of the individuals
(Réale et al., 2007). This idea that animals can have a determined personality
changes the traditional conception where it was considered that animals could be
plastic and consistently exhibit the optimum of their behaviors according to the dif-
ferent situations to which they were exposed (Sih et al., 2004a). Thus, although an
individual will not show the same behaviors in successive events, intraindividual
variations are expected to be smaller than interindividual variations (Sih et al.,
2004a, 2004b). One hypothesis posits that individuals may show differences in cer-
tain behavioral traits because, for example, they may differ in their physiological
and morphological characteristics (Stamps, 2007). Furthermore, it has been pro-
posed that personality traits are genetically inherited (van Oers & Sinn, 2011).
However, environmental factors, such as temperature and food availability, may
also influence individuals’ personalities. Undoubtedly, this field awaits further study
(Groothuis & Trillmich, 2011; Kralj-Fišer & Schuett, 2014).
We widely accept that humans have different personality traits. For example,
some are shyer than others, some are more active than others, and some are even
more aggressive than others (Sih et al., 2004a, 2004b). As far as animals are con-
cerned, studies of differences in personality traits have also been conducted in a
wide variety of vertebrates, including mammals (Koolhaas et al., 1999; Gosling,
2001), birds (Drent et al., 2003), reptiles (Stapley, 2006), amphibians (Sih et al.,
2003), and fish (Sih et al., 2004a, 2004b). For example, in the bird Parus major,
differences are observed in behavioral traits associated with exploration, where
some individuals are much more active than others, and it has been shown, thanks
to artificial selection (see Sect. 6.3.4.1), that these traits are heritable (Drent et al.,
2003; van Oers et al., 2004). In fish species such as Lepomis gibbosus (Sih et al.,
2004a, 2004b) and Poecilia reticulata (Godin & Dugatkin, 1996), individuals show
differences in personality traits associated with boldness, while others exhibit traits
of shyness.
However, as we have already said, vertebrates are just a sample of animals that
can show traits of a given personality. Even so, at present, we find it difficult to
accept that animals such as invertebrates are also capable of showing differences in
traits associated with personality, possibly because we interpret that their nervous
system, which is much less developed, has a limited capacity. In this sense, the lack
of studies on invertebrate species could be related to the fact that many consider
them to be “mini-robots” that respond similarly to certain stimuli. Therefore, it is
not expected to be a difference in the responses of different individuals (Kralj-Fišer
& Schuett, 2014). These authors reviewed that there is personality at the level of
exploratory activity, aggression, and boldness in numerous species of Arthropoda,
Mollusca, and Cnidaria.
316 6 Focusing on Dynamics: When an Exception Becomes a Rule

Within arthropods, differences in personality traits have been observed, for

example, in insect species such as Aquarius remigis, where some males are consis-
tently more active and aggressive than others. On average, more active males tend
to encounter more females and mate more frequently (Sih et al., 2002; Sih &
Watters, 2005). In fly species such as Drosophila, there are differences in levels of
aggression between individuals (Zwarts et al., 2012; Alekseyenko et al., 2013). In
Apis mellifera, individuals show differences in levels of boldness (Wray et al.,
2011), and the same occurs in Gryllus integer (Niemela et al., 2012).
Within arachnids, spiders have also been found to exhibit personality traits. For
example, females of Agelenopsis aperta showed different levels of aggressiveness
among themselves (Riechert & Hedrick, 1993). In females of Holocnemus pluchei,
there are interindividual differences in stridulation behavior in sexual interactions
(Calbacho-Rosa et al., 2019). Some females stridulate more (possibly associated
with more demanding females), while others stridulate less (perhaps associated
with less demanding females). Males of Argiope radon show consistent differences
in behaviors in sexual interactions that reflect differences in male quality (Wignall
et al., 2014).
On the other hand, within mollusks, consistent differences in behaviors associ-
ated with boldness and activity traits have been shown in the species Euprymna
tasmanica (Sinn & Moltschaniwskyj, 2005; Sinn et al., 2006), and in the species
Octopus rubescens, individuals show different levels of boldness (Mather &
Anderson, 1993). For Cnidaria, we can name the species Actinia equina, where dif-
ferent levels of boldness among individuals have also been observed (Rudin &
Biffa, 2012).
From all mentioned in this section, we can conclude that learning and personality
are not only processes exclusive to humans or higher animals but also to the vast
majority of animals, if not all of them. Perceiving lower animals as organisms with
the capacity to learn and show different personalities has remarkably changed our
perception of what occurs in nature. Here, we again emphasize the importance of
the sociocultural changes that have been developing throughout history, allowing us
to become involved in this study. As we saw, another aspect that brought about
changes in our interpretations was the critical advances in technology, which made
it possible to carry out a large number of analyses and interpretations of processes
that we had previously considered oddities simply because we could not observe
them. Of course, as has been said throughout the book, the fact that an exception
becomes a rule does not imply that it should be generalized to all organisms.
However, as exemplified by the case of the learning ability and differentiated per-
sonality traits demonstrated among invertebrates, it does mean that researchers
should take this new information into account in new experimental designs.

6.4.2.2 Neuronal Plasticity: Regeneration and New Connections

The conventional notion regarding the animal brain, including the human brain, is
that its defining cells, neurons, lack the ability to regenerate, unlike the cells found
in other organs. Advancements in technology and novel approaches have challenged
6.4 E-R Changes Due to Modifications in Scientific Interpretations 317

long-standing beliefs, including the idea that neuronal regeneration is impossible.

Presently, we have evidence to support the existence of neuronal regeneration, and
while it may not be universally the rule for all organisms, it is no longer considered
a mere exception.
First, let us clarify what we mean by the term regeneration. Regeneration, in
biological terms, refers to restoring the structure and function of a damaged part of
the organism (Bely & Nyberg, 2010; Poss, 2010). This regeneration can occur at
different levels, cellular, tissue, organ, or, in the most extreme cases, of some part of
the body (Bely & Nyberg, 2010). Three distinct mechanisms have been identified to
facilitate the process of regeneration: (1) epimorphosis (differentiation of a blas-
tema and then production of new tissue), (2) morphalaxis (transformation of exist-
ing tissues or body parts into new structures), and (3) compensatory growth (tissue
that is not damaged enlarges to compensate for the loss of tissue) (Gilbert, 2003;
Martínez et al., 2006).
Some examples of organisms showing regeneration processes in different tissues
include invertebrates such as planarians, which can regenerate half of their missing
body when cut in half (Reddien & Sánchez Alvarado, 2004; Gilbert, 2003). Hydra,
another invertebrate, has shown the ability to regenerate into complete individuals
when cut into several parts (Gilbert, 2003; Bosch, 2007). Additionally, the worm
Hofstenia miamia can regenerate the missing part of its body after a longitudinal cut
(Gehrke et al., 2019).
Among vertebrates, several examples of regeneration exist across different types
of organisms. For instance, the zebrafish (Danio rerio) is capable of regenerating
fins, as well as certain organs such as the heart and pancreas (Poss et al., 2003). In
the case of amphibians, salamanders are notable for their ability to regenerate their
limbs (Gilbert, 2003). Among reptiles, lizards have the capacity to autotomize their
tails and subsequently regenerate them, and in some turtles, regeneration of at least
some part of the shell has been observed (Alibardi, 2010). Finally, in mammals,
regeneration processes also occur. For example, hair, nails, skin, mucous mem-
branes, liver, and bone can undergo regenerative processes (Belkind-Gerson &
Suárez-Rodríguez, 2004).
Regarding neuronal regeneration, the prevailing dogma until the late 1990s was
that there was no formation of new neurons in adult organisms. Cells of the nervous
system are widely believed to be one of the few, if not the only, cell types incapable
of regeneration (Brain & Walton, 1969; Zupanc, 2008; Gao et al., 2017). However,
this concept has been progressively changing. In a broad sense, we now know that
neuronal regeneration in adult organisms exists and requires several coordinated
processes, such as proliferation and migration of neuronal precursors to sites where
some injury has occurred and the integration of the new cells into already existing
circuits (Kernie & Parent, 2010).
Among invertebrates, neuronal regeneration has been demonstrated in several
groups, for example, in the flatworm Notoplana acticola (Faisst et al., 1980) and
among annelids in the earthworms Lumbricus terrestris and Allolobophora caligi-
nosa (Hulsebosch & Bittner, 1980; Ortega & Olivares-Bañuelos, 2020). Among
arthropods, cricket species have shown regeneration of sensory neurons (Murphey
et al., 1983), and regeneration of motor fibers has been observed in cockroaches
318 6 Focusing on Dynamics: When an Exception Becomes a Rule

(Stern et al., 1997). In Orthoptera, such as Schistocerca gregaria, neuronal regen-

eration has also been demonstrated (Pätschke et al., 2004; Lüdke & Lakes-Harlan,
2008). Echinoderms, including species such as the serpent star Ophioderma longi-
cauda (Dupont & Thorndyke, 2006; Biressi et al., 2010) and the sea cucumber
Holothuria glaberrima (Ortega & Olivares-Bañuelos, 2020), serve as excellent
models for studying neuronal regeneration. In these organisms, there is compelling
evidence of neuronal regeneration following injury, which is associated with the
involvement of various neurotrophic factors.
In vertebrates such as fish, reptiles, and birds, neurogenesis has been shown
to occur in various parts of the brain (Doetsch & Scharff, 2001; Zupanc, 2001;
Kishimoto et al., 2012). In teleost fish, there is a high capacity for neuronal
regeneration after injury, as occurs in Apteronotus leptorhynchus (Zupanc,
2008; Kishimoto et al., 2012). In amphibians, particularly in frog species, such
as Rana pipiens, it has been seen that after a cut of the olfactory nerve, there is
a process of mitosis of basal cells of the olfactory mucosa that then differentiate
into neurons (Graziadei & DeHan, 1973; Zupanc, 2006). Adult reptiles, includ-
ing certain turtles such as Trachemys scripta and lizards such as Podarcis his-
panica, exhibit a remarkable characteristic: their telencephalon generates new
cells almost every day. Subsequently, a significant portion of these newly gener-
ated cells differentiate into neuronal cells, serving as replacements for those that
have been damaged (Font et al., 2001; Zupanc, 2006). Birds present an extraor-
dinary situation, particularly in songbirds, where environmental changes have a
notable impact on neuronal regeneration in adults. In species that reproduce
seasonally, the lengthening of days significantly influences the growth of song
control nuclei. This behavioral change, observed in males, is associated with the
attraction of females (Tramontin & Brenowitz, 2000; Font et al., 2001;
Zupanc, 2006).
In mammals, neurogenesis occurs in two specific areas of the brain: the anterior
part of the subventricular zone (Eriksson et al., 1998; Curtis et al., 2007; Zupanc,
2008; Kishimoto et al., 2012) and the subgranular zone of the dentate gyrus in the
hippocampus (Kempermann, 2002; Zupanc, 2008; Kishimoto et al., 2012). In some
species of mice, and even in humans, some neurotrophic substances, such as reti-
noic acid, have been shown to enhance neuronal regeneration rates in both the cen-
tral nervous system and the peripheral nervous system in vitro (Quinn & De Boni,
1991). However, the mechanisms by which these neurotrophic substances have such
an effect are still unclear. One of the proposed hypotheses is that adult neurogenesis
could be linked to learning (see Sect. 6.4.2.1) and memory processes (Font et al.,
2001). In this sense, this process in vertebrates also involves structural modifica-
tions in the brain (Alvarez-Buylla, 1992; Kolb & Whishaw, 1998). It was also shown
that although neurogenesis occurs throughout life, it decreases with the organism’s
age (Kuhn et al., 1996). Thus far, we have named a few examples to show that neu-
ronal regeneration is widely distributed among various animal species. These criti-
cal advances in our knowledge are undoubtedly due mainly to the development of
novel technologies that are continually advancing in their development.
6.4 E-R Changes Due to Modifications in Scientific Interpretations 319

For example, toward the end of the 1980s, a radiolabeling technique involving
the use of dyes, such as thymidine (3H), which is incorporated into the DNA of
dividing cells and can be detected by autoradiography, began to be used in studies
of neuronal regeneration in adults of fish, reptile, and bird species. Thus, monitoring
this dye made it possible to corroborate neuronal regeneration processes (Font et al.,
2001; Zupanc & Sîrbulescu, 2011; Hulsebosch & Bittner, 1980; Gage & Temple,
2013). It was determined in mammals that a growth factor, IGF-1, and its receptor
appear to be essential in the growth of new axons in mature cells (Dupraz et al.,
2013). The PI3K enzyme activates different signaling pathways within the neuron
that result in axon growth. Other essential advances that allowed changing our inter-
pretations about the existence of neuronal regeneration were the advances in immu-
nohistology techniques together with the use of confocal microscopy, which also
allowed the study of neurogenesis in adult organisms (Gage & Temple, 2013). In
addition, the development of methodologies that allowed the isolation, mainte-
nance, and differentiation of precursor cells of nervous system cells under in vitro
culture conditions (Kilpatrick & Bartlett, 1993; Reynolds & Weiss, 1992; Gage &
Temple, 2013) have also contributed significantly to the increased knowledge on the
subject and consequently to the change of our conceptions in terms of considering
neuronal regeneration as an exception.
Furthermore, the capacity for neuronal regeneration itself merits further discus-
sion, as it is closely connected to the continuous process of forming and refining
neuronal connections throughout an organism’s life. This vital issue for modern
medicine is linked to an old idea that neuronal connections in the brain take place
only in the early stages of development. It is now understood that this is not true.
There is a phenomenon of “neuronal plasticity” that persists throughout life, contra-
dicting the previously mentioned notion of a fixed, nonplastic system with no regen-
erative potential. Moreover, if such a nonplastic system were to exist, it would likely
be limited to certain exceptions. Precisely, it is worth mentioning the theory of neu-
ronal connections (Kandel et al., 2000), which proposes that even when the organ-
ism is an adult, there is a need for permanent contact between a neuron and its
target, which can be another neuron, a muscle fiber, or a gland (García, 2003).
Although this contact is more critical during development than in the adult organ-
ism, the cells of the nervous system need to interact with their targets to carry out
their functions (De la Cruz et al., 1996; García, 2003). Although the adult mamma-
lian nervous system does not have the capacity for the significant reorganization of
its neural pathway connections, this has been observed after neuronal injury and
motor learning (Cotman & Nieto-Sampedro, 1984; Malenka, 1995; Tsukahara, 1981).
Again, the data corroborate that neuronal regeneration and neural connections
are not exceptions. In addition, it is now known that neurons can survive some types
of axon injury and that the axon can reinnervate another target tissue (De la Cruz
et al., 2000; García, 2003). They can also recover their functional capacity, that is,
the capacity to produce synaptic potentials (Font et al., 2001; García, 2003), some-
thing that was not considered possible in the past. In addition, we also know that
axonal regeneration is different between the central and peripheral nervous systems.
This is due to differences in the environment in which axons regenerate. For
320 6 Focusing on Dynamics: When an Exception Becomes a Rule

example, it is believed that myelin in the central nervous system is an inhibitor of

axonal regeneration (Liu et al., 2011; Zou et al., 2013; Pernet & Schwab, 2014).
Among some of the mechanisms, we can highlight calcium waves, where for exam-
ple, in invertebrates such as the nematode Caenorhabditis elegans and the mollusk
Aplysia sp., it has been found that axon regeneration depends on calcium influx
(Ghosh-Roy et al., 2010; Doron-Mandel et al., 2015). Among mammals, in rat spe-
cies, for example, epigenetic modifications have been studied as another mecha-
nism that may influence neuronal growth, as they may affect changes in genes that
are associated with axon growth (VandenBosch & Reh, 2020), and local protein
synthesis mechanisms, based on the ability of axons to synthesize proteins as
mRNA, have been recorded along axons (Font et al., 2001; Zheng et al., 2001).
If we shift our attention to human beings as a study model, the remarkable
advancements in neuroscience, a discipline currently at its peak, have significantly
influenced our interpretations of what we previously considered as exceptions or
rules. As we have already said, studies in neuroscience have discovered that the
brain changes every time we learn something (Kandel et al., 2000; García, 2003).
This occurs due to a process known as neuronal plasticity, which gives the nervous
system the capacity to change its structure and function, ultimately producing
changes in our way of thinking and acting (Carlin & Siekevitz, 1983; García, 2003;
Gruart & Delgado-García, 2004). However, it has also been proposed that a more
appropriate term is neural elasticity since this involves not only changing but also
being able to return to the initial state (García, 2003). Currently, a considerable
body of research in humans is devoted to determining the frequency of neuronal
regeneration in adults and identifying the underlying mechanisms that facilitate this
process. This investigation holds immense significance due to its potential applica-
tion in therapies for patients who have suffered brain injuries or neurodegenerative
diseases. Thus, this regeneration could be responsible for the improvement in many
of them (Belkind-Gerson & Suárez-Rodríguez, 2004; Gao et al., 2017).
Neurotechnology stands out as one of the technological advancements that have
revolutionized our understanding of the mechanisms operating within the nervous
system. Neurotechnology is a developing discipline based on neuroscientific knowl-
edge, including for example, the simulation of neuronal models, the interconnection
of the brain with electronic systems, and sophisticated apparatus for analyzing brain
activity. Neurotechnology, according to its mode of implementation, can be classi-
fied as invasive when it requires surgery for, for example, the placement of transmit-
ters or receptors that capture signals from the brain or nervous system or noninvasive
when it does not require surgery for its placement. Furthermore, new appliances
available today have facilitated substantial progress in our comprehension of the
nervous system, encompassing the phenomenon of neuronal regeneration. Let us
consider that until the nineteenth century, studying the brain was limited to post-
mortem examinations, as the available technology, such as X-rays, only allowed the
visualization of the skull bones. However, a significant breakthrough occurred with
the implementation of advanced technologies such as computed tomography (CT
Scan) and magnetic resonance imaging (MRI), which revolutionized neuroscience
by enabling the acquisition of detailed neuroimages. CT Scan made it possible to
6.4 E-R Changes Due to Modifications in Scientific Interpretations 321

obtain slice images to analyze the object of interest; indeed, Allan McLeod Cormack
and Godfrey Newbold Hounsfield received the Nobel Prize in Physiology for its
development in 1979. For the development of magnetic resonance imaging, in 1978,
an image of the human brain was obtained for the first time. Magnetic resonance
imaging is currently one of the most widely used techniques for neuroimaging since
it is a noninvasive technique thanks to which soft tissues can be seen. The ability to
differentiate between gray matter and white matter within images has opened up
new possibilities for monitoring vascular diseases of the brain, including neurode-
generative processes that lead to dementia and Alzheimer’s disease. This advance-
ment in neuroimaging has significantly enhanced our understanding and diagnosis
of these conditions.
In addition, Parkinson’s disease, a neurodegenerative disorder, causes the loss of
different types of cells in the central and peripheral nervous systems, including
dopaminergic neurons in the midbrain, which produces most of the symptoms in
patients. In this sense, the analysis of the possible replacement of dopamine neurons
has been closely studied for its possible implementation as a therapeutic alternative
(Guardo-Gómez et al., 2020; Tabar & Studer, 2014). Thus, developing and imple-
menting new and innovative techniques for regenerating nervous system tissues
promises to obtain methods for the recovery of motor and sensory function of dam-
aged cells (An et al., 2006; Guardo-Gómez et al., 2020). This is an example of the
great benefits provided by the advancement of science and the possibility of having
access to more excellent knowledge, thanks to which our interpretations about a
certain subject change over time. However, their implementation requires a great
deal of development and fine-tuning to be used “massively” among patients with a
given pathology.
Moreover, while it has long been acknowledged that physical activity enhances
overall health and well-being, emerging evidence indicates that it activates specific
mechanisms that safeguard neurons. These mechanisms have been termed the
“physiological neuroprotection system” (Herrero & Ferradaz, 2011). When the
body starts moving, the brain coordinates a series of mechanisms, such as muscle
movement, increased blood flow, and alterations in breathing and heart rate.
Different nerve centers regulate everything, so physical activity causes several areas
of the brain to be activated (Herrero & Ferradaz, 2011). For all these reasons, there
is now concrete evidence that a sedentary lifestyle is a risk factor for developing
neurodegenerative diseases. All these discoveries have led to significant changes at
the social level. For example, many people have already included physical activity
as part of their daily routines to contribute to a better general state of our organism,
something that was not common before. We will return to this fact in Chap. 8.
In conclusion, our changes in the interpretations regarding neuronal regeneration
and associated topics have been possible thanks to the tremendous technological
advances that have been developed over time, some of which we have named above.
Many neurological analyses or studies of various types are now considered routine,
including those of high complexity, which was unthinkable only a couple of years
ago. Neuronal regeneration, along with the generation of new neuronal connections,
is no longer perceived as a mere curiosity or an exception in the outdated conception
322 6 Focusing on Dynamics: When an Exception Becomes a Rule

of “neurons do not regenerate” (an implicit rule of the past). As research expands to
encompass a diverse range of model species, more studies consistently reveal that
neuronal cells can regenerate in adults. This discovery is progressively shifting the
perception of neuronal regeneration from an exception to a principle, and it is antici-
pated that further investigations will solidify this notion as a widely accepted rule.

6.4.2.3 Communication in Plants

In nature and science, plants are often overlooked and marginalized (Hoekstra,
2000; Jose et al., 2019). Many perceive plants as tedious compared to animals, as
they may seem monotonous, relatively similar, and nonmobile, merely serving as a
source of food for other organisms. This is a vague and reductionist view of what
plants are. Indeed, it appears peculiar to categorize these organisms as almost “inan-
imate” and attribute no greater purpose to them beyond existence, reproduction, and
being preyed upon. It is not easy to believe they do not have a goal and means to
achieve it. Every living organism has one. Therefore, it is not strange to think that
plants can perceive the environment, respond to changes, and transmit information
to other individuals. The inability to perform these tasks would surely make the
group disappear (Gagliano, 2015).
In biology, and in simple terms, communication is often described as a system in
which at least two individuals exchange signals that lead to conditional and revers-
ible changes (Karban, 2015). In this context, the term has been applied mainly to
multicellular animals. Progressively more primitive groups, such as unicellular pro-
tists, were incorporated, and now we also speak of communication in bacteria (king-
dom Bacteria) (Taga & Bassler, 2003; Federle & Bassler, 2003; Greenberg, 2003;
Keller & Surette, 2006; Blackwell & Fuqua, 2011). The understanding of animal
communication has evolved in recent years, especially with advances in the fields of
neuroethology (e.g., Schöneich, 2020; Mariette et al., 2021), behavioral ecology
(Higham & Hebets, 2013), and behavioral genetics (Ferveur, 2005; Robinson &
Huang, 1998), moving on from past debates about instinct versus learning (Thorpe,
1956). However, a significant gap has remained almost constant regarding other
kingdoms, such as fungi and plants.
Undoubtedly, the diversity of plants pervades every ecosystem. The importance
of plant organisms in the diversification of life, together with cyanobacteria, by
providing oxygen through photosynthesis in the ancient environments of Earth has
never been denied (see Sect. 6.2.1.1). In addition, the interdependence of plant–ani-
mal interactions has been recognized and accepted since ancient times. This is most
evident in Darwin’s studies on pollinators and orchids (Micheneau et al., 2009).
Additionally, various ecological aspects, such as seed dispersal, evolutionary stud-
ies of herbivory, and the evolution and ecology of carnivorous plants, have been
subjects of investigation (Abrahamson, 1989). These studies collectively highlight
the profound connections and contributions of plants in shaping the natural world
and understanding the intricate relationships between organisms in diverse
ecosystems.
6.4 E-R Changes Due to Modifications in Scientific Interpretations 323

However, amidst all these conceptual changes, there remains an aspect that has
not received the attention it deserves, or perhaps has been underestimated: the exis-
tence of plant communication. In other words, the real presence of information
transmission between plant individuals, where at least one sender and one receiver
will share information in the form of signals, and these signals generate a response
in the receiver (Karban, 2015), as in animals, there are diverse forms (Gagliano
et al., 2012; Awan et al., 2019). In this context, current researchers broke paradigms,
implicit biases in our view in the past in science, that plants could not communicate.
Advances have been astonishing in the last hundred years. Although much remains
to be explored, today, we can say that plant communication exists and that, rather
than an exception of a particular species or case, it is the rule in plants (Baluška &
Mancuso, 2007, 2009; Karban, 2021).
Certainly, communication is not the sole outcome. Nevertheless, researchers pro-
pose that plants may possess more advanced capabilities beyond perceiving and
responding to their environment. There is a suggestion that plants exhibit electrical
transmission (Bose, 1925; Scott, 1962; Mackie, 1970; Dziubinska, 2003) akin to the
nervous system in animals, along with memory, intelligence (Trewavas, 2003, 2014;
Baluška et al., 2018), and responses to circadian rhythms, similar to our need for
“sleep” (Mancuso & Shabala, 2006; Mondal & Parui, 2013), among other traits
previously associated only with animals. Indeed, all of this falls under the umbrella
of the development of a relatively new field, the field of plant neurobiology (Brenner
et al., 2006). The findings strongly suggest that animals and plants might not be as
fundamentally different as traditionally believed. It appears that they could share
evolutionary convergence, enabling them to interact with the environment and
evolve in response (Trewavas, 2005). Here are some examples, many of them sur-
prising, of communication in plants.

Herbivory, Communication and Reaction in Plants

There is a clear example to illustrate the communication between plants resulting

from a stimulus and the subsequent response of individuals. In the 1980s, there was
a significant drought in South Africa. Kudus (Tragelaphus strepsiceros) are large
antelopes that inhabit this region and feed on various types of grass and tender
shoots throughout the season (Dörgeloh, 2001). During droughts, kudus exhibited a
preference for feeding on leaves from various Acacia species. There were many
reports of healthy animals found dead, and deaths were directly associated with
density (Van der Waal, 2005). In the rumen of dead animals, the concentration of
tannins was too high (Van Hoven, 1984). Tannins are chemical compounds (second-
ary metabolites) produced by plants for defense against herbivory (Hagerman &
Butler, 1981; Hassanpour et al., 2011) and can prevent digestion in the rumen of
ungulates (Van Hoven, 1984). Ungulates can neutralize the tannin content at aver-
age concentrations, but these chemicals can be lethal at significant and prolonged
concentrations. Acacias could quadruple the average concentration of tannins,
resulting in kudu’s death. The trigger for this response appears to be herbivory
324 6 Focusing on Dynamics: When an Exception Becomes a Rule

pressure in fenced areas of Game Ranches. The plants reacted by increasing tannin
levels in their leaves. They “did not want” to be eaten or lose their precious leaves
and responded chemically to overgrazing. Thus, the plants evaluated the environ-
ment and took action on the signal.
It was later found that plants not under high herbivory pressure (e.g., outside of
the ranch boundaries) had the same elevated tannin concentrations. This was no
coincidence. The researchers sought to elucidate whether the plants could give other
individuals an “alarm signal” about the herbivory pressure to which they were being
subjected. The hypothesis was that “there was something in the air.” Therefore, the
air around the Acacia branches was analyzed, and it was found that when the kudu
ate the leaves, the plant emitted a light gas called ethylene, which is used for the
ripening process of stored fruits (see below). This wind-borne gas reached other
leaves, signaling the production of enzymes catalyzing the production of tannins.
Thus, the plant communicates chemically with another plant and warns it of poten-
tial dangers. In turn, the plant that receives the warning responds in advance by
preparing the production of herbivore repellents. This clearly illustrates the ability
of plants to evaluate the environment and respond to changes and pressures, as well
as to warn or alarm other individuals by transmitting information. These communi-
cation concepts were not uncommon in nature; however, scientists only occasion-
ally identified them clearly. This serves as a clear example of exceptions that
eventually become rules, reflecting the evolving perception of science regarding
certain phenomena.
Let us now go deeper and explore the potential for underground communication
among plants. It is crucial to understand how our perception of how plants interact
with each other below the ground has evolved over time. In the past, it was thought
that organisms were independent in a forest and did not communicate through their
roots. Today, it is known, for example, that forests are a continuous network linked
and communicated underground. In this sense, as we have already seen, plants can
communicate via the air with other individuals and with different parts of the same
organism, but we will also see that communication can flow through the soil. Roots
are known to be selective in places with plenty of nutrients and water, but they also
form interspecific relationships with fungi and bacteria. This is known as the rhizo-
sphere (Berendsen et al., 2012). This rhizosphere is a mutualistic relationship where
the plant is provided with nutrients from the soil that would be difficult to obtain,
and in return, the symbionts obtain sugars from the plant. Obviously, and this is no
exception, some organisms take advantage of and parasitize this association
(Bouwmeester et al., 2007). Regardless, the association with fungi is very beneficial
and, in some cases, is believed to be vital for plant survival (Van der Heijden et al.,
2006). There are two leading symbiotic associations with fungi, arbuscular mycor-
rhizae (AM), and ectomycorrhizae (EM) (Lodge, 2000; Mohammadi et al., 2011).
This relationship is and has been very important for plants to such an extent that
many believe that plant radiation or the ability to colonize dry environments would
not have been possible without a mutualistic relationship with fungi and other soil
microorganisms. Mycorrhizae play a vital role in fostering connections within the
forest, where the signals exchanged are beneficial rather than competitive, contrary
6.4 E-R Changes Due to Modifications in Scientific Interpretations 325

to the longstanding belief (Castro-Delgado et al., 2020). Fungi, through mycelia,

interconnect the roots of different organisms that would otherwise never touch
(Mohammadi et al., 2011). Scientists have named this phenomenon “Wood Wide
Web” in allusion to acronyms related to the internet (Simard et al., 1997; Work &
Flowers, 2011; Castro-Delgado et al., 2020; Hooper, 2021). This is wise since this
interplant network functions as if it were the computer internet, interconnecting
nodes (organisms), and exchanging information and substances such as metabolites,
water, compounds, and signals (Castro-Delgado et al., 2020). However, although
the rule is that the exchange is beneficial for different individuals, there are some
exceptions. As with the Internet, the network can steal information, hack, or attack
another organism. For example, several representatives of a group of orchids (genus
Corallorhiza) steal resources through the mycorrhizal network. Others, such as
eastern American black walnut (Juglans nigra), disseminate toxic chemicals through
the network, such as spreading malicious code on the Internet.
This network that interconnects plants is a valuable form of communication that
goes unnoticed by most of us and can be taken as an exception when studied.
However, it is a rule in the plant world. This network interconnects the organisms in
the forest and allows intraspecific but also interspecific synergy.

Plant Senses

At this point, it is worth mentioning that the definitions with which we deal in sci-
ence are very important when cataloging a phenomenon. For example, if we want to
find senses in plants exactly like those we see in animals, it will be a difficult task.
Similarly, if we seek to define mechanisms or structures in animals and plants in the
same way, we will also be often contradicted, and we may draw false conclusions.
If the definition of the phenomenon we are studying is clear, the results we obtain
will also be clear to interpret. The senses in plants have long been neglected due to
the discussed perception that they were almost inanimate sessile organisms that had
no purpose beyond serving as food for other living things (Gagliano, 2013).
However, that conception changed substantially from the last decades of the nine-
teenth century onward thanks to the research carried out by numerous researchers,
especially many tenacious observations and questions made by Darwin himself. It
is complex to think about senses in plants because, in the collective unconscious, the
idea of senses is deeply rooted in what the senses are in vertebrates. However, we
should keep an eye on the other side of the spectrum of living beings.
The senses have always been related to animals. For example, someone has eagle
vision, lynx hearing, dog smell, and so on. However, only a few times do we hear
similar phrases with plants as protagonists. It may have to do with our idea that the
senses are associated with a more or less complex nervous system. Thus, any living
organism lacking it or in poorly developed stages is likely to lack senses.
Nevertheless, examples of minor invertebrates such as jellyfish or planarians with
distinctive sense organs, the visual acuity of an octopus comparable to that of a
vertebrate (Mathger et al., 2009; Hanke & Osorio, 2018), or the proprioception of a
326 6 Focusing on Dynamics: When an Exception Becomes a Rule

scorpion capable of assembling a map of the terrain with high precision (Wolf,
2017) are ignored. Something similar happens with plants.
To be precise in this respect, when we talk about senses, we have to think about
the capacity of the organism to capture the signal and respond to it. To the surprise
of many, plants can develop the most well-known senses, such as vision, smell,
touch, hearing, proprioception, and even memory (Chamovitz, 2020). Indeed, most
of the senses in plants do not align precisely with our current understanding.
However, as mentioned earlier, adopting a broader definition allows for a better
comprehension of how senses function in plants. We will even realize that they are
similar to how they work on animals.

Sight
Perhaps plants do not form images, nor can they discern the color of a predatory
larva or the type of fur of a savannah ungulate. However, what if we define sight as
the ability to detect electromagnetic waves of different lengths and respond to them?
We know that light is essential for them and that they can not only detect it but also
grow toward it. In 1880, Darwin, with his son Francis, studied motion in plants
(Kutschera & Briggs, 2009). They conducted an elegant experiment where they hid
a plant in the dark and left a candlelight burning. They observed that the plant grew
toward the light. They documented positive phototropism in plants (Holland et al.,
2009). This discovery seems simple, but it is gigantic. Not only did the plant detect
the light stimulus, but it sent signals to the stem to grow unevenly so that it could
direct itself to where the stimulus was coming from. Darwin, curious as he was,
sought to discern which was the detector of the stimulus in the plant (Kutschera &
Briggs, 2009; Chamovitz, 2020). Thus, he covered different areas of the stem with
opaque and transparent materials and exposed them to the same light source. Thus,
they realized that the shoot tip participated in light harvesting. This is just one exam-
ple of what plants can “see,” but it is not just a matter of detecting the faint light of
a candle.
Plants can also see different frequencies of electromagnetic waves, detect the
time of day they are in, detect how much light they are receiving, and indirectly
detect if something is blocking their light source (Chamovitz, 2020). Many of these
abilities are given by different photoreceptors. Humans have five photoreceptors,
one for lights and shadows, three for colors (RGB), and a fifth that regulates the
internal clock (Kolb, 2012). Plants possess many photoreceptors. For example,
studies in Arabidopsis thaliana showed that it has more than ten photoreceptors that
tell the plant when to germinate, when to give flowers, and the intensity of light it
receives, among others (Smith, 1982; Izawa, 2008; Babla et al., 2019; Chamovitz,
2020). The rule is that the proteins that function as photoreceptors differ between
plants and animals but fulfill the same function (e.g., two photoreceptors that detect
the color red). The exception to this rule is that both animals and plants share cryp-
tochromes, the photoreceptors involved in circadian rhythm (Chaves et al., 2011).
As Chamovitz (2020) quotes, “in this sense, animals and plants ‘see’ in the
same way.”
6.4 E-R Changes Due to Modifications in Scientific Interpretations 327

Touch
Plants feel touch but do not feel pain (Chamovitz, 2020). Plants possess receptors
that are analogous to those found in humans and other organisms. These receptors
provide plants with information about their environment, enabling them to adjust
their metabolism and respond accordingly. Although the idea of touch, propriocep-
tion, or perhaps the feeling of pain is closely related to the presence of a nervous
system, we have examples that show how plants use a similar mechanism to “feel”
without the need for a nervous system. Here, the common ground and what would
seem to be the rule in sensing is electricity in the form of an electrochemical reac-
tion, something shared by plants and animals (Baluška & Mancuso, 2009;
Chamovitz, 2020). In humans and animals, ions play a crucial role in the transmis-
sion of signals to the brain. They enter and exit the cell membranes, propagating the
signals to the brain. Something similar happens in plants without a nervous system
to mediate the process.
To illustrate, there are two iconic examples of rapid plant movement. These
plants have structures that move in a very short period of time. This type of move-
ment is different from the standard movements in plants called tropisms (Forterre,
2013). Tropisms are slow movements; remember that the times of plants are not our
desperate times (Trewavas, 2005). Plants are much slower than animals and can
afford to be because they are also among the longest-lived organisms (Chamovitz,
2020). Technology has helped analyze normal plant movement thanks to time-lapse
photography systems (e.g., Attenborough, 1995) that allow us to generate videos
with perceptible speeds. Within this classification of rapid plant movement, there
are three main groups: plants that catch and consume prey (carnivorous plants),
plants that move leaves under a stimulus, and plants that use sudden movement to
disperse seeds. In this section, we will address the first two examples. The number
of plant species that show these characteristics are few, and they would be an excep-
tion within the large group of plants.
Among the trapping plants, we have seen the fantastic venus flytrap (Dionaea
muscipula). Anyone with one of these plants will spend long periods (and many
insects) to see them in action. Therefore, the insect prowls between the two trap-like
lobes at the tips of the leaves. The trap is triggered upon stimulus, and the lobes
quickly close and trap the organism (Hodick & Sievers, 1988; Volkov et al., 2008).
Subsequently, digestive juices are responsible for dissolving and absorbing the prey
(Scala et al., 1969). During his studies in this species, Darwin noticed that dark hairs
inside the lobes function as triggers to activate the trap. Scientists have noted that at
least two of these hairs must be stimulated within no more than 20 seconds for the
trap to activate (Volkov et al., 2008; Böhm et al., 2016). This is very interesting as
the plant has to retain somehow the activation information of one of the hairs for
that period, something like a “short term memory” (see below). The hairs on these
plants are not only sensitive but also selective, as they are not activated by any prey
size. Burdon-Sanderson & Page (1877) and Burdon-Sanderson (1882) found that
activation of the hairs generated an electrical signal similar to muscle contraction in
animals.
328 6 Focusing on Dynamics: When an Exception Becomes a Rule

The second iconic example of how touch affects plants is that of Mimosa pudica.
This plant features a compound leaf, and its parts retract upon touch (Ahmad et al.,
2012). Additionally, it exhibits responses to various stressors, including damage,
vibrations, wind, and drought (Volkov et al., 2010). At the electrophysiological
level, it functions similarly to the venus flytrap (Allen, 1969). Touch produces an
electrical signal that results in leaf closure (Bose & Das, 1925). Mimosa pudica has
specialized motor cells at the base of the leaves that cause the leaves to move. The
basic principle is the movement of ions in and out of the cell that produces water
movement and changes in the turgor that causes the leaves to move.
One effect that might be considered rare is that touching can harm plants (Jaffe
& Forbes, 1993; Chamovitz, 2020). It has been found that touching plants can stunt
their growth and kill certain parts. This knowledge came from an experiment inves-
tigating growth in plants. The researchers took leaves and measured them with a
ruler every day. They noticed with amazement that these leaves never grew to a
standard size, and many died. In contrast, the surrounding leaves did not show any
problem. They realized that this was due to the manipulation of the leaves when
measuring.
Finally, many climbing plants have mobile tendrils that are very sensitive to
touch, and the slightest pressure they feel makes them grow around the object. The
tendrils generally make a circular movement trying to contact some structure that
serves as support. Once they touch something, they automatically begin to curl.
Here, we see an association between movement and touch to find an anchoring
place for the branches (Scorza & Dornelas, 2011). As we have seen thus far, plants
feel a lot. They are capable of equating with us and other vertebrates in that sense.
Regardless of the outcome, the plant rule seems to be electrical signals modulated
by ions and some proteins but without a coordinating nervous system.

Proprioception.
The answer is a resounding yes. Plants can “know” where it is down, up, and side-
ways. They know how to orient themselves and where each of their parts is (Moulia
et al., 2019, 2021). The plant “knows” where to put its roots and where the stems go.
Experiments have shown that both zones orient themselves using gravity (Levernier
et al., 2021). The roots have cells with statoliths and spherical structures that are
heavy and respond to gravity. The aerial zones have a zone called the endodermis
associated with the phloem, which also contains these statoliths. The position of the
statoliths tells the plant where it is below. In addition, as we have seen, plants have
an affinity for light or chemical cues that make them move toward the stimulus.
Similar to gravity, these stimuli are detected, and the plant responds by bending to
the position where it needs to go according to the stimulus (Vandenbrink & Kiss,
2019). It uses hormones called auxins that help in various processes. However, they
are responsible for accumulating in certain areas, informing the surrounding cells
that they must increase in size, which will cause the stem or root to bend (Levernier
et al., 2021).
6.4 E-R Changes Due to Modifications in Scientific Interpretations 329

Smell
Again, if we define olfaction as the ability to perceive odors or scents, it is easy to
fit with plants. We already had a preview of how plants use volatile compounds to
communicate, where we talked about pollinators and plants. As we previously saw,
ethylene is a gas that serves to ripen fruits and communication between individuals,
among other functions (Grierson, 2013). Plants detect ethylene particles in the air
and trigger a cascade of signals that produce, e.g., fruit softening (Barry &
Giovannoni, 2007). Fruits can communicate via ethylene, i.e., they can “smell” each
other (Chamovitz, 2020). This is demonstrated when you want to soften a fruit and
put it next to another already ripe fruit. Ethylene production helps uniform fruit
ripening and indirectly synchronizes the timing of seed dispersal. This gas is also
associated with plant senescence processes in leaves and fruits (Iqbal et al., 2017).

Hearing
Here, we find an exception to the pattern cited in this section. There are, thus far, no
rigorous and conclusive scientific studies on hearing (Chamovitz, 2020). The rule or
paradigm at this time is that plants do not hear, and many agree that, unlike other
senses, plants would not need to hear from an evolutionary perspective. However, it
may also be possible that plants do hear, but we still need to perform the proper
experiment to identify it. As happened historically with the other senses. Perhaps
the rule that plants are deaf will change to the exception in the future. Time and
scientific advances will tell.

Memory and Vegetable Intelligence?

Memory is closely linked to the senses. In our case, images, smells, or sounds can
trigger happy or ugly memories. In the case of plants, we have seen cases such as
the venus flytrap that can retain previous events and bring that information to pro-
cess at the moment (differentiated trichome stimulation). This delayed response to
a previous action requires “memory.” Plants can present a basic level of memory
called procedural memory (sensu Tulving, 1985). This simple memory results from
sensing the environment and reacting to the stimulus. Nevertheless, a memory, how-
ever simple, must have three essential components (Klein, 2015). It must have the
ability to form the memory (encode the information), retain the memory (store the
information), and retrieve the memory (obtain the information again). Let us test
this system with the example of the venus flytrap. Something unknown touches a
hair (encodes information) and then retains the information for a few seconds until
another hair is stimulated (stores the information). Once a second hair is touched, it
retakes the previously stored information and closes the trap (retrieves the stored
information). One hypothesis that explains how this happens is related to action
potentials and calcium concentrations (Hodick & Sievers, 1988). The charge and
330 6 Focusing on Dynamics: When an Exception Becomes a Rule

ion concentration of the first stimulus are retained for a few seconds, and the second
stimulus triggers another potential that, together with the previous one, exceeds a
threshold and closes the trap. If this second stimulus does not arrive, the charge and
ion concentration are lost.
Memory can be long-term, as in the case of some plants that need certain condi-
tions to flower. Researchers believe these plants remember the conditions, espe-
cially the seasons where they should flower (Sung & Amasino, 2005; Amasino,
2010; Xu & Chong, 2018). Stress-mediated memory is also transgenerational and
linked to epigenetics (Molinier et al., 2006; Iwasaki & Paszkowski, 2014; Kinoshita
& Seki, 2014). Thus, plants that suffer some environmental stress change the com-
position of their DNA and transfer this information so that the progeny makes the
same modification in their DNA without being exposed to the stressor.
Regarding intelligence in plants, the first thing to note is that there needs to be a
consensus on the definition of intelligence (Manetas, 2012). It can also be believed
that intelligence is an exception presented in humans and some groups, such as
dolphins, elephants, and cephalopods (Manetas, 2012). For plants, the term is more
elusive. When we compile a list of properties associated with intelligence, such as
information sensing, processing, and integration; decision-making and behavior
control; learning; memory; choice; self-recognition; and predictive modeling to
optimize resource acquisition efficiently, we can observe that many of these traits
are shared by plants (Trewavas, 2005).
As we have seen in the previous paragraphs, plants can sense the environment
and respond accordingly. They can solve problems to be more efficient and have
overall higher fitness. Beyond the issue of intelligence, let us keep in mind the cur-
rent rule that plants are aware of their environment (Chamovitz, 2020). Let us recap,
they are aware of electromagnetic waves (light), where it reaches, if it is reaching
them, how much they should reach and what to do to get the most out of it. They are
aware of the chemicals around them and in the air. They are aware of the touches
they receive, gravity, their position relative to other plants, structures, the sun, and
their environment. Plants are more aware of their environment than most of us! All
the rest is widely speculative at the moment. Better development of the scientific
paradigm coupled with new ways of assessing intelligence may give us a better view
of the phenomenon in the future. The new branch of study called plant neurobiology
is very suggestive and invites serious scientific discussion (Chamovitz, 2020).
From what we have seen in this whole section devoted to communication in
plants, we should be generous when discussing rules and exceptions. Once more,
we should remember that the results and discussions at a given time are restricted by
the scientific paradigms and social thoughts of that particular moment, in addition
to the technical and mental capabilities.

6.4.2.4 Epigenetics: When Environment Matters

In science, particularly in biology, there has been a well-known belief, often referred
to as a “dogma,” regarding the “gene–environment association.” According to this
traditional view, information flows solely from genes to the external environment
6.4 E-R Changes Due to Modifications in Scientific Interpretations 331

through the production of proteins via RNA (a concept known as the genetic “uni-
directionality” dogma) (Crick, 1958). As a result, it is commonly believed that if an
organism is born with a specific genotype, it cannot be altered or modified. However,
recent developments have shown the necessity to correct this perception. While this
idea-dogma might have been useful in the early days of modern genetics, it no lon-
ger stands unchallenged today, especially in light of the growing evidence suggest-
ing a significant influence of the environment on genes. Consequently, this notion
can no longer be sustained without facing criticism similar to that encountered by
ideas proposing a strong environmental impact on genetic expression. In his theory
of evolution (previously discussed in Sect. 4.2 of this book), Lamarck postulates
two laws. The first law addresses the fortification or weakening, and even disappear-
ance, of organs based on their respective use or disuse. The second law is more
controversial and proposes that nature preserves these changes in organs by passing
them on to the next generation through the inheritance of acquired characters
(Lamarck, 1809). This theory was discarded in the 1960s, and Charles Darwin’s
theory of evolutionary changes produced by natural selection was favored. However,
it is now being realized that some evolutionary changes are close to the Lamarckism
of that time (Ward, 2018). As mentioned earlier, the Lamarckian theory has regained
attention and interest due to the progress in genetics and our enhanced understand-
ing of DNA. This renewed fascination has been termed “neo-Lamarckism.” The
reason behind this resurgence is that several scientific findings can no longer be
fully explained by Darwin’s evolutionary theory alone; instead, they align more
closely with Lamarck’s theory. This necessarily means that evolutionary theory is
being modified and updated, with the addition of new aspects that reinforce it.
Within this framework, epigenetics stands out, defined as the mechanisms that regu-
late gene expression, which occurs without modifying the DNA sequence (Zulet
et al., 2017). Epigenetics causes evolutionary changes; it is a process still poorly
understood by some but of much importance for evolutionary theory (Ward, 2018).
The most critical part of epigenetics, or at least the most controversial, is behavior
inheritance. This theory was refuted many times for decades. However, several stud-
ies in mice have shown that acquired behavior can be inherited from one generation
to the next (Francis et al., 2003; Darnaudery & Maccari, 2008; Champagne, 2014).
This type of study caused evolutionists to reconsider adding these “neo-­Lamarckian”
findings to the current theory of evolution (Ward, 2018).
Epigenetics provides insight into how certain acquired proteins or life changes
can be passed onto future generations through inheritance. In other words, it high-
lights the significance of recognizing that the conventional “rule” stating that infor-
mation is solely transmitted from genes to the external environment is not entirely
valid. The opposite exists, perhaps not only for the mere regulation of a gene or
genes but also for modifying it, and this modification is inherited (epigenetically,
this change). Today, for example, it is recognized that the nervous system possesses
enormous plasticity. This flexibility can be translated into morphological and func-
tional changes resulting from epigenetic mechanisms in response to some environ-
mental signals. The processes observed in learning, memory, cognitive aging,
addiction, depression, etc., can be regulated by epigenetic mechanisms, which were
unthinkable some time ago (Mahgoub & Monteggia, 2013; Colciago et al., 2015). It
332 6 Focusing on Dynamics: When an Exception Becomes a Rule

has recently been shown that chronic stress, for example, predicts accelerated epi-
genetic aging (Juster et al., 2010; Zannas et al., 2015) and that meditation can sig-
nificantly decrease these stress levels and age-related neuroplastic changes; hence,
it has become a focus of scientific interest to promote healthy aging (Chaix
et al., 2017).
The first discovery where unusual genome results were observed, in which the
responses were not predictable (and thus initially thought to be rare), was made in
the 1940s by Barbara McClintock (McClintock, 1942). In her dissertation upon
receiving the Nobel Prize in 1983, McClintock stated that, building upon those early
results, it was necessary to subject the cell to the same challenge repeatedly to
observe the nature of the changes. She stated that the responses of genomes to
unforeseen challenges are not precisely programmed. However, these challenges
are detected, and the genome responds in a discernible but initially unthinkable way.
These responses, now known to occur in many organisms, are essential for appreci-
ating how a genome can reorganize itself when faced with a difficulty for which it
is unprepared. Our current knowledge of genome responses suggests that these reor-
ganizations originated from some “shock” that forced the genome to restructure
itself to overcome a threat to its survival. Cells can “feel” what is happening. From
this, in a certain way, they make decisions and act on them so that the DNA mole-
cule is correct after accidents that occur inside the cell or outside, such as infections
by viruses, poisons, and altered environments (McClintock, 1984). An example
studied in the framework of epigenetics and its action is that of DNA methylation
processes and others of this type (see table in Rey et al., 2016), which increasingly
encompasses all living beings.
DNA methylation (the addition of a methyl group to a DNA nucleotide) modifies
the accessibility of DNA for protein synthesis, which most often has consequences
for gene expression (Bird, 2002). Some of these methylations can be reestablished
during meiosis, but they can also be maintained between generations and lead to
heritable phenotypic changes (Daxinger & Whitelaw, 2012). Regardless, methyla-
tion is one of many chromatin marking systems. This is obvious if we consider
invertebrates, which have almost no methylation in their DNA. However, cellular
phenotypes are transmitted to daughter cells. In the fruit fly Drosophila, for exam-
ple, there are practical reasons to suggest that they may do so because protein com-
plexes that bind to DNA may act as heritable chromatin marks; however, this is still
unclear, and how that mechanism of inheritance works is not yet understood
(Jablonka & Lamb, 2005). Another process within this framework is histone modi-
fications in DNA, which can also affect the accessibility of its sequence to transcrip-
tion enzymes and ultimately affect genes and their expression (Strahl & Allis, 2000).
Some of these modifications are heritable and associated with changes in the organ-
ism’s life history (Baulcombe & Dean, 2014).
Advances in cell and molecular biology have allowed and continue to allow dis-
coveries in the processes of DNA regulation and demonstrate how specific mecha-
nisms in cells, which could be seen as rare or which were unknown or understudied,
can now be considered as a pattern of cell behavior in terms of gene expression
mechanisms and therefore of (often heritable) changes in phenotype. Recent
6.4 E-R Changes Due to Modifications in Scientific Interpretations 333

progress in transcriptomics, for example, revealed a staggering diversity of RNAs

that do not encode proteins but are involved in the control of transcription and post-
transcription gene expression, being integral parts of epigenetic regulation—even
being inherited from one generation to the next through parental gamete tissues as a
source of nongenetic inheritance (Luteijn & Ketting, 2013; Holoch & Moazed, 2015).
As the field of epigenetic studies expands, so does the interest in exploring new
technologies. To date, numerous methods have been developed to provide a better
and more accurate understanding of the functions of epigenetic regulation. Thus, the
advancement in new methodologies allows the use of multiple strategies, such as
high-quality antibodies, functional chromatin assays, imaging tools, and high-­
throughput sequencing technologies (Zheng & Bernstein, 2015). A breakthrough
occurred with bisulfite sequencing, which is now a standard method for DNA meth-
ylation detection. This method led to numerous subsequent technologies, such as
methylation-specific PCR (MSP) or combined bisulfite restriction (COBRA). New
protocols have also been developed, combining basic techniques to provide a com-
plete understanding of the overall dynamics of epigenetic processes in modulating
the phenotypic expression of the genome (Tollefsbol, 2011). Along with these
advances in methods to unravel the epigenome, challenges have also arisen in man-
aging massive amounts of information. Therefore, new developments in bioinfor-
matics and computational sciences are critical in managing datasets and interpreting
epigenomic functions, as well as multiomics data derived from combinatorial inte-
gration analyses, to further advance the rapid development of epigenetics (Li, 2021).
Recently, there has been increasing interest in the study of whether environmen-
tal factors (such as chemical pollutants, dietary components, and temperature
changes) modulate the establishment and maintenance of epigenetic modifications
and, therefore, whether they could influence gene expression and phenotype (Feil &
Fraga, 2012). To date, the central focus in “Environmental Epigenetics” is centered
on DNA methylation. A classic example in plants is Linaria vulgaris, in which the
flower can present inheritable bilateral or radial symmetry. The change from one
type of flower to the other occurs occasionally and involves alterations in DNA
methylation in a gene encoding a transcription factor without apparent genetic
mutations (Cubas et al., 1999). In addition, there are studies on wild plant popula-
tions in which differential phenotypes have been identified that are associated with
specific DNA methylation profiles, which could appear because of selection
(Herrera & Bazaga, 2010; Lira-Medeiros et al., 2010).
In animal models, it has been shown that nutrition and exposure to certain envi-
ronmental factors during development can lead to specific changes in particular loci
of the epigenome (Rosenfeld, 2010). Concerning human studies, in addition to what
has already been mentioned above regarding the nervous system, it is known that
nutrition and exposure to toxic components at the gestational stage can have long-­
term phenotypic effects involving changes in DNA methylation (Heijmans et al.,
2008; Waterland et al., 2010).
Most epigenetic variation is restored between generations. However, in some
cases, environmentally induced epigenetic variation can result in heritable pheno-
typic plasticity that invokes Lamarckian-like inheritance. However, it can also result
334 6 Focusing on Dynamics: When an Exception Becomes a Rule

from random epimutations that may have higher mutation and reversion rates than
DNA sequence mutations (Robertson & Wolf, 2012). Epigenetics today represents
an additional source of variability, acting as an evolutionary force alongside natural
selection and genetic drift (Schrey et al., 2012). Future research is still needed to
understand the interactions of genotype, epigenotype, and environment and how
they relate to selection. However, epigenetics provides a clear link between a gene’s
genotypic and phenotypic nature (Bolondi et al., 2017). As Jablonka & Lamb (2005)
discuss in their book Evolution in four dimensions (genetics, Epigenetics,
Behavioral, and Symbolic Variation in the History of Life), heritable epigenetic dif-
ferences may also play an essential role in the origin of species. The authors argue
that although speciation is a hotly debated topic, it is generally agreed that new spe-
cies appear when populations become isolated from each other by a geographic or
ecological barrier, which may cause populations to change. These changes prevent
individuals from interbreeding successfully if they meet again. Although we gener-
ally assume that the changes are genetic, they can sometimes be thought of as epi-
genetic because while populations are isolated, they experience different conditions,
use different resources, or experience a different climate. In this case, new epigen-
etic marks could be induced in both somatic and germline cells, which may affect
the functioning of the organisms in the new environment and their ability to inter-
breed between populations. Then, if two previously isolated populations have
acquired different epigenetic variations, the incompatibility between the marks
transmitted by the gametes may prevent a hybrid embryo from developing typically.
Thus, the initial reproductive barrier formation may result from epigenetics rather
than genetic changes (Jablonka & Lamb, 2005).
In this framework, the genetic and epigenetic aspects of the gene can be com-
bined structurally and functionally to include its different levels uniquely (Bolondi
et al., 2017). The latter reinforces our idea that what was previously thought of as a
unidirectional pathway of gene transcription can now be viewed differently and that
in the pathway of selection, not only the gene as a transcribed DNA segment itself
acts but also external factors that could modify its expression, even going so far as
to make it heritable. Epigenetic mechanisms challenge this traditional view and
demonstrate that environmental influences can have an impact on heredity, offering
a more nuanced understanding of the complexities involved in genetic inheritance.

6.4.2.5 Genome Transposons

Linked to the framework also provided by epigenetics to mitigate the unidirectional

view of DNA, the history surrounding the discovery, and studies on transposable
elements within the genome indicates that this was not an isolated event, restricted
to certain plants, as was initially thought. The discovery of transposons dates back
to the mid-twentieth century, as previously mentioned in the context of epigenetics.
This was made possible through the groundbreaking work of Barbara McClintock,
who specifically studied chromosomal breakage in maize plants. From an experi-
ment that aimed to isolate mutants in progeny of self-pollinated maize plants with
6.4 E-R Changes Due to Modifications in Scientific Interpretations 335

broken chromosome ends, it soon became evident that modified gene expression
patterns were occurring (McClintock, 1942). After observing these results,
McClintock concluded that the regulation of the gene expression pattern was associ-
ated with an event occurring in mitosis, in which one daughter cell had gained
something that the other daughter cell had lost. After that, he turned her attention to
determining what one cell had gained, and the other cell had lost. It was then shown
that these transposable elements could regulate gene expression precisely
(McClintock, 1950, 1951, 1952, 1953). These accidental discoveries, with surpris-
ing results for the time, were the origin of much of the subsequent research.
However, her discoveries were not appreciated until the first studies on transpo-
sons in bacteria became known, which allowed an understanding of the importance
of these segments in the bacterial genome and DNA transfer (Shapiro, 1995;
Biémont, 2010). Advances in biology have confirmed that these elements are pres-
ent in bacteria and plants and a wide range of eukaryotes, including several proto-
zoa. Therefore, we know that DNA transposons no longer represent a rare natural
phenomenon, as initially thought. In fact, they must have diversified very early in
evolution and have been maintained in all major branches of the eukaryotic tree of
life (Feschotte & Pritham, 2007; Pritham, 2009). These transposable DNA seg-
ments are an obvious source of mutations, and their activation can affect both
genome structure and function, gene regulation and expression, and alter their epi-
genetic state (Lisch, 2009; Sahebi et al., 2018).
The above has important implications in the combined use of mediated adapta-
tion processes in organisms via epigenetics or transposons, making the issue more
interesting, especially in the face of global climate and environmental change (Rey
et al., 2016). Transposons play a vital role in evolution by generating new genetic
information and regulating stress responses. They contribute to the development of
phenotypes that are tolerant to various stresses, including those related to fruit color
and shape in plants (Makałowski et al., 2019). Numerous studies have shown how
transposons can adapt under different conditions, thus facilitating the survival of
organisms in specific environments and, as a consequence, the expression of genes
in response to stimuli in different organs (Woodrow et al., 2010; Lu et al., 2011;
Ishiguro et al., 2014).
The frequent mobility of transposons can accelerate mutation rates, generating
genetic variability. One example we can mention and demonstrate is the activity of
the Tol2 element in the medaka fish Oryzias latipes, which is responsible for a
1000-fold increase in mutation rate in the pigmentation gene, resulting in different
phenotypes of albino-like individuals (Koga et al., 2006). In addition, transposons
can also generate genetic variants from which functional evolutionary innovations
can arise (Lisch, 2013) and thus also generate genetic diversity. They can affect the
expression of particular genes if inserted into gene-associated regions or promoter
regions (Rey et al., 2016). However, the most important and studied perspective is
related to the epigenetic mechanisms mentioned above, especially DNA methyla-
tion (Galindo-González et al., 2018). Epigenetic mechanisms help to respond rap-
idly to environmental stress through transient or heritable changes. In this context,
transposons also respond to stress and are influenced by changes in the epigenetic
336 6 Focusing on Dynamics: When an Exception Becomes a Rule

state of the genome. This process is essential, given that when a transposable ele-
ment is inserted in or near a coding region, it can modify the epigenetic state of
adjacent gene regions (de Souza et al., 2013). In summary, this new perspective
discussed in these last two sections is very promising. This finding reinforces the
fact that epigenetic mechanisms (not only methylation) and transposons play a fun-
damental role as “classical” alternatives (e.g., random mutation and subsequent
natural selection) in the adaptation of living beings to changing environments. They
are no longer viewed as rare mechanisms and processes but contribute to shaping
the genome architecture, leading to the emergence of genetic innovations from a
wide variety of lineages (Feschotte & Pritham, 2007).

6.4.2.6 Microbiome and Host

Recent advances in microscopy techniques have greatly contributed to our under-

standing of the intimate association between the intestinal microbiome and the host
(Shapira, 2016). This knowledge has been facilitated, in part, by routine use of
advanced biochemical techniques for identifying the bacterial flora within the diges-
tive system. Indeed, while it could once have been considered an exception, thanks
to the use of new technologies such as genomics, transcriptomics, or metabolomics,
it is now accepted that all animals harbor diverse symbionts that aid in the genetic
variation of the individual (Gilbert et al., 2012). Bacteriophages, for example, are
known to be vehicles that allow horizontal gene exchange between different bacte-
rial species and are, therefore, determinants in bacterial evolution (Brüssow et al.,
2004). The ecological and evolutionary significance of these symbioses is of funda-
mental importance when considering the applications of such knowledge.
Furthermore, it has been possible to exponentially increase knowledge about micro-
bial communities and to characterize, for example, human and animal microbiota
and describe new genes, proteins and organisms in various ecological niches.
Continuous technological progress and the search for novel strategies have become
increasingly accessible (Quiroga, 2016).
Symbiosis represents biodiversity in action and is a fundamental life strategy
requiring the exchange of information, products, and mutual regulation between
individuals to ensure stability and adaptability. The microbiome is the most striking
evidence of this (Munzi et al., 2019). We know that the microbiota influences sev-
eral aspects of the biology of its host animal, including food choice, reproduction,
and immune response (Fraune & Bosch, 2010; Ezenwa et al., 2012; McFall-Ngai
et al., 2013). As previously discussed in the chapter on rules and earlier sections of
this book, the profound implications of understanding the intimate interaction
between the intestinal microbiome and the host are evident.
A remarkable example of this interaction is the discovery that the gut microbi-
ome of flies can influence their behavior at the brain level, prompting them to con-
sume specific types of food containing essential amino acids needed by the bacteria
(Leitão-Gonçalves et al., 2017). In this case, essential amino acids and gut bacteria
6.4 E-R Changes Due to Modifications in Scientific Interpretations 337

are critical modulators of protein appetite in flies. The lack of any essential amino
acids in the diet of flies causes them to have a strong appetite for protein-rich foods.
However, flies with a good microbiome do not. This occurs because two species of
gut bacteria (Acetobacter pomorum and Lactobacillus sp.) work to suppress the
appetite for protein and cause flies not to reduce their reproductive allocation
(Leitão-Gonçalves et al., 2017). The impact that bacteria have on the host is due to
complex interactions. Therefore, mapping metabolic interactions in the gut micro-
biome is key to understanding how it influences the host. Advances in metabolomics
have helped to understand and demonstrate how relationships between flies and gut
bacteria function to enable them to alter the feeding decisions of the host. These
metabolic interactions allow bacteria to become resistant to detrimental host diets
and ensure the constant flow of metabolites used by the microbiome to alter their
reproduction and behavior (Henriques et al., 2020).
The microbial community of each animal species has its own functions. For
example, the intestinal microbiota in humans performs metabolic activities that pre-
vent energy losses, help absorb nutrients, and protect the host against pathogenic
microorganisms (Guarner & Malagelada, 2003). A healthy intestinal flora is said to
be the first barrier to avoiding diseases. It creates a protective barrier that hinders the
establishment of pathogenic organisms (Doe, 1989; Ramiro-Puig et al., 2008). To
understand these functions, it is necessary to know the structure and behavior of
microbial communities (Human Microbiome Project), which is why new DNA
sequencing technologies have been advancing rapidly (Escribano, 2016). The same
happens with technologies applied to other vertebrates, such as poultry, where for
example, the advance of metagenomics stands out, offering an alternative for a bet-
ter understanding of the bacterial microbiota and the identification of antibiotic
resistance genes, identification of mobile genetic elements and the effective design
of intervention strategies to break, for example, the transmission of pathogenic
microorganisms during the poultry production cycle (Mantilla & Sáez, 2019).
Thus, data collection from different symbiotic systems using standardized
research methodologies provides insights that are exploited through comparative
analyses and using bioinformatics tools that were previously unknown (Munzi
et al., 2019). Multiomics technologies provide detailed information on different
microbial activities in the environment. Over the past few years, the cultivation of
microorganisms has been overlooked and underestimated. However, its significance
has now been recognized, allowing for the combination of omics techniques to ana-
lyze microbe–host interactions. This has revealed that we inhabit a symbiotic world,
where what was once considered an exception is now acknowledged as the norm
(Munzi et al., 2019). Global data analysis is also becoming more critical to achiev-
ing a broader view of the studied systems. This led to new forms of research, such
as interactomics, to study interactions and transomics to build global biochemical
networks using integrated data (Quiroga, 2016). There is still much to be known,
and we must have reasonable access to new technologies and regulations for their
use. This entails a primarily ethical discussion in terms of research involving
humans and animals, which should start soon (Quiroga, 2016).
338 6 Focusing on Dynamics: When an Exception Becomes a Rule

Holobionts

The knowledge gained in recent years about the existence of an intimate association
between the microbiome and its host has allowed the postulation of principles that
would have been almost unthinkable before, since this phenomenon was considered
a rarity or something exceptional. Animals and plants are no longer announced as
autonomous entities but as biomolecular networks composed of the host plus its
associated microbes, i.e., “holobionts” (Bordenstein & Theis, 2015). This concept,
which we discussed in previous sections (see Sect. 6.2.1.5), was mentioned by Lynn
Margulis in her article “Words as battle cries—symbiogenesis and the new field of
endocytobiology” (Margulis, 1990). She uses this term to refer to symbionts trans-
mitted from one generation to the next. Margulis realized that there were life forms
that were linked almost to their entire existence through a relationship that defined
them. Following his theory, Margulis referred to the holobiont concept as “the sym-
biotic complex” (Margulis, 1991) or “the product, temporary or permanent, of the
association between its constituent bionts” (Margulis, 1993). Before her, Meyer-­
Abich used a somewhat different holobiont concept, describing holobionts as “spe-
cific bionts within an integrated whole,” which he called the “holobiome.” However,
he addressed the same evolutionary and developmental phenomena as Margulis
(Meyer-Abich, 1943).
Subsequently, “holobionts” began to be used to talk about organisms that have a
long-lasting symbiotic relationship (Díaz, 2015) and then to refer to the symbiosis
between a host and several microorganisms (Mindell, 1992; Jorgensen, 1993;
Rohwer et al., 2002). It finally gained popularity when it was associated with the
concept of hologenomic evolution in 2008 by Eugène Rosenberg and Illana Zilber-­
Rosenberg. They postulated that all macroorganisms are holobionts and that the
unity between the host and its entire microbiota constituted a biological individual,
a unit of selection (Zilber-Rosenberg & Rosenberg, 2008). In this paper, the authors
proposed to describe corals as holobionts formed by cnidarians and their algal
symbionts.
The concept of the biological individual, as we saw earlier in this book, allowed
the study of organisms to be facilitated in several disciplines, such as physiology
and genetics, and, added to this, technological advances in these disciplines made it
possible to demonstrate the existing associations between hosts and their symbionts
(Gilbert et al., 2012). We now know that a holobiont is an entity formed by associat-
ing different species that give rise to an ecological unit. This concept has some simi-
larities with the so-called superorganism; however, they should be distinct. Wheeler
initially used the latter term to refer to eusocial insects (Wheeler, 1928). It is a term
used for organisms that establish colonies of individuals with an organized social
structure and division of labor among their members. Superorganisms are formed
by individuals of the same species, different from holobionts (Kramer & Bressan,
2015). In turn, due to the intimate associations between the respective genomes of
the holobiont individuals, they are all taken as a functional unit in terms of physio-
logical and ecological networks, the term hologenome being used for this purpose
(Theis et al., 2016; Rosenberg & Zilber-Rosenberg, 2016).
6.4 E-R Changes Due to Modifications in Scientific Interpretations 339

There is a tendency to argue that it would be incomplete not to consider the

holobiont concept in models on evolution, emergence, and biological complexity
in living beings, suggesting replacing a more reductionist classical view with a
more holistic one. It is in this framework that ten principles (Bordenstein & Theis,
2015) on holobionts and hologenomes have been proposed (Bordenstein & Theis,
2015) to organize this knowledge for future studies in the field, namely, (1) holo-
bionts and hologenomes are units of biological organization; this means that com-
plex eukaryotes are not autonomous organisms but are organizations of several
symbionts and their genomes (Rosenberg & Zilber-Rosenberg, 2013). The asso-
ciations between them are similar to an interaction of genotypes rather than an
interaction between genotype and environment (Thompson, 2013). (2) Holobionts
and hologenomes are not organ systems, superorganisms, or metagenomes, and
this should be distinguished within biology. These terms are used to refer to inter-
actions between symbionts and their hosts but do not imply organization, which is
one of the principles when we talk about holobionts (Baquero & Nombela, 2012).
(3) The hologenome is an integral genetic system consisting of a nuclear genome,
organelles, and microbiome. Thus, variations occurring in any of the genomic
subunits cause hologenomic variation (Bordenstein & Theis, 2015). (4) The con-
cept of the hologenome again takes into account some elements of Lamarckian
evolution, such as that the microbiome is initially acquired from the environment
and can be inherited (Rosenberg & Zilber-Rosenberg, 2018). (5) The variation of
hologenomes includes all mutational mechanisms. Each hologenome is composed
of multiple mutants, i.e., it encompasses mutations occurring in each of the indi-
vidual genomes of its parts (nucleus, organelles, and microbiome) (Rosenberg &
Zilber-Rosenberg, 2013). (6) Hologenome evolution becomes more comprehen-
sible when we draw an analogy between a gene in the nucleus genome and a
microbe in the microbiome. The evolution of genes and symbionts is a change in
population frequency observed over successive generations, i.e., the fraction of
holobionts carrying that particular gene or microbe. Moreover, this evolution fol-
lows a joint inheritance of gene combinations, which ultimately functions like
population genetics (Bordenstein & Theis, 2015). (7) The concept of a hologe-
nome is adapted to selection theory. A holobiont is exclusively a host and its
associated microbiota; therefore, different holobionts, for example, a pollinator
and a flower, interact with each other under specific ecological characteristics
(Lloyd, 2007). (8) The hologenome is shaped by selection and neutrality, which
means that selection can propagate advantageous nuclear mutations or microbes
or eliminate detrimental mutations. When selection does not act, the propagation
of hologenome variation occurs exclusively by chance, i.e., as a stochastic process
(Hubbell, 2005; Sloan et al., 2006; Nemergut et al., 2013). (9) Hologenomic spe-
ciation combines genetics and symbiosis. The study of hologenomic speciation is
no longer optional. It is a necessary frontier that must be crossed to fully under-
stand the origin of species (Bordenstein & Theis, 2015). (10) Holobionts and their
hologenomes do not change the rules of evolutionary biology. Although the con-
cept of what an animal or a plant is redefined, this does not change evolutionary
theory. If the microbiome is a significant component of holobiont DNA, genetic
340 6 Focusing on Dynamics: When an Exception Becomes a Rule

variation can result in new adaptations and speciation (Peiffer et al., 2013;
Goodrich et al., 2014).
The structure of the holobiont makes us consider that selection then acts at mul-
tiple levels. Within the microbiome itself, all kinds of biological and ecological
interactions are present. Therefore, host characteristics are only one of the factors
that determine it. Biotic interactions within this holobiont and selection pressures
may play an essential role in determining this structure (Cerqueda-García & Falcón,
2016). In conclusion, the discovery of the holobiome and its subsequent in-depth
study opens up new opportunities and possibilities for research about the factors
influencing the evolution of species, which until now were limited. The concepts of
holobionts and the hologenome do not transform evolutionary thinking. Instead,
they affirm that hosts and their symbiotic microbes are complex units of organiza-
tion upon which ecology, evolution, and selection act (Bordenstein & Theis, 2015).

6.4.2.7 About “Cryptic” in Biology

In various fields of biology, researchers have unveiled the existence of mechanisms

and cryptic processes that are not immediately evident but are nonetheless present.
These processes are more prevalent than previously believed, challenging the notion
that they are mere rare occurrences. In a broad sense, by being cryptic, we refer to
different characteristics that organisms can present that make it possible for them to
go unnoticed by other animals (Allaby, 2015). Among these characteristics, one
notable example is camouflage, which can either involve fixed coloration (as seen in
classic examples such as striped patterns in zebras and tigers) or changing color-
ation (as observed in chameleons and cuttlefish that adapt their color based on their
environment). In addition to visual crypsis, there are examples of olfactory crypsis,
such as the case of squid ink (Conover, 2007) or the case of acoustic crypsis in some
nocturnal butterflies to confuse predators (Miller & Surlykke, 2001), to name just a
few examples. Indeed, these examples have been nothing new to the reader since
they are widely accepted mechanisms in the contexts where they have been
described. However, as we acquire more knowledge of the biodiversity surrounding
us, these examples are multiplying. Let us also think of new technologies for detect-
ing ultrasonic sounds, such as acoustic crypsis, where we were unaware of their
existence because we did not have the necessary equipment for their detection.
In this context, it is crucial for scientists to acknowledge the minor genetic varia-
tions that may be involved in cryptic processes. Even though these variations may
have a limited or no immediate impact on the phenotype, they can manifest them-
selves under specific conditions. The “crypsis,” the hidden, can also encompass
physiology. For example, hidden processes, not “so visible” that have been
neglected, as was the communication in plants that we have already discussed ear-
lier in this chapter. The concept of cryptic holds significant potential for analysis, as
it transforms from being disregarded or viewed as rare and abnormal to something
familiar. It is possible that we had not paid enough attention to it before due to tech-
nological, methodological, or theoretical challenges (such as paradigms,
6.4 E-R Changes Due to Modifications in Scientific Interpretations 341

perspectives, biases, etc.). As we delve deeper into this concept, we uncover its
importance and relevance in various biological phenomena. In this sense, we will
focus on two examples of the cryptic biology studied recently, mainly due to
advances in schools of thought, technologies, and more excellent knowledge of
diversity.

Cryptic Genetic Variation

The variation in the genome that is not expressed in the phenotype observed in a
population is called cryptic genetic variation (CGV) (McGuigan & Sgro, 2009;
Gibson & Dworkin, 2004; Paaby & Rockman, 2014). The CGV indicates that the
genetic diversity observed in a population is only a part of the potential diversity
that can be produced and is a long-standing topic of study in evolutionary genetics,
driven by the need to explain the adaptive capacity of populations to the constant
changes that are occurring in the environment they inhabit (Gibson & Dworkin,
2004). Stress conditions that are generated in the environment where a given popu-
lation inhabits and new conditions that populations may face (e.g., colonization of
new environments, see Sect. 6.2.2.1) are suitable scenarios for CGV to become vis-
ible, as they contain mutations that were invisible when they emerged but may
become evident under new circumstances (Paaby & Rockman, 2014).
In this sense, CGV studies became more frequent when analyses of the high
levels of genetic variation associated with new phenotypes in a given environment,
for example, after disturbance processes, began to be carried out (Gibson &
Dworkin, 2004). However, what is the importance of having the tools provided,
thanks to advances in genomic technologies, that allow us to know the CGV? Here,
we can name some critical advantages that their knowledge offers us. For example,
being able to know how organisms might respond to specific mutations, both in
evolutionary and health contexts (such as diabetes and autoimmune diseases, for
example), would undoubtedly be beneficial since we would know in advance how
organisms might adapt or not adapt to specific changes in the environment, for
example (Gibson & Dworkin, 2004). CGV could also take place in artificial selec-
tion processes in animals to contribute to the stabilization of new phenotypes, for
example (see Sect. 6.3.4.1) (Gibson & Dworkin, 2004).
CGV can be viewed from a molecular or quantitative point of view (Paaby &
Rockman, 2014). From molecular genetics, cryptic genetic variations are polymor-
phic loci that do not affect phenotype until they are perturbed by some rare condi-
tion (Gibson & Dworkin, 2004). From quantitative genetics, cryptic genetic
variation is an increase in heritable phenotypic variation that arises when a popula-
tion is exposed to rare conditions (Hermisson & Wagner, 2004; Paaby & Rockman,
2014). Additionally, CGVs may have a role in disease development. In this sense,
alleles that accumulate while hidden may cause the onset of diseases in humans.
However, thus far, the existing evidence is insufficient to support this hypothesis.
Undoubtedly, studies in this field could be very advantageous when predicting, for
example, the onset of certain diseases (Paaby & Rockman, 2014). To date, the
342 6 Focusing on Dynamics: When an Exception Becomes a Rule

models traditionally used for the detection of CGV have been Drosophila melano-
gaster and Arabidopsis thaliana (Gibson & Dworkin, 2004). However, these study
models will undoubtedly be expanded in the coming years.

Cryptic Female Choice: From Restricted to Rule

A field where the cryptic aspect has been analyzed in increasing depth is sexual
selection. We will devote more space to it since it is a rich subject. First, let us put
the subject in context. Sexual selection mechanisms can occur in a precopulatory
context through competition between males for access to females through ritualized
fights or demonstrations (intrasexual selection) and choice of females where the
evaluation criteria can be very varied (intersexual selection), obtaining direct bene-
fits such as food or shelter, or indirect benefits through higher quality offspring
(Darwin, 1874; Trivers, 1972). These mechanisms have mainly influenced the
development of secondary sexual characteristics in males. Think of the classic
examples of the antlers of cervids or the striking colors of the peacock’s tail (Darwin,
1874; Trivers, 1972; Firman et al., 2017).
Concerning the sexual selection mechanisms associated with cryptic organisms,
our focus of interest here is after copulation has begun, i.e., in a postcopulatory
context (Andersson & Iwasa, 1996; Eberhard, 1996; Jennions & Kokko, 2010;
Hosken & House, 2011). In this sense, if we consider processes that are not directly
available to the observer’s view as cryptic, we can name sperm competition (Parker,
1970) and cryptic female choice (Thornhill, 1983; Eberhard, 1996), as these pro-
cesses take place within the female reproductive tract. Sperm competition is a post-
copulatory extension of male–male competition, where males compete through
their ejaculates within the reproductive tract of females for access to fertilization of
their eggs (Parker, 1970). This competition is framed in game theory as males try to
do their best to maximize their reproductive success against the interests of other
males. The male needs to think about what is best for him, but it depends on what
the other males do. Selection pressure favors traits in males that will help them
increase their fertilization success, favoring the ability to outcompete the sperm of
males that were previously copulated with the female and reducing competition
with sperm from subsequent males (Thornhill, 1984; Cordero, 1990; Alcock, 1994;
Calbacho-Rosa & Peretti, 2015). Studies of sperm competition that show their evo-
lutionary importance in the processes linked to sexual selection have received par-
ticular interest in recent years, showing that they occur in many species of different
taxa, no longer as specific exceptions (Andersson, 1994; Birkhead & Møller, 1998).
The increase in this type of study has undoubtedly been possible thanks to techno-
logical advances, for example, the development of filming equipment that has
allowed us to observe the process of intromission of the copulatory organs of males
in the reproductive tract of females to be able to associate them, for example, with
the placement of sperm in a particular area to favor its use, or the removal of sperm
that the female may already have from previous copulations, to name just a few
examples.
6.4 E-R Changes Due to Modifications in Scientific Interpretations 343

However, the term cryptic has been explicitly used as a form of female choice not
to confuse the reader; when we refer to cryptic, we refer to female choice processes.
Therefore, cryptic female choice (CFC) is the process of female choice that contin-
ues during and after mating, allowing females to bias (through morphological,
behavioral, and physiological mechanisms—Arnqvist, 2014) paternity by “choos-
ing” the sperm from which males will fertilize the majority of their eggs (Thornhill,
1983; Eberhard, 1996; Biswas et al., 2022). Let us keep in mind that until only a few
years ago, it was thought that males controlled all processes associated with repro-
duction in animals. In this sense, as mentioned above, males competed for access to
females in a precopulatory sexual selection framework, and their ejaculates contin-
ued to compete within the reproductive tract of females for fertilization of eggs in a
postcopulatory sexual selection framework; and females … What role were females
supposed to have? None of their roles was passive, and they were only considered
“simple reservoirs” of sperm. The idea that monogamy was the rule and that polyga-
mous species were instead the exception, mainly in the animal kingdom, was also
deeply rooted. However, thanks to changes in scientific interpretations, undoubtedly
based on advances in sociocultural thinking, females began to be seen as active
participants with the capacity to “choose” or bias in reproductive processes. In the
same way, it was seen that the rule in nature was polygamy favoring these processes
of sexual selection. In this sense, a female can also select with which male she will
copulate, a female choice in a precopulatory framework, and even choose with the
sperm of which male she will fertilize her eggs, a cryptic female choice in a post-
copulatory framework. So you see, females have an active role just like males. This
acceptance has undoubtedly had a significant impact on the current paradigm shifts.
Our interpretations have undergone such significant changes that concepts such as
female choice no longer seem strange to us. In fact, we have progressed to the point
where considering the possibility of cryptic female choice does not appear far-­
fetched. This openness to new ideas and possibilities reflects the evolving nature of
scientific understanding and our willingness to explore and embrace novel concepts
in biology. From the beginning of copulations, several processes are controlled by
females. For example, staying quiescent to facilitate the spatial location of the male
and the insertion of intromittent organs, allowing the placement or transfer of sperm
to storage and fertilization sites, sperm nutrition, egg maturation, and implantation
in the uterus, among others. These examples almost naturally show that females
have an active role in sexual interactions (Eberhard, 1985, 1991, 1996; Shuker &
Simmons, 2014; Biswas et al., 2022).
In his book, published in 1996, Eberhard shows that CFC processes are wide-
spread in numerous insect species based on different behaviors that males develop
during or after mating. These behaviors exhibited by males, which aim to stimulate
females to utilize the sperm of a specific male, are referred to as copulatory court-
ship. This courtship behavior can be classified into two types: genital or nongenital,
depending on which body structure the male uses to stimulate females (Otronen,
1990; Eberhard, 1991, 1994, 1996, 2009; Calbacho-Rosa & Peretti, 2015).
Technological advancements, such as the development of video cameras with slow-­
motion capabilities, played a crucial role in drawing attention to male behaviors
344 6 Focusing on Dynamics: When an Exception Becomes a Rule

associated with copulatory courtship. These cameras enabled the detection of high-­
speed behaviors that were previously challenging to observe (Dell et al., 2014), as
mentioned earlier in Sect. 6.4.2.1. Additionally, detailed descriptions to determine
frequencies, relationships, and chronologies of particular behaviors in sexual inter-
actions allowed for fine-grained descriptions of behavioral patterns. However, to
demonstrate that a behavior functions as copulatory courtship, it must also be asso-
ciated with increased fertilization success for a given male. This idea proposes that
males stimulate females, which allows the female to bias paternity toward the male
she “thinks” did better! In this sense, genomic tools such as multiallelic variable
number of tandem repeat (VNTR) polymorphism analyses were also very useful
(Pena & Chakraborty, 1994). Additionally, many studies in arthropods have shown
that copulations are more prolonged than necessary if the only function involved is
sperm transfer; this gives the possibility that males are developing other behaviors,
for example, those linked to copulatory courtship (Eberhard, 1996, 2009; Calbacho-­
Rosa et al., 2013).
On the other hand, and associated with CFC, we can name genital evolution,
which has been studied and demonstrated in numerous species in recent years. One
of the most striking evolutionary trends is the significant divergence and complexity
observed in male genitalic structures across various taxa with internal fertilization
(Eberhard, 1985; Leonard & Córdoba-Aguilar, 2010; Peretti & Aisenberg,
2015; Eberhard & Lehmann, 2019). In contrast, females do not exhibit such diver-
gence, and their genitalia typically have a uniform appearance. Like copulatory
duration, this great complexity and variation in male genitalia would not make
much sense if the only function was sperm transfer to females (Eberhard, 2009).
Therefore, these genitalia may serve other functions, such as those associated with
CFC, where male genitalia, through copulatory courtship, stimulate females to bias
their sperm use during egg fertilization (Eberhard 1985, 1996; Eberhard & Lehmann,
2019). The advancement of equipment, including powerful stereo microscopes and
various types of microscopes (e.g., compound microscopy, transmission micros-
copy, phase-contrast microscopy, confocal microscopy, and scanning electron
microscopy), has facilitated the observation of genital structures with exceptional
precision. These developments, along with progress in physiology and histology,
have been instrumental in investigating and identifying significant variations in
genital structures. As Eberhard (1991, 1996) points out, in various species with
internal fertilization and where CFC takes place, copulation does not always lead to
insemination, nor does insemination guarantee egg fertilization. Consequently, it is
reasonable, and perhaps even logical, to consider the occurrence of cryptic mecha-
nisms in such a crucial process as offspring production. These mechanisms are more
likely to be a pattern rather than an exception.
Due to the substantial resistance among many researchers to accept the possibil-
ity of CFC while acknowledging sperm competition, Eberhard and Lehmann (2019)
raise an important question in their paper. They inquire about the amount of evi-
dence needed to definitively establish the existence of the CFC, considering the
skepticism surrounding this hypothesis. Crickets of the species Roeseliana roeselii
and flies of the genus Glossina show us significant evidence in favor of CFCs. In the
6.4 E-R Changes Due to Modifications in Scientific Interpretations 345

case of these flies, sperm transfer occurs at the end of copulation, and males perform
various nongenital behaviors during copulation. The function of these behaviors is
copulatory courtship to stimulate females (Jaensen, 1979; Briceño et al., 2007). On
the other hand, the males of R. roeselii, as occurs in many other cricket species, have
titillators. These titillators are paired chitinized structures that do not directly func-
tion in sperm transfer (Wulff & Lehmann, 2016). Movement of these structures
during copulations is associated with female stimulation under CFC (Wulff &
Lehmann, 2016; Eberhard & Lehmann, 2019). According to Eberhard and Lehman,
while expecting absolute confirmation of the hypothesis may not be logical, there is
a wealth of evidence in the form of morphological and behavioral traits in both
males and females. These pieces of evidence strongly support the existence of CFCs
in numerous species across different taxa. From our perspective, scientific interpre-
tations are evolving due to advancements in technology and sociocultural changes.
Cryptic phenomena are no longer considered mere rarities but are increasingly rec-
ognized as widespread occurrences. This shift in understanding is facilitated by
improved technological capabilities and changes in societal attitudes.
Beyond the mere behavioral evidence, there are some other cases that favor the
CFC. In some species of insects and spiders, for example, males give nuptial gifts
to females at mating. These gifts are usually prey that the females may eat during
mating. The nuptial gifts may be an honest signal representing the quality of the
male, so it is a trait that may be under CFC. Among insects, for example, females
regulate oviposition according to the size of prey given as nuptial gifts, resulting in
a bias toward those males in fertilization (Thornhill, 1983). Another example is the
nursery web spider Pisaura mirabilis, where gift-giving males have more signifi-
cant mating and fertilization success (Stalhandske, 2001; Prokop & Maxwell, 2009).
The CFC hypothesis has also been linked to the evolution of male parasperm, a
nonfertile type of sperm (Hayakawa, 2007). While previous work shows that sperm
and nonsperm components of the ejaculate can serve in the CFC (Eberhard &
Cordero, 1995; Cordero, 1998), it has recently been suggested that the parasperm
evolves as a function of CFC (Swallow & Wilkinson, 2002; Oppliger et al., 2003;
Holman, & Snook, 2006). Parasperm could lead to increased ejaculate size and
movement within the spermatheca (Shepherd & Bonk, 2021), which could stimu-
late females to use the sperm of a particular male for the fertilization of their eggs
(Holman & Snook, 2006). This has been observed in butterfly species such as Pieris
rapae (Wedell & Cook, 1999) and Plodia interpunctella (Gage, 1995). It should be
noted that this type of analysis has been possible thanks to more advanced physio-
logical studies that have made it possible to differentiate which components of the
ejaculate are spermatozoa and which are not so that different functions can be attrib-
uted to them.
Another less studied advantage attributed to CFC is that females could avoid
inbreeding depression by avoiding fertilizing their eggs with sperm from related
males. CFC would favor utilizing sperm from genetically different males (Løvlie
et al., 2013), as seen in the cricket Gryllus bimaculatus (Tregenza & Wedell, 2002)
and the domestic fowl Gallus gallus (Birkhead et al., 2004). Similarly, this prefer-
ence of females to avoid inbreeding could be detected thanks to technological
346 6 Focusing on Dynamics: When an Exception Becomes a Rule

advances in genetic studies that allow us to know the degree of kinship between
individuals. The possibility of CFC in humans is much more controversial and even
less studied. Currently, some studies seem to show that follicular fluid may differ-
entially regulate sperm behavior and thus influence fertilization success (Ralt et al.,
1991; Fitzpatrick et al., 2020), although many studies are still needed to obtain suf-
ficient evidence to support the occurrence of this process. Undoubtedly, with the
advancement of science, this type of study could be developed with much more
frequency and accuracy, having precise results on issues that today seem distant.
As we have been saying, CFC is the process of choice by females, which takes
place during and after mating, allowing them to “choose” the sperm of which male
they will use to fertilize most of their eggs. However, Kekäläinen (2022) suggests
that there is evidence to show that females may also select among sperm from the
same male. In this sense, CFC acts through prefertilization processes at the cellular
and molecular level that facilitate gamete-mediated mate choice (GMMC,
Kekäläinen & Evans, 2018), allowing fertilization bias toward genetically compat-
ible sperm haplotypes (Kekäläinen, 2022). This may happen as gametes are geneti-
cally unique, and then different sperm can be expected to differ in their compatibility
with female eggs, which will ultimately have consequences on offspring fitness
(Immler et al., 2014; Alavioon et al., 2017, 2019; Kekäläinen, 2022). This raises the
possibility that GMMC evolves to select compatible sperm genotypes within the
ejaculate of the same male (Kekäläinen, 2022).
As we have already said, trends in scientific thought have always been associated
with the sociocultural context of the moment. The study of female choice processes
has received relatively little attention within the field of evolutionary biology and
has often been regarded as rare exceptions. In the past, the prevailing paradigm in
the context of sexual events focused on the notion that males solely controlled these
processes. In the past, it was not widely acknowledged that females could actively
participate in these scenarios by exercising choice in selecting their mating partners.
Moreover, the idea that mate choice processes could extend beyond the initial stages
of mating was not commonly believed, as mentioned earlier in this discussion.
However, as research has progressed, we are now beginning to recognize and appre-
ciate the active role that females play in these processes and the potential for mate
choice to continue beyond the initial mating stages. The hypothesis of female
choice, encompassing both precopulatory and postcopulatory choices, has been
steadily gaining acceptance and overcoming previous biases. We now acknowledge
that females are generally polyandrous, engaging in multiple mating, and actively
contributing to decisions related to reproduction. It has been a significant change in
the paradigm that predominated until few years ago. Scientific interpretations no
longer only focus on the explanations of the operant processes from the approach of
the males, analyzing their costs and benefits but also from the point of view of the
advantages of the females.
Therefore, what is certain is that, to a greater or lesser extent, what is happening
is a significant change in the views of the roles of each sex and the mechanisms
involved in decision-making, among others (Eberhard, 1996; Peretti & Aisenberg
2015). Indeed, the need for a robust theoretical framework shows that cryptic
6.4 E-R Changes Due to Modifications in Scientific Interpretations 347

processes are much more frequent than we think. This lack may also have been
responsible for these rejections of the increasingly eloquent evidence that it is, for
example, the CFC hypothesis that specific mechanisms are operating
(Eberhard, 1991).
Finally, the study of sexual cryptic processes requires an understanding of mech-
anisms associated with insemination, storage, and fertilization that, until a few
decades ago, were little explored areas (Birkhead, 1998; Biswas et al., 2022).
Consider the technological advances that have allowed differential paternity studies,
the key to supporting sperm competition, and CFC hypotheses (Simmons & Wedell,
2020). For example, innovative techniques that allow assessment of sperm storage
and fertilization sites within the female genital tract, techniques that consist of ster-
ilization of males by exposure to X-rays (which do not affect the fertilization capac-
ity of sperm but do cause embryo death at an early stage of development—e.g.,
Kaster & Jakob, 1997 in spiders) and innovative microsatellite techniques to be able
to determine, by DNA analysis, the paternity of eggs (Weber et al., 2018; Forsdick
et al., 2021). Additionally, in vitro technologies developed in recent years have
aided the understanding of cryptic processes, which, together with an increased
acceptance of female participation, have favored the study and development of
cryptic female choice (Firman et al., 2017).

6.4.2.8 Sexual Selection in Plants: From Simple Curiosities

to a Generalized Fact

As we said, the history of sexual selection is complicated from its beginnings, and
many factors influenced this. One of the strongest was that Darwin developed this
theory in the Victorian era. This was quite a turbulent time for such revolutionary
and new theories. Victorian society was entirely dominated by demureness, moral-
ism, and discipline, with rigid prejudices and severe interdictions, which can be
roughly summarized as repression (Aksenchuk, 2006). It was a society where men
were the ones who ordered and dominated the public space, and women were lim-
ited to the private space under a submissive status. Victorian values could currently
be classified not only as sexist but also as “puritanical,” and the most prominent
were the values of thrift, hard work, the extreme importance of morality, the duties
of faith, and Sunday rest (Charlot & Marx, 1993). Let us imagine then how difficult
it must have been to develop a theory with a taboo subject such as sex in such a
puritan society (Vandermassen, 2004). Darwin was struck by the number of charac-
ters that are exaggerated and hard to explain by natural selection. He saw that, in
general, males develop fighting or attention-seeking characters and that females
develop an “advent for beauty” (Stephenson & Bertin, 1983; Andersson, 1994).
Thus, males fought directly or indirectly among themselves to be chosen by females
and to leave offspring.
As mentioned in the previous section, sexual selection arises as an extension of
natural selection in which both males and females develop tactics and traits that
allow them to reproduce more and better. Just as in natural selection, the organism
348 6 Focusing on Dynamics: When an Exception Becomes a Rule

that does not adapt does not survive; in sexual selection, the organism that is not
reproductively successful does not necessarily die but leaves no offspring, some-
thing like a “reproductive death.” The theory of sexual selection was conceived
based on higher vertebrates such as mammals and birds and has a strong influence
on human beings. Darwin did not wholly account for lower organisms, not even
arthropods, and much fewer plants (Andersson, 1994; Arnold, 1994; Moore &
Pannell, 2011). The latter fact is striking, considering the avid studies on plants car-
ried out by Darwin and his son Francis (Darwin, 1875; Darwin, 1899; Darwin &
Darwin 1880, 1888). The prevailing paradigm or the way plants were perceived at
the time dated back to the time of Aristotle. The view was that plants were consid-
ered vegetative organisms lacking a “soul” and a “specific purpose in life.” This idea
contrasted with animals, organisms that had voluntary movement. Because of this
view, the scientific models were primarily animals, especially vertebrates, that
showed much more visible behavior to researchers. Added to this strong bias toward
animals was the strong anthropocentrism reigning since antiquity. Consequently,
plants have received limited scientific attention beyond their practical applications
in everyday food and medicine (Jones, 1996; Petrovska, 2012).
On the other hand, we must keep in mind that sexual selection was developed
with dioecious organisms. However, it only requires sexual reproduction and not
necessarily two sexes (Andersson, 1994). Again, with this premise, some lower
organisms and most plants are left out. In addition, male reproductive success in
plants is more difficult to quantify than in animals (Andersson, 1994). Finally, the
concept of sexual selection was perhaps too strict for plants to fit. A subtle relax-
ation of the definition allows us to incorporate plants and other organisms, which
were not contemplated at the beginning of the theory (Andersson, 1994; Moore &
Pannell, 2011). Sexual selection was not a theory embraced by the scientific com-
munity quickly (Moore & Pannell, 2011). Indeed, except for a brief lapse in the
early twentieth century (e.g., Fisher, 1930; Noble 1934, 1936), it was not until the
late 1960s and early 1970s that sexual selection, and especially female choice, was
progressively analyzed in depth both theoretically and empirically.
Plants have always seemed to fall outside the framework of sexual selection.
Darwin did not consider them and mentioned them vaguely in his theory. He con-
sidered that sexual selection did not represent a crucial selective force in them and
in lower organisms since they could not “appreciate the beauty in the other indi-
vidual” (Moore & Pannell, 2011). Thus, until relatively recently, sexual selection in
plants was mainly ignored (Stephenson & Bertin, 1983). In botany, at most, anec-
dotal examples were cited that were no more than curiosities or exceptions at the
time but could rarely be generalized to the majority of the group. In the early twen-
tieth century, Correns (1917, 1928), Heribert-Nilsson (1923), and Brink (1927)
believed that pollen competition could have evolutionary consequences. Similarly,
Haldane (1932) and Mulcahy (1979) postulated that competition between pollen
grains is essential for the reproductive success of plants. Haldane (1932) also real-
ized that plants produce much more pollen than is necessary to fertilize ovules.
Huxley (1942) suggested that competition between pollen grains favors the speed of
pollen tube growth. Until that time, these were all anecdotal observations, with a
6.4 E-R Changes Due to Modifications in Scientific Interpretations 349

certain amount of hypothesis and speculation. It was not until 1948 that there was
an essential change in the conception of sexual selection in plants. Bateman
unequivocally suggested the existence of sexual selection in plants (Andersson,
1994; Birkhead & Møller, 1998). Recall that Bateman developed the principle that
female reproductive success is limited by the number of eggs the female produces
(fecundity), while male reproductive success is limited by the number of matings
the male can make (Bateman, 1948; Trivers, 1972).
At present, we can say that there is a break in thinking, going from perceiving
sexual selection as something rare in plants to a phenomenon that occurs. However,
there still needs to be more discussion of the extent of this phenomenon in plants as
a group. Although it was an important milestone to have determined that sexual
selection could also operate in plants, there was little interest for almost 30 years. It
was not until the 1970s that numerous papers came to light that spoke of pollen
benefiting from larger inflorescences (Willson & Rathcke, 1974), reaffirming the
idea that there is an increase in both pollen and nectar and linked it to male flowers
(Gilbert, 1975), and spoke of mating preference in plants (Janzen, 1977—although
he does not mention sexual selection). Willson (1979) suggests that sexual selection
may be responsible for different evolutionary phenomena, such as the emergence of
pollinia and different mating systems. More recent work in the 1980s considers the
influence of sexual selection on the evolution of plants and mating systems, with
emphasis on dioecious systems (Lloyd, 1979; Bawa, 1980a, 1980b; Givnish, 1980;
Bawa & Beach, 1981; Webb, 1981; Casper & Charnov, 1982). By that time, bota-
nists had already applied the idea of sexual selection with plants in mind, but some
difficulties arose (Moore & Pannell, 2011). For example, we already cited that
Darwin avoided hermaphroditic organisms, and we know that many systems in
plants are hermaphroditic. In addition, conspicuous secondary sexual characters are
absent, such as those in animals. Since the 1990s, numerous papers have explored
different examples of characters shaped by sexual selection (reviewed in Skogsmyr
& Lankinen, 2002); these authors state that although sexual selection in plants is not
denied today, there is much controversy in the interpretation of specific mechanisms
and the function of certain structures.

Analogies Between Plants and Animals

The rule is that sexual selection operates in plants. Perhaps what is confusing is try-
ing to visualize sexual selection at the prefertilization stage of plants. The exception
at this level is the production of enormous amounts of pollen, even far over the
number of ovules to be fertilized. This can be directly compared to the production
of large quantities of sperm in the males of most animals. However, it will be harder
to see if we are looking for something similar to precopulatory competition between
animal males. Imagine that the display of males is hardly perceived by “females” in
plants, or at least it has not been demonstrated thus far. Thus, the showiest flowers
do not target the female flowers or the female part of the plant, but their primary
target is the pollinators. Recall that to transfer pollen, pollinators or means of
350 6 Focusing on Dynamics: When an Exception Becomes a Rule

pollination, such as wind, are needed. This fact makes the idea of sexual selection
even more distant and complex if we compare it to animals. However, once the pol-
len reaches the pistil and starts to compete, it becomes a much more familiar selec-
tion scenario comparable to sperm competition in animals.
From a precopulatory point of view, physical confrontation was evidence that
helped Darwin devise the concept of sexual selection; thus, confrontational behav-
ior between males is commonly known among animals (Andersson, 1994). This
was thought to be rare or absent in plants (Lloyd & Webb, 1977; Queller, 1987;
Grant, 1995; Murphy, 1998; Skogsmyr & Lankinen, 2002; Delph & Ashman,
2006; Moore & Pannell, 2011), but recent studies in pollinaria strongly suggest
that this would not be difficult to find in plants. For example, direct competition
has been found to exist between pollinaria of Apocynaceae (milkweeds) (Cocucci
et al., 2014). Pollinaria compete for access to specific points on the pollinator’s
body and can sometimes concatenate to existing pollinaria. This causes a decrease
in the reproductive display of the resident pollinium. Thus, from a sexual selec-
tion standpoint, there are individuals who better exploit optimal anchorage sites
on the pollinator previously occupied by pollinia of rival individuals (but see
Coombs et al., 2012 for a noncompetitive explanation). There is evidence that
horn development in pollinators is a strategy that avoids concatenation. Here, we
see that reproductive success depends on physical interference between individu-
als in the absence of autonomous movement and sensory perception as present in
animals.
From a perspective closer to postcopulatory in animals, in addition to the produc-
tion of large amounts of pollen, pollen tubes compete with each other once they
reach the pistil, similar to how sperm from different males compete to fertilize eggs.
This phenomenon can be taken as an extension of the intrasexual competition that
we cited as an example previously among pollinia (Cocucci et al., 2014) and similar
to what occurs between male–male competition in animals and its extension to the
postcopulatory level (Birkhead & Møller, 1998; Simmons 2001, 2014). Gamete
aggregation structures also transfer more significant numbers of gametes in a com-
pact form. Examples are pollinia, as mentioned earlier in plants (e.g., orchids and
Asclepias), and sperm packages, sperm bundles or spermatozeugmata in animals
(Pitnick et al., 2009). These would be mechanisms to win the competition between
different individuals. However, will there be mechanisms to prevent competition? In
animals, structures such as genital plugs prevent the female from mating with a new
male, something like a chastity belt (Simmons, 2001; Kunz et al., 2014; Stockley
et al., 2020; Fromhage, 2012). In addition, there are guarding behaviors where
males generally do not let other males contact the female (mate guarding) (Alcock,
1994; Simmons, 2001). In plants, structures similar to genital plugs are not cited,
but there is a similar mechanism: the inhibition of pollen grain germination by the
presence of adjacent pollen. Some pollen grains do not germinate in the presence of
other grains, either from the same male or from other males (Skogsmyr & Lankinen,
2002). There are also examples where large pollen deposits cover the female stigma,
preventing the germination of pollen from other individuals (Skogsmyr & Lankinen,
2002). In plants, pollinators favor pollen transfer. In this sense, if we consider that
6.5 Key Concepts and Ideas in This Chapter 351

pollinators allow transport and reach the site of gamete deposition (the pistil), we
could say that they fulfill a function partly analogous to the structures that animals
use for sperm transfer (e.g., spermatophore, insect aedeagus, penis).
On the other hand, there is room for cryptic female choice in plants (e.g., Janzen,
1977; Charnov, 1979; Willson & Burley, 1983; Galen & Rotenberry, 1988; reviewed
in Charlesworth et al., 1987; Queller, 1987; Lyons et al., 1989; Marshall & Folsom,
1991). Cryptic choice appears once pollen reaches female reproductive structures
(Bernasconi et al., 2004; Paterno et al., 2020). These structures can select pollen
according to their compatibility (self-incompatibility—Haring et al., 1990;
Takayama & Isogai, 2005) according to genetic compatibility systems or by dis-
tance from which the pollen originates (Outcrossing distance Price & Waser, 1979;
Waddington, 1983; reviewed by Bertin, 1988; Doust & Doust, 1988; Waser, 1993).
In the first case, this system may have evolved to avoid inbreeding, and this type of
choice does not favor any particular phenotypic trait (Waser, 1987; Andersson,
1994). We see that histochemical control is common in pistil receptivity and pollen
germination itself (whether she “allows” it or not), but there is also evidence of
selective seed abortion, something similar to what can occur in animals (Simmons,
2001; Simmons, 2014). However, some researchers suggest that selective abortion
is not a mechanism to select mates but rather one to ensure a fitter offspring (e.g.,
Queller, 1987).
In conclusion, to summarize the idea of this section on sexual selection in plants,
we see that there has been a profound paradigm shift since Darwin. The issue of
sexual selection was resisted at first, but then it was taken as a strong evolutionary
force in animals. Plants were slow to join this paradigm due to old conceptions that
considered plants “vegetables” and “soulless” organisms. The change of conception
added to the relaxation of the definitions of sexual selection, and the advent of
microscopic molecular studies and laboratory assays allowed the shape of the idea
of sexual selection in plants from an exceptional idea to a fairly widespread, mas-
sive rule in the plant kingdom.

6.5 Key Concepts and Ideas in This Chapter

• In biology, as occurs at the epistemological level with the advent of new para-
digms, there are transitions from rarities or exceptions to patterns or rules. This
is part of an intrinsic dynamism linked to our way of conceiving scientific knowl-
edge, but it is also a property of biological systems. We review multiple examples
of these transitions in biology.
• The dynamics of E-R can be the result of natural processes, anthropological
processes linked to activities of human beings, and finally changes in the percep-
tion of science and nature and the development of technological advances.
• Although life is currently the rule on planet Earth, it was originally an exception.
In primitive environments where the rule was a lack of oxygen, the first organ-
352 6 Focusing on Dynamics: When an Exception Becomes a Rule

isms were responsible for modifying the atmosphere so that life could become
the rule we know today.
• Other illustrative and key examples in the evolution of life as we know it today
were the appearance of eukaryotes, multicellularity, and sex. These rare and
uncommon events can be seen as “teratological” phenomena that were success-
ful, linked to changes in gene expression, becoming rules later on.
• Today, the earth is dominated by living beings, but there was a time when the rule
was the opposite and there were no terrestrial organisms. The terrestrial conquest
was an exceptional milestone, and the organisms that achieved it were also
exceptional. Most likely, these organisms were rare, with “extreme” qualities to
tolerate transitional terrestrial systems. That is, traits that are rare and a priori
useless at one time can become an advantage at another time and make the trait
the rule at another time under different conditions.
• In general, when colonizing individuals possess genes that are not representative
of the population, the new population descending from them may have an altered
gene frequency. This founder effect can lead to the appearance of traits or dis-
eases that were rare in the original population. Thus, there is a change from
exception to rule but also from rule to exception since the few individuals from
the original population that may be in the new population carry the alleles that
will now be rare in this new population.
• Phenotypic plasticity is a phenomenon whereby organisms with the same geno-
type can express a different phenotypic range depending on the environment.
The characters to be expressed may at first be hidden and suddenly, if the envi-
ronment is favorable, generate a novel character that may initially be a rarity.
This change in the environment can also be due to atypical, rare conditions that
did not occur before and did not allow the character in question to be revealed.
• Another example of the dynamism of exceptions to rules is observed in intro-
duced exotic species, which in general tend to present a great competitive ability
and capacity for propagation, which makes them quickly become common and
abundant in new environments.
• Global processes such as diseases that can even become pandemics begin as an
exception, which in a certain space and time, with the help of changing human
habits and relationships, can become a rule.
• Human action processes such as environmental pollution and climate change
have accelerated in recent times, so many patterns that were rare before are very
common now.
• Trends in scientific ideas have always been very closely linked to the sociocul-
tural context that is validated or current at the time. Some witness cases that have
been changing are, for example, the field of animal learning or personality, the
senses in plants, or female cryptic choice in sexual selection. The changes in
perspective and increase in the number of studies have led us to know more
examples, and although these phenomena are not considered as rules, they are
now accepted not only as mere exceptions.
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Chapter 7
Focusing on Dynamics: When a Rule
Becomes an Exception

In science it is important to modify and change own ideas as

science advances
—Herbert Spencer

Contents
7.1 Introduction 406
7.2 R-E Changes Due to Nature’s Own Action 407
7.2.1 Reductions and Disappearances of Characters and Interactions 407
7.2.1.1 From Common to Vestigial and Rare Structures 408
7.2.1.2 Behaviors that “No Longer Fit” 411
7.2.1.3 Altered Interspecific Interactions 412
7.2.2 From Dominant to Rarities and Major Extinctions 414
7.2.2.1 Changes in Population According to Inhabited Space 415
7.2.2.2 Climate Relics 417
7.2.2.3 Relictual Species 418
7.2.2.4 Great Extinctions: From R to E to Disappear 420
7.2.2.5 Living Fossils 423
7.3 Human-Induced R-E Changes over Nature 425
7.3.1 Reduction or Loss of Changing Capacity in Living Organisms 425
7.3.1.1 In Animals and Plants: The Effect of Artificial Selection
and Associates 425
Global Pollinator Crisis 428
7.3.2 In Humans: Reduction of Human Integration to Natural Dynamics 429
7.3.2.1 Toward a More Artificial Human Species? 429
7.3.3 Toward the Extinction of Organisms as a Massive Phenomenon (“Folding”
Life Diversity) 431
7.3.3.1 Effect of Deforestation, Hunting, and Fishing 433
7.3.3.2 Effect of Introduced Species 435
Animals 436
Plants 438
7.3.3.3 On Secondary Extinctions of Biodiversity 439
7.3.4 Climate Change and its Effect on the Dynamics of R to E 440
7.3.4.1 Effect of Global Warming on Organisms 441
Changes in the Distribution, Hybridization Processes, and
Interactions of Animal Species 441

© Springer Nature Switzerland AG 2024 405

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_7
406 7 Focusing on Dynamics: When a Rule Becomes an Exception

 ollinators and Plants: Phenological and Distributional Changes

P
That Result in Mutualistic Interaction Interference 443
7.3.4.2 Modification or Disappearance of Water Sources and Watercourses 444
Lakes, Rivers, and Permanent or Seasonal Ice 444
Oceans and Their Communities 446
7.4 R-E Changes Due to Modifications in Scientific Interpretations 448
7.4.1 Key Factors Linked to Change 448
7.4.1.1 Biases in Study Approaches 448
Use of “Model Species” and Generalized Extrapolation 449
A Witness Field: Sexual Selection 450
7.4.1.2 Knowledge of Biodiversity and Evolutionary Framework 451
Geographic (Intraspecific) Inadequacy 454
Phylogenetic (Interspecific) Inadequacy 456
7.4.1.3 Linked to Current Equipment and Methodologies 457
Monogamy in Sensu Stricto in Birds 457
Thermoregulation in Ectothermic Animals 458
Sexual Cannibalism: From Conjecture to Reality in Scorpions 459
7.4.2 With “Potential” of R-E by the Change in Interpretations 461
7.4.2.1 Is Life Confined to Earth? 461
7.5 Key Concepts and Ideas in this Chapter 465
References 467

Abstract In this chapter, we look at the other side, the cases where the rules have
become exceptions. The factors responsible for these changes are diverse. Let us
consider, for example, those changes produced by nature itself, where certain char-
acters, behaviors, and even interactions that were previously very common became
rare or even disappeared; changes associated with climatic relics, relict species, up to
major extinction events. Let us also think of the changes that humans have made in
nature that are responsible for certain rules becoming exceptions, the effects of arti-
ficial selection, deforestation, species introduced into environments that are not natu-
ral, and of course the climate change in which we are major participants, to name just
a few examples. Additionally, the changes from rules to exceptions can result from
changes in scientific interpretations, such as biases in study approaches, biases in the
choice of model species for research, and their general extrapolation of results with-
out, in many cases, the necessary precautions, in addition to the biases in interpreta-
tions associated with the use of certain current equipment and methodologies.

7.1 Introduction

As we explored in the previous chapter, on exceptions that became rules, in many

cases, this includes the reverse situation, i.e., a rule that became an exception. For
example, an exotic organism introduced into a given territory was initially a rarity
numerically speaking, but over the years, it became a rule compared to other organ-
isms inhabiting that territory. This, therefore, implied that other native organisms
that, for example, were displaced from their niches by the intruder gradually became
7.2 R-E Changes Due to Nature’s Own Action 407

rarer and scarcer, becoming the exception. In this example, they shifted from being
considered a rule at the group level to becoming an exception.
In the following, we will expose some examples that imply a passage from rules
to exceptions, sometimes following this idea of opposites, implicit twins, as we
have already mentioned. Other examples may not have been discussed in previous
chapters. The idea is that we observe specific examples of rules falling, not through
a complete replacement by another rule leading to their disappearance but rather
through their “restriction” to exceptions within certain contexts of time, space,
and group.

7.2 R-E Changes Due to Nature’s Own Action

7.2.1 Reductions and Disappearances of Characters

and Interactions

When it is generally mentioned in the biological evolution literature about the

reduction of a trait (e.g., Darwin, 1859; Ha & Nehm, 2014; Kraaijeveld et al., 2016),
the topic itself is closely connected to what we have discussed about how a rule
could vary over time from the condition of being a “norm” to becoming a rarity later
on. In essence, we are discussing rules (represented by the mean phenotype, the
most common one) from an adaptive standpoint. Over time, due to directional selec-
tion favoring another phenotype (which might have been previously at the extreme
end of the distribution), it becomes the less common pattern. This shift can cause the
altered structure to remain within the range of characteristics found in the standard
distribution but now extend toward the extremes. This process could be attributed to
the influence of natural selection and sexual selection acting on that specific trait.
For example, by changing predation pressure, the environment, etc., it becomes the
exception now (e.g., in a specific environment, with x predator in place). We are
then talking about a “mix” of change in one or more traits of a given group, in a
given space, and in a given time. It would be reductionist to limit this situation to
only one of these contexts. At this point, then, when we speak of patterns that
became rarities, we can refer to those traits that we observe in nature, whether mor-
phological or behavioral, for example, that were once very frequent and are no
longer so (Darwin, 1859; Porter & Crandall, 2003). Indeed, these traits once had a
specific function. Nonetheless, certain changes, as mentioned earlier, such as envi-
ronmental shifts or interactions with other species, rendered their function unneces-
sary for individuals or, in extreme cases, even harmful to them (Darwin, 1859; Lahti
et al., 2009; Maughan et al., 2006; Walker-Larsen & Harder, 2001).
One of the research goals of evolutionary biology is to determine why new traits
arise and how they influence the better fitness of individuals (Ellers et al., 2012).
However, less attention has been given to the evolutionary loss or decline of particu-
lar traits (Darwin, 1859; Royer et al., 2016). Only in recent years have researchers
paid more attention to the study of the processes that trigger the loss of traits, taking
408 7 Focusing on Dynamics: When a Rule Becomes an Exception

them from being the most frequent to just rarities (Ellers et al., 2012; Lehmann
et al., 2007). As with acquiring new traits, trait loss can occur at different levels
ranging from total loss in extreme cases to vestigialization (see below, subitem
7.2.1.1). In this sense, the evolution of morphological traits, which includes the
acquisition and loss of traits, is made possible by changes in embryonic develop-
ment (Gould, 1977; Prud'homme et al., 2007). In the 1980s, significant technologi-
cal advancements, particularly in histochemistry, biochemistry, and DNA and RNA
analyses, allowed for a substantial increase in the number of analyses and interpre-
tations of previously unknown processes. As a result, the identification of genes
involved in morphological evolution began in specific animal models (Prud'homme
et al., 2007). The development of morphological traits, involving their acquisition
and loss, is based on the expression of particular genes encoding transcription fac-
tors and molecules for cell signaling (Carroll, 1995; King & Wilson, 1975;
Prud'homme et al., 2007).
Different evolutionary causes can lead to the loss of traits (Ha & Nehm, 2014;
Kraaijeveld et al., 2016), in this sense going from being the most frequent and stan-
dard to being considered rare when observed in nature. Some of these causes include
natural selection (such as changes in the environment and predation pressure, as
mentioned earlier), as well as intraspecific and interspecific competition, external
biotic factors (e.g., interspecific interactions, as discussed below), and abiotic fac-
tors (such as food and resource availability and colonization of new environments)
(Darwin, 1859; Royer et al., 2016). These factors ultimately lead to a particular trait
or structure becoming obsolete in its function. Making an analogy with item 6.2.2.1,
where individuals who colonize new environments may not possess the most com-
mon allele frequency in the population, and due to gene drift processes, such as the
founder effect and bottleneck, these allele frequencies may become common in the
new population. The opposite may also occur in a nonexclusive manner. Specific
allele frequencies that were common or the rule may now become rare or may not
even remain in the population once it has settled in the new location. In addition, the
loss of certain traits may be the product of molecular causes, such as deleterious
changes and mutations in specific genes that alter their function (Drouin et al., 2011;
Hiller et al., 2012; Kraaijeveld et al., 2016). In some cases, trait loss can occur rap-
idly over time, which is an exception to the general rule that evolution occurs
through small changes over long periods (Johnson et al., 2012). In the following, we
will analyze some classic and not-so-classic cases of traits that are no lon-
ger common.

7.2.1.1 From Common to Vestigial and Rare Structures

When we discuss vestigial organs, we refer to those structures that have lost, during
evolution, their original function, which contrasts with the functionality they may
have had in ancestral species and related species (Smith & Wright, 2018). If the
presence of the trait does not cause any disadvantage in individuals, it might not be
eliminated or take a long time to do so. However, all structures need energy for their
development and maintenance, which also means that there is selective pressure to
7.2 R-E Changes Due to Nature’s Own Action 409

eliminate structures that do not increase the fitness of individuals. At one extreme,
if the trait becomes detrimental, it should be eliminated more quickly.
Although vestigial structures have lost their original function, they may still have
other minor functions (Muller, 2002). Darwin (1859) said, “An organ may become
rudimentary for its primary purpose and be used for a different purpose.” For exam-
ple, penguins’ wings are vestigial, as they have lost their original flight function but
have a new function associated with locomotion in water. In ostriches, wings have
also lost their original flight function but now have functions associated with tem-
perature control and display in males in reproductive contexts. Boas and python
snakes show traces of the pelvis, and the toes in some species, such as horses, are
examples of vestigial structures. In cetaceans (whales, dolphins, and porpoises),
limbs and fur have been reduced or even disappeared. The loss of limbs was favored
by natural selection for greater swimming efficiency (Johnson et al., 2012; Xiong
et al., 2009). However, one of the most notorious examples of vestigial structures is
those observed in cave-dwelling species. In these species, it is common for the eyes
to have ceased to be functional (in addition to a reduction in pigment and metabolic
rate and hypertrophy in nonoptical sensory organs) (Borowsky & Wilkens, 2002;
Porter & Crandall, 2003). For example, in the fish Astyanax mexicanus, although
embryos develop optic primordia, these degenerate during ontogeny so that adults
lack eyes (Jeffery & Martasian, 1998; Yamamoto & Jeffery, 2000). Other traits go
from being a pattern to just a rarity in terms of their frequency in nature; i.e., the loss
of a particular trait occurs in cases where sexually reproducing organisms switch to
an asexual mode of reproduction (Kraaijeveld et al., 2016). For example, among the
traits lost by these organisms, we can name the ability to attract mates and fertilize
eggs (van der Kooi & Schwander, 2014).
Plants may also show vestigial structures, such as stipules and carpels, which no
longer have a clear function (Knobloch, 1951), as well as a reduction in flower size
in those that reproduce without crossing (Eckert, 2002). The aquatic plant Decodon
verticillatus shows a sexual or asexual reproductive system depending on its distri-
bution area. The loss of the ability to reproduce sexually in this species may have
occurred several times in evolution, where populations with asexual reproduction
show lower values of genetic and morphological variability (Dorken & Eckert,
2001; Johnson et al., 2012). Among the hypotheses given by the authors to explain
why the loss of sex could have occurred, we can name, for example, mutations that
lead to the loss of sexuality and advantages of asexual reproduction in the fact that
it frees resources previously destined for sexual reproduction (Eckert, 2002; Johnson
et al., 2012).
In humans, since Darwin (1859), organs or structures that would be in the vesti-
gial category have been recognized; here, we will give just a few examples. The
appendix, for example, is considered vestigial because it does not maintain its
digestive function. However, the appendix maintains functions associated with
immunology and maintains the intestinal flora (Muller, 2002). In turn, the wisdom
teeth are vestigial from human ancestors, where their function was associated with
grinding food, but this function was gradually lost as the human diet shifted toward
more prepared and softer foods; in some people, these teeth are no longer present
(Bollinger et al., 2007; Rozkovcová et al., 1999). Some muscles of the human body
410 7 Focusing on Dynamics: When a Rule Becomes an Exception

have also become vestigial. The musculature in monkeys’ ears is significantly more
developed than that in humans, granting them the ability to move their ears for
enhanced hearing, especially in response to potential threats. In contrast, as men-
tioned before, humans have less developed ear muscles and compensate for the
inability to move their ears by having the capacity to turn their heads. The muscle
on the dorsal part of the head that attaches to the ear (auricular superior muscle)
varies in its frequency of occurrence in the current population; for example, it is
present in 36% of the European population, 56% of the African population, and
50% of the Asian population (Macalister, 1871). The palmaris muscle is absent in
14% of the population, with no function today, but is believed to have been involved
in locomotion on trees in primates (Tamatsu et al., 2007). The vomeronasal organ,
an organ associated with olfaction, whose primary function is the detection of pher-
omones in sociosexual contexts, is considered a vestigial structure in humans
(Meredith, 1991).
Among the vestigial structures in humans, we can also include embryological
remnants that serve a function during development, such as the belly button, and
analogous structures between the biological sexes. For example, males are born
with two nipples, and we do not know what function they serve compared to females.
The tailbone or coccyx, despite being a vestige of the primate tail, serves a func-
tional purpose for us, such as providing the insertion point for pelvic muscles and
muscles that aid in bowel movements (Saraga-Babić et al., 1994). Human embryos
develop a tail formed by the last vertebrae in the early stages of development, but
after approximately 8 weeks, these disappear completely (Smith & Wright, 2018)
(see below how, in some cases where this disappearance does not occur, they are
considered teratologies). The loss of the tail, a pattern in our ancestors, is thought to
have occurred as part of the evolution of humans to favor our bipedal stance.
Determining how the loss of this conspicuous morphological trait occurred in our
ancestors has been a source of research for scientists (Smith & Wright, 2018). In
recent years, thanks to significant technological advances, it has been possible to
determine that the loss of this trait would have its basis, similar to most evolutionary
changes, in genetics. The cause could have been the alteration in the location of the
gene related to the presence of the tail or a different site in the genome in a primate
species, which generated a mutation that ultimately resulted in the disappearance of
the trait (Smith & Wright, 2018). Vestigial molecular structures also exist in humans.
For instance, the L-gulonolactone oxidase gene, responsible for producing an
enzyme that synthesizes vitamin C, is functional in most mammals. However, a
mutation in this gene in humans has rendered it incapable of performing such a
function (Ohta & Nishikimi, 1999).
However, with many of these vestigial cases becoming extreme or exceptional
cases, this change from being the pattern to rarity could result in such a modification
of the trait in question that it becomes something “quasi-teratological” from a bio-
medical point of view, that is, if such a structure is no longer used and is strikingly
odd when it appears. This implies that rather than on a continuous trait, something
discrete, qualitative, quite distinct, does or does not appear, and when it does, it is
very striking to the rest of the population. This may occur in ancient structures,
without current use and due to a “long-term time” action, which means that what
was the norm is now no longer even an extreme in the original distribution. However,
7.2 R-E Changes Due to Nature’s Own Action 411

if it appears (i.e., is rarer, outside the new distribution limit of the trait), it is terato-
logical in the classical concept, already discussed in the chapter focused on
exceptions.
Is this possible? We will mention some examples below, which do not make it
thus far-fetched, mainly when focusing on humans. As we said before, we have the
example of tail loss in humans. There are exceptional cases where these tails do not
disappear. Babies can be born with tails, which can be considered teratology. These
are vestigial protrusions and are considered pseudotails, not true tails, because
although they have muscles and nerves and are covered by skin, they do not possess
bone and are not connected to the spinal cord (Mukhopadhyay et al., 2012; Smith &
Wright, 2018; Xia et al., 2021). A congenital disability results in babies being born
with this pseudotail (Dao & Netsky, 1984; Dubrow et al., 1998). Again, technologi-
cal advances allow these pseudotails to be surgically removed and the individual to
live an everyday life (Spiegelmann et al., 1985). Another trait that can be considered
teratology in humans is excessive hairiness. In the 1860s, a woman of Mexican
nationality showed some features that made her “attractive” at that time. Features
such as short stature, multiple teeth, protrusions with excrescences, and a significant
presence of hairiness all over her face and body made her an “ape-like freak” to use
the terminology of the time. Worthy of display in circuses, this woman was pre-
sented as a hybrid between a human and an orangutan (Moros, 2004).

7.2.1.2 Behaviors that “No Longer Fit”

In the previous section, we discussed and provided examples of morphological

traits that can be considered vestigial. Due to the loss of their function, these traits
have transitioned from being predominant patterns to becoming rare occurrences,
and in the most extreme cases, they are considered teratologies. However, the traits
we can refer to are not only morphological, but we can also include certain behav-
iors that, by loss of their function, cease to be the predominant pattern (Rognini,
2018). For example, let us think about the classic cricket song; in most species,
males perform a chirp, a function mainly associated with mate attraction. However,
the males of a population of Teleogryllus oceanicus do not perform this characteris-
tic behavior. The reason is linked to the fact that this song attracts, in addition to
females, the parasitoid fly Ormia ochracea. Thus, when males sing, they have a
higher risk of parasitism (Johnson et al., 2012; Schneider et al., 2018). Another case
to mention is that of some species of frugivorous birds, where males have changed
their usual pattern of showy coloration to a more monotone hue, a trait directly
associated with attracting females (Johnson et al., 2012). This loss of sexual traits
may be linked to the presence of a new parasite or predator, which is also attracted
to this trait (Johnson et al., 2012). These examples illustrate how selection pres-
sures, in this instance, the presence of a parasitoid species, can influence the modi-
fication of traits from being the most common behavioral pattern (Tinghitella &
Zuk, 2009; Zuk et al., 2006). Another factor that can lead to a sexually selected trait
becoming rare is if the communication channel between individuals is disrupted.
For example, the water in some lakes has become polluted to the point of becoming
so turbid that it makes it impossible for females of some fish species to see
412 7 Focusing on Dynamics: When a Rule Becomes an Exception

underwater, which reduces the selection pressure for conspicuous coloration of

males, leading to a shift from conspicuous coloration, which was the predominant
pattern, to a duller coloration (Johnson et al., 2012).
In humans, we can also name some behaviors that no longer “fit” today. The forma-
tion of goosebumps in humans under stress is a vestigial reflex; its function in human
ancestors was to raise the hair from the body to create a larger appearance, aiding in
scaring away predators and maintaining a higher body temperature through the creation
of an extra layer of air (Foltán & Šedý, 2009). Another behavior linked to vestigial
reflexes is hiccups; in this case, researchers have proposed that hiccups are a remnant of
amphibious respiration (Straus et al., 2003). Children’s and some adults’ fears of the
unknown, darkness, and loud noises have their basis in ancestral self-protective behav-
iors in the face of potential danger (Carleton, 2016; Craske, 1999; Rognini, 2018).
Additionally, infants’ reflex behaviors, such as finger-­prehensile behavior, are consid-
ered vestigial. It is postulated that an ancestral primate would have had sufficient body
hair for the offspring to grasp tightly, unlike in modern humans, where the prehensile
response, while evident, is comparatively of lower strength (Futagi et al., 2012; Rognini,
2018). The sudden reflex extension of the arms and legs in infants in response to sudden
stimuli, which may have served the purpose of staying close to the mother, could also be
considered vestigial behavior (Ropper & Brown, 2005).

7.2.1.3 Altered Interspecific Interactions

Several factors can lead to changes in interspecific interactions or even specific

traits in interacting species, resulting in the most common pattern (rule) becoming
rare. One example arises when one of the species experiences a decline or complete
extinction in its population due to natural or artificial causes, thereby significantly
impacting the other species’ way of life. Here, we will focus on changes in the inter-
actions between species produced by natural causes and, later in this chapter, on
those interactions that have been altered by human action.
Numerous examples of changes in interspecific interactions resulting from the
disappearance of one species can be traced back to the great extinction of mega-
fauna at the end of the Pleistocene, approximately 12,000 years ago. This extinction
was primarily caused by the direct or indirect effects of modern humans (Araujo
et al., 2015; Galetti et al., 2018; Guimarães Jr. et al., 2008) and climate change
(Alroy, 2001; Guimarães Jr. et al., 2008). For instance, in South America, at least
seven genera of large mammals became extinct (Guimarães Jr. et al., 2008).
While the causes of this mass extinction have been subject to extensive debate, the
current focus is on its consequences (Galetti et al., 2018; Johnson, 2009; Malhi et al.,
2016; Smith et al., 2016). Among the consequences of this great extinction, we can
expect the loss of other species that were dependent on extinct species, a phenomenon
known as coextinction, especially in closely intertwined interactions such as parasit-
ism and mutualism (Colwell et al., 2012; Galetti et al., 2018; Pires & Guimarães Jr.,
2013). As a result, interspecific relationships that were once prevalent are now almost
nonexistent. However, some species associated with extinct megafauna managed to
survive by adapting and establishing new interactions with their environment. For
instance, they adopted asexual reproduction strategies and even formed associations
7.2 R-E Changes Due to Nature’s Own Action 413

with secondary dispersers such as humans, though often displaying examples of evo-
lutionary anachronisms (Galetti et al., 2018; Janzen & Martin, 1982).
Moreover, what do we mean by evolutionary anachronism? This concept in evo-
lutionary biology refers to traits of living species that are best explained by coevolu-
tion with species that have become extinct. Evolutionary anachronism has been
discussed mainly considering the contexts of seed dispersal (fruit morphology) and
defense strategies shown by numerous plant species associated with interactions
with extinct animal species (Guimarães Jr. et al., 2008; Janzen & Martin, 1982).
Large herbivores disappeared, but the plants that evolved along with them did not,
remaining without their primary natural disperser and forming part of what has been
called “evolutionary ghosts” (Barlow, 2001; Guimarães Jr. et al., 2008). Let us keep
in mind that a trait that is considered an evolutionary anachronism is not the same
as a trait that is considered vestigial (see item 7.2.1.1) since the former retains its
original function while the vestigial trait does not.
Now, let us explore examples of species with anachronistic evolutionary traits
resulting from changes in species associations over time. One well-studied case
involves the morphological characteristics of large, fleshy fruits, which once relied
on large mammals for seed dispersal (Galetti et al., 2018; Janzen & Martin, 1982).
These large mammals were extinct 12,000 years ago. We have the case of avocado
Persea americana, a medium-sized tree with a tasty fleshy fruit containing an enor-
mous seed. The animals that consumed this fruit were large animals, such as giant
elephant species of the Gomphotheriidae family, giant sloths, and toxodonts, now
extinct. The size of its seed makes it almost impossible for today’s animals to con-
sume and disperse it; however, the avocado survived because it is a species culti-
vated by humans, first in Mesoamerica and now worldwide. A similar case of a plant
surviving through human intervention despite the extinction of its consumers and
main dispersers is the mango (Mangifera indica) (Agnolin et al., 2001).
Other illustrative cases are the Louisiana orange tree (Maclura pomifera) with
ample fruits and the Kentucky coffee tree (Gymnocladus dioicus) with thick, sweet-­
smelling seed pods. Additionally, the large, fleshy fruits of the lucumo (Pouteria
splendens) and lucumillo (Myrcianthes coquimbensis) found in northern Chile may
have been eaten by the mylodon (Mylodon darwini). Additionally, the classic exam-
ple of the pink shower tree Cassia grandis, which Janzen and Martin (1982) noted
that the local fauna did not consume its large fruit, on which they based their argu-
ment of evolutionary anachronism. Guimarães Jr. et al., (2008) formulated an exten-
sive list of characters that show the fruits of the plants cataloged under evolutionary
anachronism; for example, the large, mature fruits germinate where they fall, they
are not attractive to arboreal mammals or current fruit-eating birds, and their distri-
bution is fragmentary since their main dispersers are extinct (Agnolin et al., 2001).
Other traits observed in some plants and considered evolutionary anachronisms
are spines and toxins that protect them against large herbivores that no longer exist
(Bond & Silander Jr, 2007; Galetti et al., 2018; Greenwood & Atkinson, 1977). In
the first case, Janzen & Martin (1982) also included among plants with anachro-
nisms several species of Bromeliaceae, such as pineapple (Ananas bracteatus),
because of its complex, spiny leaves around the fruit (Agnolin et al., 2001). Another
example is Ibicella lutea, whose fruits have long spines and sticky hairs, which
would have allowed them to adhere to the legs of extinct megafauna for dispersal
414 7 Focusing on Dynamics: When a Rule Becomes an Exception

(Agnolin et al., 2001; Barlow, 2001). Regarding the presence of toxins, Janzen and
Martin (1982) also included among the plants with fruits with traits associated with
evolutionary anachronism the Genipa americana tree with fruits with a thick and
toxic shell (Agnolin et al., 2001). Additionally, the Kentucky coffeetree named
above is an example since its peel and pulp are poisonous (Zaya & Howe, 2009).
Other examples are several species of the Cucurbitaceae family, such as Cucurbita
foetidissima, which produce bitter-tasting toxins and are harmful to humans and
livestock (Agnolin et al., 2001; Barlow, 2001).
The study of the consequences of the Pleistocene megafaunal extinction on
plant-frugivore interactions has been deepened in recent decades (e.g., Guimarães Jr.
et al., 2008; Loiselle & Blake, 2002). From the perspective of our book, what is
certain is that numerous processes that were the norm, the rule in interspecific inter-
actions, became rarities or even disappeared altogether, as we have seen. For exam-
ple, we can think of the dispersal of a smaller number of seeds over much shorter
distances than usual, as well as alterations in the genetic structure of populations
due to a decrease in gene flow (Guimarães Jr. et al., 2008; Jordano et al., 2007). The
extinction of megafauna also produced alterations in other animal species with
which they interacted. For example, in New Zealand, there are bird species with
specific coloration patterns and nocturnal habits, which could reflect the existence
of predatory species that influence these behaviors and are now extinct (Johnson,
2009). Another behavior considered an evolutionary anachronism is shown by the
American pronghorn, Antilocapra americana, which develops a high escape speed
from its current predators, much faster than necessary for a successful escape. In
this sense, this incredible speed was necessary to escape Miracinonyx, which is now
an extinct cheetah-like predator that inhabited North America. The extinction of
numerous herbivores also produced alterations in their predators that managed to
survive. For example, the jaguar Panthera onca prefers smaller prey than other
felids. It is believed that the species underwent a dietary shift toward smaller prey,
as larger prey became extinct. This adaptability allowed the species to survive
(Galetti et al., 2018; Hayward et al., 2016).

7.2.2 From Dominant to Rarities and Major Extinctions

The history of life on our planet is a continuous process of the creation of new spe-
cies and the extinction of others, which made it possible to form an enormous vari-
ety of natural branches in the tree of life. From the beginning, as we have already
mentioned earlier in this book, from the appearance of eukaryotic cells and their
organelles, the patterns began to change, going from organisms that were the only
known or standard form to slightly more complex organisms. The same is true for
the transition from unicellular to multicellular life forms, which has occurred more
than once throughout evolution. Organisms have evolved, and while some remain
unicellular, others have become multicellular organisms, such as animals and plants.
This shows how patterns change evolutionarily, leaving some organisms that were
once the rule as rare or less common forms.
7.2 R-E Changes Due to Nature’s Own Action 415

Suppose we continue this line of thought at another level of organization. In that

case, the same thing happens with the appearance of new species and the reduction
or spatial disappearance/extinction of others. Concerning this, in the history of life,
disturbances caused by geological, astronomical, or climatic agents have led, at
some points in history, to significant extinctions, in which many species have disap-
peared in a short time (Keller & Kerr, 2014). When a species disappears, it ends its
entire evolutionary history. Additionally, it affects many other species that have
evolved in an intimate relationship with it and, sometimes, are even dependent on it.
Some species are forced to change and sometimes even disappear along with the
species to which they are related. Countless extinct organisms, populations, and
species were also part of evolution since they left offspring that survived to repro-
duce with the same or different characteristics (Emer et al., 2019). Therefore, “evo-
lution” refers to the “changes” that were transmitted from one generation to the
next, comprising all those that took place at the morphological, physiological,
behavioral, biochemical, genetic, molecular, and ecosystemic levels (Madrigal &
González-José, 2016). These changes mean that the species and populations that we
observe today are not the same as those that were dominant in the past, and this
causes the rule to change, and the pattern species become rare species or directly
disappear. In the history of the Earth, mass extinctions, for example, repeatedly
changed the course of evolution: It was probably no accident that reptiles radiated
in the Triassic after the Permian mass extinction wiped out other groups, just as
mammals radiated in the Paleocene after the tremendous Cretaceous extinction
wiped out most reptiles (O'Leary et al., 2013; Sue, 2019).
Patterns in the abundance or existence of species change over time due to differ-
ent natural processes. In addition to significant historical events, such as the extinc-
tions already mentioned, these patterns can change due to comparatively “simpler”
natural events. An example of this may be a change in the abundance of species in
different areas of their distribution due to interactions between them or environmen-
tal factors such as climate or altitude. Then, species that are the exception in some
places could be the rule in others, sometimes even remaining as relicts in a geo-
graphical space. In the following sections, we discuss all these cases, focusing on
how nature can shape patterns over time and the evolutionary history of species.

7.2.2.1 Changes in Population According to Inhabited Space

The areas of distribution of species on the planet are not random. They evolve as
different environmental factors, such as relief, soil, climate, relationships between
organisms, and even human activity, and as a function of species evolution (Bravo,
2003). Some species have a large area of distribution on the planet, but within it,
they have a different abundance everywhere. Climate change, for example, affects
species interactions, community structure, and biodiversity and can induce signifi-
cant shifts in geographic ranges (Post, 2013; Visser, 2016). However, not all species
will respond to these changes in a similar way (Springate & Kover, 2014). When the
environment is variable and changing, species with broad global distributions will
have a more significant genetic variation that allows them to adapt to climatic and
416 7 Focusing on Dynamics: When a Rule Becomes an Exception

environmental gradients (Jump & Peñuelas, 2005). Cosmopolitan species, for

example, have a high rate of genetic diversity and high phenotypic variation, which
gives them greater flexibility to evolve in response to change, unlike species with a
more restricted geographic distribution (Lavergne & Molofsky, 2007). For example,
the common reed (Phragmites australis) has a global distribution, has high genetic
and phenotypic variation, and is found in many environments (Eller et al., 2017).
However, some populations may experience a decrease in genetic diversity during
acclimation and adaptation processes (Almeida et al., 2013). While it is unlikely for
species with high intraspecific diversity to face total extinction, they may still
undergo changes in genetic composition, leading to genetic impoverishment within
a population (Franks et al., 2014; Valladares et al., 2014). Thus, while some species
may inhabit extensive areas and adapt to heterogeneous conditions, they will have a
different abundance everywhere, so they may be expected in some places. In con-
trast, they will be rarer species in others.
In this same context, there are species that, having adapted to specific climates
better than others, are limited to regional distribution, being common only in some
environments. An example of these species is the coastal penguin Pygoscelis papua,
which inhabits the sub-Antarctic region but is not found elsewhere (BirdLife
International, 2024a). The same is true, for example, of the Andean condor (Vultur
gryphus), which inhabits South America and ranges along the Andes Mountains and
coasts of the Pacific and Atlantic Oceans (BirdLife International, 2024b). These
species, like many others, are the rule in their regional area of distribution but are
the exception in other parts of the world. Within plants, the same can be observed
for Coihue (Nothofagus dombeyi) growing in the Patagonian forests of South
America (Barstow et al., 2017) or araucaria (Araucaria araucana) of the sub-Ant-
arctic forests (Premoli et al., 2013), among many other species of regional distribu-
tion in the world.
Similarly, species adapt to various environments based on the factors mentioned
above, with some being more successful in adapting to urban areas. In cities, natu-
ral habitats undergo significant modification and alteration due to construction and
the replacement of native species with nonnative vegetation (McDonnell et al.,
1993; McKinney, 2002). This means that species with more significant adaptive
capacity benefit and can colonize urban environments or remain in them. Cities
create their microclimate, increase the average temperature concerning their sur-
roundings, and offer shelter in their buildings and various feeding possibilities.
However, they are an inhospitable habitat for most species. A small number of
animals make use of urban settlements. They are cosmopolitan and opportunistic
organisms that are generally prolific and omnivorous. These species include
pigeons (Columba livia), sparrows (Passer domesticus), rats (Rattus norvegicus),
and mice (Mus musculus), for example (Giménez, 2009). In Argentina, certain spe-
cies of scorpions, such as the medically significant Tityus carrilloi. Populations
living in urban areas of the center of the country reproduce through parthenogen-
esis and demonstrate remarkable adaptability to urbanized environments.
Consequently, their populations in cities are steadily increasing, leading to frequent
encounters with them (de Roodt, 2014). Due to their ability to adapt and take
7.2 R-E Changes Due to Nature’s Own Action 417

advantage of resources, all these species and many more can become a rule in
urban settlements and large cities. In contrast, many others that do not possess
these capabilities eventually disappear.
The variation in species abundance across different regions on the planet illus-
trates how climate, biotic interactions, environmental factors, and community
dynamics can influence the patterns and processes of species. Consequently, we can
observe that species we sometimes see as standard become rare or exceptions
according to changes in their habitat, resulting in dynamic communities throughout
their life history. In the following, we will mention two situations linked to the
reduction of something generalized to something circumscribed or restricted,
mainly by the action of nature and at the level of space and group, respectively.

7.2.2.2 Climate Relics

Closely linked to the previous point, there are cases where climate change (natural
or not) results in isolated populations called climatic relicts, which have been frag-
mented by environmental changes and habitat loss caused by climate (Hampe &
Jump, 2011; Woolbright et al., 2014). These climatic relicts form natural laborato-
ries regarding the dynamics of the populations involved (ecology) and their evolu-
tion. They preserve ecological and evolutionary histories that can span millennia.
They make it possible to study how environmental change affects species and popu-
lations over the long term. However, they can also be beneficial for studying interac-
tions between species and how they can affect communities and the ecosystem, for
example. The main characteristic of these relicts is the lack of gene flow between
them, which causes their low genetic differentiation. In turn, within relicts, natural
selection and genetic drift also act by decreasing genetic variation within popula-
tions (Woolbright et al., 2014).
In these relicts, the abiotic environment governs population patterns to a greater
extent. However, there may also be an influence on biotic interactions. Competition
(Ejankowski, 2010), predation (Castro et al., 1999; Hampe & Bairlein, 2000),
pathogen infection (Linares et al., 2010), herbivore action, and invasive species can
have negative or positive consequences at small population sizes. For example, it is
known that aspens (Populus spp.) adjacent to an isolated spring, all trees may be
clones of the same genotype, having survived through asexual reproduction
(Woolbright et al., 2014). This low genetic variation means they have little resis-
tance, for example, to pathogens or herbivores (Busby et al., 2013), and the popula-
tion may decline rapidly in the event of an attack. As a result of this characteristic,
species found in climatic relics can sometimes be common in some sites but rare or
even absent in others. In addition, the lack of genetic variation may cause species to
disappear due to biological interactions in relicts and thus become rare species even
within the same relict.
Climate change is one reason that biotic interactions are changing and may influ-
ence the ability of species to adapt to new habitats and persist (Gilman et al., 2010).
For example, glacial relict populations of the shrub Dryas octopetala are the only
418 7 Focusing on Dynamics: When a Rule Becomes an Exception

hosts of ectomycorrhizal fungi in the Burren steppes of western Ireland (Harrington

& Mitchell, 2002; Liston & Harrington, 2012). These fungi are typically associated
with forest trees (e.g., Scots pine Pinus sylvestris), which are not found in that cli-
matic relict (Roche et al., 2009). The novel associations of the fungus with shrubs
in glacial relicts may explain the persistence of the fungus, which would otherwise
have become extinct. Variations in this community may be explained by soil and
vegetation characteristics that allowed them to live in atypical habitats (Schechter &
Bruns, 2008). However, it could also be influenced by genetic variation in the host
plant. If this is the case, the population could be a geographic mosaic (Smith et al.,
2011; Thompson, 2005), creating natural laboratories that could reveal how climate
affects genetically controlled interactions among species, which not only shape
communities and ecosystems in changing environments but also drive evolution,
diversification, and speciation (Woolbright et al., 2014). Indeed, climate relict spe-
cies and communities exhibit unique patterns that are not observed in other areas,
enabling them to thrive and dominate in their specific habitats, even though they
might be considered exceptions in other regions.

7.2.2.3 Relictual Species

The concept of “relictual” species refers to those species that were once abundant in
a more extensive distribution area and became confined to smaller areas (Fig. 7.1).
They are generally species that are in a state of regression. This regression may be
caused by climatic changes, competition, or interactions with other species and is
called biogeographic relicts (Lomolino et al., 2006). An example is the relict for-
ests, which remain vestiges of more extensive areas than they were previously occu-
pied. However, there are also taxonomic relicts, species with a few survivors of a
once very diverse taxonomic assemblage. The two forms sometimes coincide, for
example, in the case of misnamed “living fossils,” which we will discuss below.
Relict species, in general, are often valuable for evolutionary biology and bioge-
ography to help address extinction issues. Within molecular phylogeny, they allow,
for example, the estimation of extinction rates (Crisp & Cook, 2009; Nee et al.,
1994). In addition, these species allow us to identify the characteristics that make
them survive extinction and model niches according to environmental change
(Graham et al., 2006; Grandcolas et al., 2011). However, in tune with the theme of
this book, they are representatives of larger groups that have partially disappeared,
so they give us information on the diversity of the past of existing groups in terms
of ancestral species (Assmann et al., 2010; Fjeldså & Bowie, 2008; Pellens &
Grandcolas, 2015). This characteristic will become increasingly important in the
coming decades as the current major extinction crisis will make it necessary to con-
serve species for ecological services and as representatives in the tree of life
(Grandcolas et al., 2014).
One example of a relictual species is termites of Mastotermes darwiniensis, the
only living representative of the family Mastotermitidae (Legendre et al., 2008).
The family is now restricted to northern Australia. They are closer to cockroaches
7.2 R-E Changes Due to Nature’s Own Action 419

Fig. 7.1 Distribution of two European bison species. (a) Holocene (Bison priscus only) range map
in orange. (b) Historical range (B. bonasus range in the high middle ages in green). (c) Relict
B. bonasus populations in the twentieth century in red

and share interesting morphological and social characteristics. For example, they
care for their young and feed on dead wood (Donovan et al., 2000; Legendre et al.,
2008). In addition, they lay an egg mass similar to the ootheca of cockroaches, their
reproductive individuals are winged, and their symbiont bacteria are similar to those
found in cockroaches. The current distribution of these termites can be interpreted
as a worldwide extinction of the family throughout its former distribution, except in
Australia. Fossils have been found dating back to the Eocene, indicating that they
were present on almost all continents (Grandcolas et al., 2014). This is a clear exam-
ple of a species that went from being the rule, distributed almost everywhere in the
world, to being the exception in only one restricted area.
Many thermophilic organisms are also relevant examples of relictual species.
They survived the last ice age in relatively small refugia, such as, for example, on
the peninsulas of southern Europe. During interglacial periods, these species were
able to colonize large areas. Thus, many temperate species that are widespread
today existed as small relict populations only a few 1000 years ago (Schmitt, 2007).
In contrast, many cold-adapted species show evidence of formerly broad distribu-
tions followed by severe range restrictions during postglacial warming. Butterflies
of the species Proclossiana eunomia and Lycaena helle are examples of the latter.
420 7 Focusing on Dynamics: When a Rule Becomes an Exception

They are currently found only in high-altitude mountains and more northern lati-
tudes, coinciding with distinctive genetic groupings (Habel et al., 2009a). Although
these species today are restricted to small areas, they may have the potential to
recolonize larger areas if the climate cools again (Habel et al., 2009b).
Range restrictions and expansion are also known to result from human-mediated
landscape changes. For example, in central Europe, forests covered large areas
before deforestation. Especially during the Middle Ages and early Modern Times,
these extensive forests were degraded, leaving only small remnants. After the estab-
lishment of modern forestry and changes in land use, forest cover increased again
enormously. The old forest retains preserved plants and animals. Some of them still
show relict-like distributions, but others were able to recolonize large areas
(Assmann, 1999; Drees et al., 2008).
These examples demonstrate once again the historical dynamic changes in popu-
lations and species. Some species restrict their distribution and are even representa-
tives of larger groups that have disappeared due to climatic and ecological changes.
Some of them may even recolonize previously inhabited areas. Thus, pattern spe-
cies soon become exceptions, limited only to certain places or only to certain spe-
cies of a larger group that may have become extinct.

7.2.2.4 Great Extinctions: From R to E to Disappear

As we outlined at the beginning of the chapter, mass extinctions are another case of
the rule-exception dynamic. At a specific moment, some species were the pattern or
the rule and became the exception or even ceased to exist. Throughout history, the
planet has experienced six major mass extinctions caused by various contingencies,
including volcanism, epidemics, interspecies competition, and climate change.
These catastrophic events have led to significant losses of biodiversity and have
played a crucial role in shaping the course of evolution on Earth. Mass extinctions,
in general, were terminal extinctions in which more than half of the species that
were present at the time disappeared without leaving descendants (Keller & Kerr,
2014). These extinctions marked a change in the composition of the communities of
species that inhabited the Earth, either by the disappearance of some or the evolu-
tion of others.
In the Ordovician-Silurian period, two major extinctions occurred, resulting in
the second-largest extinction of all occurring on Earth (Bond & Grasby, 2020). At
that time, the most complex organisms were marine, and more than 100 biological
families became extinct, representing 85% of the species. The groups that suffered
the most significant consequences were brachiopods, bryozoans, trilobites, con-
odonts, and graptolites. Due to the disappearance of large invertebrates, the first
fishes occupied empty biological niches until reaching more evolved life forms,
such as amphibians, reptiles, or even mammals (Sheehan, 2001).
After this great extinction, during the Devonian, there was a significant diversi-
fication of fish, a remarkable growth of coral reefs, the first trees appeared, and the
first tetrapods conquered the land. The next mass extinction had more significant
effects on the seas at tropical latitudes. The organisms that inhabited the planet’s
7.2 R-E Changes Due to Nature’s Own Action 421

temperate zones suffered the most significant effects (Hallam & Wignall, 1997).
There was biodiversity loss because speciation rates were low, and many species
almost disappeared. Coral populations declined considerably, with almost 85% of
their species becoming extinct (Hallam & Wignall, 1997). Ninety-seven percent of
shallow-water rugose corals disappeared, as did 60% of deeper-water corals and
80% of tabulate corals. Calcareous algae also disappeared, as did different species
of jawless fish, placoderms, cephalopods, ostracods, and sponges, among others.
The species that remained after this extinction began to repopulate the planet until
the Permian–Triassic period, when what is commonly known as “The Great
Permian Extinction” or “The Great Mortality” occurred. This was the most exten-
sive extinction ever to happen on Earth. Ninety-five percent of marine species and
70% of terrestrial vertebrates have disappeared (Benton, 2003; Sahney & Benton,
2008). After this event, life took a long time to recover. There is no certainty on the
possible causes of this extinction. The hypotheses suggest extreme volcanism, the
impact of a giant asteroid, or the release of gases from the bottom of the ocean.
Nevertheless, it is believed that there must have been a convergence of several fac-
tors that caused this level of species disappearance, making this event the most
devastating and significant destruction of the biosphere ever known (Song
et al., 2013).
After this significant mortality, reptiles and amphibians began to populate the
continent. The first dinosaurs, pterosaurs, and crocodylomorphs appeared. The first
small mammals and different terrestrial arthropods also appeared. Pteridophytes,
cycads, and conifers predominated among the vegetation. In the aquatic environ-
ment, ichthyosaurs, plesiosaurs, nothosauroids, and placodonts diversified, as did
many groups of fish. Many invertebrate groups also radiated in this period, such as
corals, dinoflagellates, brachiopods, and mollusks (Abdala & Ribeiro, 2010; Ogg
et al., 2004; Sue & Fraser, 2010).
During the Triassic-Jurassic period, there were substantial volcanic eruptions
coupled with climatic fluctuations, sea level changes, and anoxia (Hautmann, 2012).
Once again, these factors significantly impacted life on land and in the oceans.
Approximately 20% of marine families, archosaurs, therapsids, and large amphibi-
ans disappeared. Many biological niches were then released, and dinosaurs took a
dominant role in the following period (Hautmann, 2012).
In the Cretaceous, a sudden mass extinction caused three-quarters of the Earth’s
animal and plant species to disappear. Except for sea turtles, crocodiles, and other
ectotherms, no large tetrapods survived (Muench et al., 2000; Renne et al., 2013).
The best-known species that did not survive this great extinction were nonavian
dinosaurs and many other terrestrial organisms, such as mammals, birds, lizards,
insects, and plants. For marine species, plesiosaurs and mosasaurs, mollusks such as
ammonites, many teleost fishes, and sharks disappeared. Many plankton species
also vanished (Jablonski & Chaloner, 1994; Renne et al., 2013).
However, this event provided new empty niches and evolutionary opportunities
for groups that could adaptively radiate and diversify into new species, particu-
larly mammals. The surviving dinosaurs evolved into modern birds. Teleost fish
and lizards also diversified (Cracraft, 2001; Longrich et al., 2015; Wilson
et al., 2012).
422 7 Focusing on Dynamics: When a Rule Becomes an Exception

Amid these mass extinctions, other events also occurred that caused a change in
the patterns of existing species on the planet. One of them was the Messinian salt
crisis, an event characterized by the accumulation of salt at the bottom of the
Mediterranean, which also included its almost complete desiccation (Sternai et al.,
2017). During the Messinian age, at the end of the Miocene, the Mediterranean Sea
was isolated from the Atlantic due to the tectonic uplift of the Betic (south of the
Iberian Peninsula) and Rifian (north of Morocco) mountain ranges. This process led
to the drying and transformation of this sea into a large salt marsh. Later, the flood-
ing of the Mediterranean by Atlantic waters through the Strait of Gibraltar ended
this crisis (Garcia-Castellanos et al., 2009). However, in response to these changes
in the natural environment, it is accepted that the Mediterranean flora and fauna
come from Atlantic species that have populated it during the last five million years
(Hsü et al., 1977; Naveh & Vernet, 1991). This invasion resulted in a change in spe-
cies patterns, where those common in the Mediterranean Sea mostly disappeared,
while Atlantic species became the new pattern in this environment.
The sixth mass extinction or Holocene mass extinction is the last extinction event
in the current Holocene period and resulted mainly from human activity. This is the
period of large megafaunal disappearance. As we saw, this extinction affected many
species, including the mammoth, the dodo, and countless others that continue to
become extinct yearly. After the last glaciation, the continents were populated by
Homo sapiens, whose activity, directly or indirectly, contributed to the extinction of
all these species. Activities such as the hunting of large animals, the transformation
of the environment by fire, cultivation, erosion, and the transport of exotic species
to new environments contribute to the extinction of species (Corlett, 2007;
Fernandez, 2015). The uncontrolled action of human beings continues and exacer-
bates at present, which is why many scientists discuss the possibility of being
immersed in the seventh mass extinction, caused in this case by uncontrolled human
action (Turvey, 2009). The planet’s current biodiversity may be reaching a turning
point in which human activity has accelerated the end of several species by destroy-
ing their habitats. More than 300 vertebrate species have become extinct since 1500,
and invertebrates have decreased their populations by approximately 45%, while the
human population has doubled (Ceballos et al., 2015). Globally, for example, pol-
linators appear to be declining sharply in abundance and diversity. The significant
problem is that the decline of affected species will have a cascading effect on eco-
system functioning, ultimately affecting human well-being (Cardoso et al., 2020).
Extinctions occurring across various evolutionary periods up to the present day
indicate the diversification of species. Some species inhabit different regions of the
planet, while others face extinction. Abundant species, at times, diminished or dis-
appeared, making room for other diversified groups. As a result, both terrestrial and
marine ecosystems underwent changes in their community composition, highlight-
ing the dynamic nature of species diversity. This exemplifies the topic discussed in
this section, where patterns are not static. Throughout history, patterns change,
allowing new species to emerge, while others vanish or decrease in number, creating
opportunities in ecological niches. Hence, the evolution and interactions among
organisms, the abiotic environment, and human influence maintain the possibility
for rules to become exceptions in the history of life on Earth.
7.2 R-E Changes Due to Nature’s Own Action 423

7.2.2.5 Living Fossils

Regarding the previous point, certain species have survived mass extinctions and
exhibited gradual evolution, closely resembling their ancestors in overall phenotype
(Beierkuhnlein, 2007; Lomolino et al., 2006). These are the so-called living fossils,
an incorrect designation since, by definition, a fossil is not alive (Fig. 7.2). However,
to simplify things, we will take this name. They are organisms documented in the
fossil record and are now represented by a few extant species in which the charac-
ters have been “fossilized”; i.e., they have remained without much change over time
(Grandcolas et al., 2014). They are not identical, as many of these organisms change
in some characteristics from their ancient versions (Cavin & Guinot, 2014). Living
fossils are unique lineages characterized by stable morphology, low taxonomic
diversity, and some rarity (Werth & Shear, 2014). Their apparent lack of diversifica-
tion and stability suggests that they have adapted so effectively that they reduced the
need to exhibit phenotypic changes in response to environmental change (Kin &
Błaźejowski, 2014). Consequently, these species can serve as valuable long-term
evolutionary witnesses. There is no universal consensus on which lineages consti-
tute genuine living fossils, but some universally recognized cases include Ginkgo
tree, Tuatara, lungfishes, coelacanths, and nautiluses (Ward, 1984; Werth &
Shear, 2014).

Fig. 7.2 Ancient beginnings of living fossils. The silhouettes show when each “living fossil” first
appeared. Every group seen on this tree is still alive today
License: own creation. Free images from https://www.phylopic.org
424 7 Focusing on Dynamics: When a Rule Becomes an Exception

Ginkgo (Ginkgo biloba) is known to have existed since the Jurassic period, 170
million years ago. However, there is no complete understanding of its evolution
because of a gap in the fossil record of more than 100 million years. Ginkgo trees
grow in China, Korea, Japan, Europe, and the United States. They can be up to 30
meters tall, 15 meters in circumference, and can live up to 1000 years. They were
the first plants to grow back after the nuclear bomb was detonated in Hiroshima,
with no signs of genetic mutations. Because of this resilience, these trees are fre-
quently planted in large cities such as New York and Tokyo (Jacobs & Browner, 2000).
Another example mentioned above is the coelacanth (Latimeria spp.), which
inhabits specific sectors of the Indian Ocean. This lobe-finned fish represents an
early evolutionary deviation from the lineage that led to terrestrial vertebrates and is
of great scientific interest (Amemiya et al., 2013). It has changed very little in
appearance from the fossilized coelacanths of the Cretaceous (aprox. 145.5 to 65.5
million years ago) (Cavin & Guinot, 2014). The coelacanth’s ancestors evolved
more than 400 million years ago, surviving the movement of continents and the
great extinction that ended with the dinosaurs. They are very slow-evolving fishes
but may be the key to elucidating the rate and mode of evolution from fish to tetra-
pods. The knowledge of their genome is essential to elucidate how ancestral aquatic
vertebrates evolved into terrestrial animals (Nikaido et al., 2013). Additionally, in
the aquatic environment, we still find sharks and rays, whose anatomy and life
forms appeared in the Devonian (Peristeraki & Megalofonou, 2007). Like the coel-
acanth, these fish have retained their morphology for approximately 350 mil-
lion years.
Another remarkable living fossil is the nautilus (Nautilus pompilius), the only
cephalopod mollusk that retains a true external shell. Currently, this feature is a
rarity in the class Cephalopoda. In the basal groups of this class, having an exter-
nal shell was the norm, but it was gradually abandoned in favor of improved
hydrodynamics. Consequently, certain groups evolved with reduced and light-
weight internal shells, such as cuttlefish and squid, while others completely lost
their shells, such as octopuses (which granted them better maneuverability in ben-
thic environments, e.g., for hiding and ambushing prey) (Ruppert et al., 2003).
Nautiloids once constituted a diverse and widespread group within the mollusks,
nearly becoming extinct at the end of the Permian and Cretaceous (Teichert &
Matsumoto, 1987), leaving only a lineage comprising some living Nautilus and
Allonautilus species. According to paleontological evidence, the genus Nautilus
has existed for at least 100 million years without any apparent significant morpho-
logical changes (Ward, 1984). Nautiloids are a model for paleontologists, as their
condition makes it possible to infer the biology of a large group of external-shelled
cephalopods known only from fossil records (Harvey et al., 1999; Saunders &
Landman, 2010). Unlike other living fossils, nautiloids now inhabit a relatively
large area in the Indo-Pacific region, although they are difficult to observe in
nature (De Angelis, 2012).
Tuatara (Sphenodon spp.) is also an example of a living fossil in the terrestrial
environment. It is the only representative of the early-branching sphenodont-­
lepidosaur group and may be evidence for the antiquity of the New Zealand biota
7.3 Human-Induced R-E Changes over Nature 425

(Jones et al., 2009). However, this genus shows a high rate of molecular change,
inferred from comparisons between subfossils and modern individuals (Hay et al.,
2008). Another example of an animal that has changed little or not over millions of
years is the platypus (Ornithorhynchus anatinus). This monotreme mammal is one
of the few descendants of a common ancestor that diverged from mammals 150 mil-
lion years ago. It retains primitive features such as its leathery eggs and the absence
of nipples, unlike more evolved mammals. Skulls of ancestors similar to platypuses
have been discovered dating from the Cretaceous period. Like those mentioned
above, these animals have a prolonged evolution, causing them to retain their
appearance for millions of years, making them almost an exception (Chimento
et al., 2013; Komblihtt, 2009).
In arthropods, many insects are also ancient inhabitants of our planet, with cock-
roaches standing out among the best-known. They appeared more than 300 million
years ago and show morphological characteristics that have not changed much
since. These insects have adapted to all environmental changes and were even the
first animals found undamaged after nuclear explosions (Copeland, 2003). Just as
hardy and ancient are scorpions, which emerged along with other arachnids and
mites 350 million years ago (Gomes & Gomes, 2015).
The list of “living fossils” is extensive, but the aforementioned cases illustrate
how species that were once widespread in their habitats millions of years ago are
now apparent exceptions, rarities, and, in some cases (e.g., the coelacanth), even
considered previously extinct. All these examples of once dominant groups become
rarities, as discussed in this section, provide valuable insights into the patterns of
species diversification on our planet and the changes that various groups may
undergo due to interactions between species and their environment.

7.3 Human-Induced R-E Changes over Nature

7.3.1 Reduction or Loss of Changing Capacity

in Living Organisms

7.3.1.1 In Animals and Plants: The Effect of Artificial Selection

and Associates

Human beings are indeed impeding the normal course of evolution in numerous
living organisms, particularly in groups inhabiting “hot spots” or facing endanger-
ment. This interference stems from various actions, such as artificial selection,
genetic manipulation, breed manipulation, direct or indirect impacts on extinction,
climate change, and the introduction or control of species. Specific cases presented
below will show that humans affect living organisms through these activities and
remove their chances of evolving in time and form in the face of these scenarios
imposed by them. It is interesting to discuss this point because it may be central and
globalizing for many of the ideas in the book.
426 7 Focusing on Dynamics: When a Rule Becomes an Exception

Darwin, in The Origin of Species, already saw a parallelism between natural

evolution and artificial evolution carried out by humans. Thus, examples of different
breeds of pigeons with different attributes are sketched (Darwin, 1859). Since the
beginning of time, humans have selected organisms for their benefit. As mentioned
earlier in Chap. 6, first in a more natural way, with humans functioning as any other
animal in the ecosystem, but then at the time of a more stable settlement, they began
to exert a much higher selective pressure, to the point of totally modifying some
organisms. The most significant pressure was on organisms linked to the basic
requirements of food and shelter. Humans selected the crops they preferred and
cultivated the varieties that gave them the highest yields. The original species that
were the rule at the beginning of nature declined in abundance or ceased to exist to
give way to new species or varieties. A unique example is that of maize, where the
original species of maize called perennial teosinte (Zea perennis) presented a fruit
with a tiny corn cob with four rows of kernels. This original variety, which was the
rule in the past, was modified over time until it reached the current corn cob. As we
said in Chap. 6, the current crop is a hybrid (Zea mays) with a much larger corncob
and multiple rows of larger kernels. A similar situation occurred with cattle. It is
impossible to compare the musculature, milk-producing capacity, or wool produc-
tion of the current varieties to the original from which they descended. Essential
species that would not naturally exist, such as mules, were also created for work.
Beneficial associations were also generated, for example, with wolves, which, when
selected, gave rise to modern dogs.
Certainly, while certain organisms experience favorable selection pressures, oth-
ers have been significantly threatened for various reasons. Some of these reasons
include fear factors (e.g., snakes and spiders), associations with diseases or ailments
(e.g., rats), superstitions (e.g., cats during medieval times associated with witch-
craft), environmental modifications (e.g., deforestation affecting forest species, as
discussed in item 7.2.2.3), or indiscriminate hunting (e.g., American bison).
Precisely, as already mentioned, a large-scale example of indiscriminate hunting
happened in the Quaternary with the mammalian megafauna. Hunting selection
pressure by humans and other factors favored the extinction of this large group of
animals (Diamond, 1989; Brook & Bowman, 2004; Bulte et al., 2006) (see item
7.2.2.4). Indeed, some Australian species face the detrimental effects of human
neglect when placental mammals are introduced through expeditions and coloniza-
tion voyages (Woinarski et al., 2015). This introduction of foreign species had sig-
nificant impacts on the local ecosystems, leading to the decline and endangerment
of certain native species in Australia. As mentioned elsewhere in the book, the intro-
duction of exotic species is a phenomenon that has shaped the population dynamics
and environment of certain regions quite a bit and is generally directly related to
human activity. The introduction of exotic species is one of the greatest threats to
biodiversity in the world. It has been noted that a small number of species are slowly
replacing species that are threatened by human activities. Historical empirical data
show what happens when there is a widespread invasion of organisms. South
America was a relatively isolated place until the Pleistocene. After the formation of
Central America, massive migration and invasion of many organisms began,
7.3 Human-Induced R-E Changes over Nature 427

replacing the South American natives. In fact, approximately half of the current
South American mammals originated in North America (Goin et al., 2012; Marshall
et al., 1982).
Some groups of organisms are common and declining due to human activities. In
many cases, the dominant or common groups are threatened by specific changes or
pressures that can reduce their numbers or completely extinguish their population.
We have seen examples throughout the book where fish replaced groups such as
Paleozoic cephalopods in the marine ecosystem. If we analyzed it in sequence,
cephalopods were dominant in the environment and were the rule at that time.
Gradually, fish appeared, which were evolutionarily better, and displaced them from
the environment until certain groups became extinct, and the number of the group in
general decreased notably. Today, we can see something similar where the human
being is a crucial participant. With their activities, humans shape the environment,
and many organisms are affected and cannot adapt well or fast enough. Hence, they
decrease their numbers, become extinct, or have the potential to do so. As we recog-
nize the significant role of human activities in causing extinction, the concept of
species conservation has become increasingly prevalent (Akcakaya et al., 2004).
Unlike in the past, there is now a greater emphasis on the importance of conserva-
tion efforts. However, while striving for a more comprehensive approach to conser-
vation by encompassing numerous groups and species, humans tend to prioritize
certain species known as “charismatic” species, which are more beloved (Colléony
et al., 2017; Ducarme et al., 2013). Indeed, the selective pressure exerted by humans
becomes favorable for certain species that would otherwise face natural extinction
(Courchamp et al., 2018). The giant panda (Ailuropoda melanoleuca) serves as a
clear example of this phenomenon. This species, which might have already disap-
peared in the wild for various reasons, continues to exist thanks to extensive human
efforts, economic contributions, and technological advancements dedicated to its
conservation.
Another example of species being selected by humans and linked to scientific
and technological advances is the controversial GMOs or genetically modified
organisms. These organisms have alterations in their genome, where genetic mate-
rial from another organism has been introduced (Husby, 2007). There are currently
many examples linked to consumption by the human population itself. In nature, for
example, if we consider crops or livestock, we find that modified organisms are
becoming the rule, and 100% “natural” organisms are slowly becoming the excep-
tion. GMOs have become organisms with attractive attributes (Hug, 2008). They
present, for example, resistance to insects (Edgerton et al., 2012; Jouanin et al.,
1998) and herbicides (De Greef et al., 1989; Duke, 1998), tolerance to different
types of stress (Bhatnagar-Mathur et al., 2008), and increased yield potential
(Edgerton et al., 2012) and can be used as bioreactors to produce various therapeutic
agents (Houdebine, 2000; Jänne et al., 1998), among other outstanding characteris-
tics. However, with these potential benefits come many concerns associated with the
properties of the modified organisms, the possibility of spreading the transgenes to
other organisms, and the potential problems of their release into nature (Rastogi-­
Verma, 2013). A case that draws attention and is directly related to genetically
428 7 Focusing on Dynamics: When a Rule Becomes an Exception

modified organisms is the monopoly of seeds by large multinationals. This phenom-

enon can be cited as a change from rule to exception. In the old days, the rule was
to be able to obtain and sow the seeds that the producer wanted. However, now, the
rule in many places is that the producer must buy or “ask permission” from the
multinational to produce a crop. We must try to make this type of bio-monopoly the
exception rather than the rule (see Kloppenburg, 2014).
We will now look at some key and well-known examples of groups that are
affected by human activity and, as a result, are seeing their numbers decimated with
the potential risk of extinction. This is what we call in this book a change from rule
to exception due to human activity.

Global Pollinator Crisis

Pollinating insects play a crucial role in providing essential ecosystem services that
enhance and stabilize global crop production (Klein et al., 2007 in Vanbergen &
Initiative, 2013; Zayed & Packer, 2005). As discussed in Chap. 6, pollination is the
primary process through which plants achieve reproduction. This vital ecosystem
service is crucial because plants, unlike animals, cannot move to seek mates and
thus rely on pollinators to facilitate their reproduction. Among these pollinators,
animal pollinators, particularly arthropods, play a critical role in ensuring success-
ful pollination. There are now many studies showing how various types of pollina-
tors have been declining in number in recent years, both locally and globally
(Steffan-Dewenter et al., 2005; Potts et al., 2010; but see Ghazoul, 2005). Much has
been discussed about this. The facts confirm this pattern, a decrease in the diversity
and abundance of pollinators, mainly arthropods. If this process accelerates, we will
discuss a change from rule to exception with potentially catastrophic results
(Steffan-Dewenter et al., 2005). This decline has a substantial impact on plant-ani-
mal interactions. All pollinators are affected, especially butterflies and bees. Bees
are particularly haplodiploid and have genetic conditioning that predisposes them to
extinction (Zayed & Packer, 2005).
Human activities are a significant driver of change, leading to accelerated rates of
evolution and extinction, resulting in the loss of biodiversity (Cane & Tepedino,
2001; Vanbergen & Initiative, 2013). One of the most cited causes of these changes
is the intensification of land use for agricultural activities, often associated with the
indiscriminate use of pesticides that can harm both crop pests and vital pollinator
species. Climate change also contributes to environmental issues, causing habitat
alterations and species interactions, potentially leading to the decline of some spe-
cies (see below). Additionally, the decline of pollinators is associated with the spread
of exotic species and the emergence of pollinator diseases, pathogens, and parasites.
The complex interplay between the mentioned pressures, biological processes,
and scales contributes to an overall decline in arthropod pollinators in natural eco-
systems (Vanbergen & Initiative, 2013). This decline can affect various animal spe-
cies that depend on plant production, including humans. For instance, reduced
pollination can lead to increased inbreeding and inbreeding depression, which
7.3 Human-Induced R-E Changes over Nature 429

plants typically strive to avoid. Self-incompatible plants may suffer from blocked
stigmas due to pollen from neighboring related flowers (Waser, 1978), which can
accelerate pistil senescence (Scribailo & Barrett, 1994). These effects ultimately
impact fruit and seed production.

7.3.2 In Humans: Reduction of Human Integration

to Natural Dynamics

Following the reasoning presented in the previous point, we can observe that, with
the exception of certain tribes or Western groups that embrace a more ecological
lifestyle, humans, as a species, have disrupted the natural “continuum” to which
they once belonged. Human activities now exert control and modification over
rhythms and natural processes, resulting in humans no longer being merely a part of
the ecosystem and nature. Instead, they have become a dominant and invasive spe-
cies that poses a threat to nature itself.
Before the establishment of towns and cities, humans functioned as animals
within the natural framework of the ecosystem. However, as humans settled, they
began to distance themselves from this natural setting and embarked on modifying
the environment to suit their needs. Over time, human activities evolved toward
dominating and significantly altering nature, particularly with the advent of the
Industrial Revolution. As evident from stratigraphic markers in sediments, humans
have left a distinct mark that differentiates this new era from the Holocene (Waters
et al., 2016). This epoch’s inception can be traced back to the emergence of agricul-
ture and deforestation. Other pivotal milestones in human history include the
exchange of species following the conquest and colonization of America, the onset
of the Industrial Revolution, and, presently, the exponential growth in the human
population.
Each of these milestones represents a significant departure from stability, often
transforming exceptions into the norm. Globally, this process can be understood as
the breaking of the rule that humans are just one of many regular organisms. Humans
have become the sole species capable of generating changes of such magnitude on
the planet, fundamentally altering ecosystems and the global environment.

7.3.2.1 Toward a More Artificial Human Species?

It has become increasingly uncommon to find individuals who are completely “nat-
ural”—that is, without any prostheses, surgeries, repairs, grafts, implants, or foreign
bodies within their bodies. This characteristic extends even to various animal
groups, including those of economic importance or those under conservation efforts,
which might lead to a situation described as “synthetic biodiversity conservation”
(Piaggio et al., 2017). In this scenario, future instances of untreated or nongeneti-
cally manipulated specimens may become rare.
430 7 Focusing on Dynamics: When a Rule Becomes an Exception

The advent of technology has played a significant role in advancing practices and
manipulations that were once only seen in science fiction novels. Especially in the
field of medicine, these technological advancements have allowed humans to live
longer, which, in some ways, puts additional pressure on nature. This is because a
larger population of longer-lived individuals may necessitate increased resource
consumption and pose new challenges for the environment.
Indeed, the trajectory of medical advancements and genetic technologies sug-
gests that in the not-too-distant future, virtually every human being may experience
some form of disease or covert ailment that has been addressed from birth or at an
early age. This means that not only individuals with well-known conditions such as
diabetes, allergies, or immunodeficiencies will be affected, but there will likely be
no lineages of individuals who can be considered 100% healthy in a strictly pure
sense. The growing utilization of organ donation and “mixed” tissues (e.g., pig +
human) due to the scarcity of donors may lead to a rarity of individuals who have
never received a “mixed” organ in certain regions (e.g., large cities in developed
countries) during their middle to third age. Consequently, in the future, finding a
naturally born individual, including newborns, might become uncommon.
However, in preventive medicine, we can say that it is rare to find humans who
have never been vaccinated with inactivated viruses or bacteria or their inactivated
antigens for certain mass diseases, such as poliomyelitis, tuberculosis, and smallpox.
Until a couple of decades ago, this practice was nonexistent and later became rare
(e.g., during the early days of health plan application). Over time, it has progressively
become the norm, even explicitly mandatory in the childhood immunization sched-
ule. If it continues to remain rare, it may be limited to countries and regions with a
low socioeconomic level. This persistence suggests that a problem that should have
been eradicated is still being maintained due to socioeconomic issues. However, in
developed countries, anti-vaccine movements profess the often conspiratorial ideol-
ogy that vaccines are harmful. These movements often rely on erroneous premises
and sometimes lack a thorough understanding of how vaccines actually work.
However, there is also some secrecy and misinformation from different actors directly
linked to health, which weave a curtain that facilitates these conspiratorial beliefs.
These ideas can generate the reappearance of many diseases known to have been
eradicated or targeted for eradication thanks to vaccines (see Hinman, 1999; Kayser
& Ramzan, 2021). This movement can favor diseases thought to have been dimin-
ished or eradicated or even the infamous COVID-19 to reappear or perpetuate,
becoming a rule again. Currently, there is a unique phenomenon where the rule is to
read the news that appears on social networks or comments from influencers or the
press and leave aside data and scientific facts consensual by most scientists. This
change from rule to exception is hazardous to cultivate. This fact is superbly cap-
tured by the movie “Don’t Look Up” from 2021. Returning to diseases, this disbe-
lief is a phenomenon that indirectly generates a change in disease dynamics. The
incidence of diseases can be higher, as we said, because of beliefs that go against
scientific facts that have been studied and proven but that, as with almost everything
in science, we cannot assure 100%. Indeed, scientific studies should also be rigor-
ous and have no background interest, which honestly often are utopies and favor
7.3 Human-Induced R-E Changes over Nature 431

even more conspiracy scenarios. These practices leave the substrate ready for dis-
ease variants to occur. Any of the mutated strains of the virus can transform from
local exceptions to potential pandemics with the capacity to reinfect the population
worldwide and generate isolation, psychosis, and general discomfort. We have the
tools to avoid this; vaccination is the only and most powerful. Suppose we add anti-
biotic resistance and the appearance of mutant agents of these diseases. In that case,
the conditions could turn from exceptions to potential rules, and the situation would
become even more complicated.
The phenomenon of increasing resistance to antibiotics by bacteria is of great
concern. This characteristic, among other things, is generated by self-medication
and the abuse of antibiotic substances, even for conditions that do not require their
use, such as a viral infection. The rule is that antibiotics are potent agents for treat-
ing bacterial infections. However, developing effective antibiotics is becoming
increasingly challenging, and their action may become exceptional in the coming
years. Imagine a person falling off a bicycle, scraping his knee, becoming infected,
and after a while dying from a bacterial infection that would be easily treated today.
This situation shows a complicated future we would want to avoid reaching.
Fortunately, RNA therapies are being developed that will probably replace antibiotic-­
based therapies (Mourenza et al., 2022; Vogel, 2020).
Additionally, currently, with the demands of everyday life and added to a large
number of activities to maintain and strengthen the body, there is an increase in the
consumption of vitamin supplements and steroids that improve people’s perfor-
mance. This practice was perhaps uncommon in the past, and all these nutrients
were incorporated in smaller amounts through food (Kaebnick, 2013). Today, it is a
gigantic industry that also helps to generate artificial humans that are starting to
become the rule. Another stepping stone related to superpeople generation is the
possibility of modifying genes through gene therapies to generate a desirable physi-
cal attribute.
In summary, the examples presented in this discussion highlight how human
activity directly or indirectly leads to environmental changes. These changes, in
turn, cause certain phenomena or organisms that were once common to alter their
structure or abundance, becoming rare and exceptional. This dynamic of change and
species replacement has been a natural occurrence on the planet for millions of
years, but in this particular case, it is driven by human actions rather than natural
processes, often occurring at an unprecedented speed.

7.3.3 Toward the Extinction of Organisms as a Massive

Phenomenon (“Folding” Life Diversity)

We have already seen that extinction processes have occurred due to abiotic natural
causes (e.g., various cataclysms, gradual modifications of the atmosphere, and ter-
rain) and biotic causes (e.g., interspecific competition) throughout the evolutionary
history of organisms. However, we have already addressed the terrible role that
432 7 Focusing on Dynamics: When a Rule Becomes an Exception

human activity has played, directly (hunting, fishing, or uncontrolled deforestation,

for example) or indirectly (environmental pollution and climate change), on many
of the world’s ecosystems. Throughout the history of mankind and more strongly
marked after the Industrial Revolution, we know how various human events have
implied a radical alteration for local communities or even the destruction of the
environment (Fig. 7.3a, b). Since ancient times, the environment has been modified
for forestry, livestock, and agriculture. Indeed, humans have had a significant impact
on the environment, landscapes, and diverse range of species inhabiting our planet.
This influence can be observed across the entire animal kingdom. Among verte-
brates, birds and mammals have been particularly affected by human activities,
often experiencing near “annihilation” levels in numerous cases. For example, since
human colonization, it is estimated that approximately 1800 species of birds have
become extinct (Steadman, 2006). In addition, records on extinctions of large mam-
mals, birds, and reptiles date back to the seventeenth century, with species such as
the dodo (Raphus cucullatus), the Steller’s sea cow (Hydrodamalis gigas) and the
giant tortoise (Cylindraspis peltastes) (Ceballos et al., 2015). Reptiles, amphibians,
and fish have been documented as extinct since the twentieth century (Baillie &
Cokeliss, 2004). Even some species that are not currently threatened face the wide-
spread disappearance of certain populations, which may be a prelude to extinction
at the species level (Ceballos & Ehrlich, 2009).
From the perspective of the book, in the case of the extinction of a living species
by direct (e.g., hunting) or indirect human action (e.g., pollution, introduction of
exotics), we would be talking about a change from Rule to Rule, i.e., from “the spe-
cies being present” to “the species no longer being present.” This transition from
Rule to Rule is the extreme case. However, an intermediate case would be species

aa b b

Fig. 7.3 Rate of extinction in bird species produced by man. (a) Number of species extinct over
time. (b) Extinct species per year and extinction rates. (Based on https://evolution.berkeley.edu/
mass-­extinction/the-­earths-­sixth-­mass-­extinction/; from Pimm et al., 2006; Barnosky et al., 2011)
7.3 Human-Induced R-E Changes over Nature 433

“in danger” of extinction, where their numbers are reduced to values of simple
exceptions or rarities, either worldwide or in certain regions. In any case, it is
because they are interrelated that they are presented here and not in the Rule-Rule
chapter since it is a transition from Rule to Exception and then from Rule to Rule.
We must not lose sight of the fact that everything is ultimately closely linked (e.g.,
if there was an intruder species that now occupies the niche of the native species, as
we saw in the previous chapter, essentially, it went from Exception to Rule).
We will now review some of these witness cases, many of which are well-known.
The objective is to highlight what we mean when we say that humankind is rapidly
and systematically turning the drastic reduction of entire groups of living organisms
into a rule, even up to the total disappearance not only of one species but of several.

7.3.3.1 Effect of Deforestation, Hunting, and Fishing

When the balance ruling in ancient human communities for these activities was
abandoned, human occupation of natural environments and land-use inevitably
changed and led to a reduction in the number of species (Ceballos & Ehrlich, 2002;
Dirzo et al., 2014). Even pristine environments have not been immune to species
loss, primarily driven by various human exploitation activities, be it for subsistence
or commercial purposes (Peres & Palacios, 2007; Young et al., 2016). For instance,
the Amazon rainforest and the tropical rainforests of Southeast Asia have experi-
enced significant species loss due to activities such as deforestation and habitat
destruction (Donald, 2004; Koh & Wilcove, 2007; Rudel et al., 2009). Similar sce-
narios can be observed in Madagascar, Africa, and other regions, where large areas
are rapidly disappearing as they are converted for commercial agriculture (Vieilledent
et al., 2018). Agriculture is a major cause of extinction and threatens wild biodiver-
sity (Norris 2008; Butler et al., 2007). Millions of forests and natural habitats have
been cleared for agricultural use, resulting in landscape fragmentation and soil and
water degradation, leading to the extinction of many species (Benton & Twitchett,
2003; Foley et al., 2005; Tscharntke, 2002). Sometimes, farmers even eliminate
wild species to reduce the effects of pests, predators, and weeds, which affects bio-
diversity, often leading to the eventual disappearance of plants and animals
(McNeely & Scherr, 2003).
However, certain ecosystems have remained relatively unaltered, but they have
not been immune to the impacts of activities that exploit natural resources and
endanger numerous species. In some cases, exotic species are introduced for recre-
ational activities such as hunting and fishing, leading to competition with native
species for resources and potentially displacing them. Additionally, these practices
can directly target native species, and if not properly controlled, they may contribute
to the disappearance of those species.
An example of indiscriminate hunting of a species is that of the American bison
(Bison bison), which, before the arrival of Europeans, inhabited North America.
Bisons began to be hunted for their meat, then for their skin and finally for sport.
The creation of reserves during the nineteenth century favored the survival of only
434 7 Focusing on Dynamics: When a Rule Becomes an Exception

two species currently living (Navarro, 2011). Another well-represented example is

black rhinoceros (Diceros bicornis), whose constant slaughter by hunters led to the
disappearance of at least two of its subspecies. Its horns are heavily traded in the
Near Eastern and East Asian markets, either as ornamentals or for medicinal pur-
poses (Martin, 1983; Penny, 1988). The problem becomes even worse, as the
decreasing availability of these animals by hunting greatly increases the value of
their horns. This supply and demand phenomenon creates truly catastrophic reper-
cussions for the species because all ages and sizes of the animals are now suscepti-
ble (Ashley et al., 1990; Leader-Williams, 1988). Additionally, in the northern
hemisphere, anthropogenic activity has caused the decline of up to 95% of the
extension of gray wolf (Canis lupus) populations, which were found in almost all
territories of the Iberian Peninsula (Blanco & Cortés, 2003). During the 1950s and
1960s, these populations declined due to human persecution (Valverde, 1971; Vila
et al., 1993). In 1970, the species was protected by hunting law, which was key to
its conservation (Arija, 2010). In the Southern Hemisphere, we find the same prob-
lem with many species threatened by poaching. One of these species is the jaguar
(Panthera onca) in northern Argentina. This species is becoming very depleted, and
a medium-term extinction is highly probable if the threat persists (approximately by
the year 2050). Most of these animals are killed by hunters looking for trophies or
hides (Paviolo, 2010). The same occurs with the South American tapir (Tapirus ter-
restris), which in Argentina is considered an endangered species (García Fernández
et al., 1997) due to hunting and habitat destruction and currently survives only in
some populations in the north of the country (García, 1972; Richard & Juliá, 2000).
In the aquatic environment, the same pattern can be observed due to the exploita-
tion of fisheries, which affect the abundance of fish species due to the introduction
of other fish or exotic crabs, habitat destruction, and pollution, among others
(Doadrio, 2001; Doadrio & Elvira, 2002; Nicola et al., 2013). Fish are one of the
most threatened vertebrate groups on the planet (Baillie & Cokeliss, 2004; Burkhead,
2012), and the extinction of many species occurs in a very short time span and in an
accelerated manner (Rodríguez et al., 2020). One of the main causes of this decline
is excessive and indiscriminate fishing and the lack of compliance with regulations
prohibiting capture.
The common hammerhead shark (Sphyrna lewini) is one of the most exploited
species in fisheries, sought after for its meat and even for its unique shape, as its
head is used for ornamental purposes. To protect this endangered species, specific
laws have been implemented in certain countries, such as Costa Rica and Ecuador.
Additionally, the common hammerhead shark is listed on the red list of threatened
species by the International Union for Conservation of Nature and Natural Resources
(IUCN, 2023). Other groups of cartilaginous fish, such as rays and sawfishes, are in
the same situation, and there is evidence that their extinction is a real possibility.
The golden cownose ray (Rhinoptera steindachneri), for example, is a very suscep-
tible species, as it produces one young per year and is highly affected by overexploi-
tation (Bizzarro et al., 2007; Burgos-Vázquez et al., 2019). Similarly, the sawfish
(Pristis and Anoxypristis spp.) is being driven to extinction by this cause. The sus-
tainability of the populations of these fish is only possible if mortality and the catch
7.3 Human-Induced R-E Changes over Nature 435

rate per fishery are reduced due to their capacity for recovery, given their reproduc-
tive potential (Acevedo et al., 2007).
In the Southern Hemisphere, many fish species are also strongly affected by
overfishing. One of these is the Argentine hake (Merluccius hubbsi), whose decline
occurred in a very short period of time because the current regulations did not pro-
hibit its capture (de Villalobos, 2002). Additionally, the catch of mollusks and crus-
taceans has also grown in volume in that area, much more than the catch of fish. The
Argentine squid (Illex argentinus), for example, represents 95% of the catch. This
rate of exploitation shows immediate consequences, and the estimates are for a con-
tinuous decline in fish and other organism biomass (Casal & Prenski, 2000).
All these examples show that the abundance of species is not only affected by
nature. Humankind has a crucial role in these processes. Due to exploitation, spe-
cies that were the rule in different areas of the planet have become the exception or
even disappeared. This reduction is accomplished through activities such as defor-
estation, hunting, fishing, and the degradation of natural environments. The leading
cause of the mismanagement of natural resources and the change in species from
being patterns to exceptions due to overexploitation is the lack of management poli-
cies. The measures taken concerning these exploitations can help reduce the disap-
pearance of species already in danger of extinction and thus recover some
populations. Indeed, while these measures may not fully address irreversible extinc-
tions, they can still be instrumental in mitigating the damage to species that are
experiencing declining populations. Implementing such measures can help prevent
these species from reaching the point of extinction and provide a chance for their
populations to recover and stabilize.

7.3.3.2 Effect of Introduced Species

Another consequence of human interference in nature is the introduction of invasive

alien species, which, as mentioned in the previous chapter, pose a threat to native
species and the ecosystems they inhabit. These invasions often result in extinction
or a significant reduction in the abundance of various local plant and animal species.
The detrimental effects of invasive species can include hybridization, transmission
of diseases or parasites, competition for resources, alteration of the behavior and
reproduction of native species, and other impacts (Allison & Vitousek, 2004;
Lambrinos, 2004). As these adverse effects spread, they can transform the structure
and functioning of the environment.
Initially, exotic species in relatively low numbers may coexist with native species
over an extended period. However, when their reproductive capabilities are
exploited, they can become more aggressive and escalate their impact on native spe-
cies, exacerbating the problem further. The introduction of certain species into new
environments is often accidental. This can occur, for example, when species inad-
vertently hitchhike on ships or other types of transportation, unintentionally being
transported to regions far from their native habitats. However, in other cases, exotic
species are intentionally introduced, generally for economic purposes. For example,
436 7 Focusing on Dynamics: When a Rule Becomes an Exception

many species are introduced for agriculture or livestock or, as mentioned in the
previous item, for recreation (e.g., hunting and fishing). Many plants are introduced
for gardening, landscaping, or forestation. All these situations imply the possibility
that these species become invasive and go from being the exception to being the
rule, as already pointed out in Chap. 6. In this case, we focus inversely on the pro-
cess that now leaves native species as exceptions in their environment due to the
introduction of exotics.
Many times, the native flora and fauna are not prepared to adapt to changes in a
short time. The alterations that have occurred in the climate due to global warming
favor species that have been introduced voluntarily or involuntarily by human action
and can expand into new areas. Due to this expansion, invasive species are respon-
sible for approximately 15% of extinctions worldwide, making them a significant
threat. In Europe, as elsewhere in the world, there are a large number of native spe-
cies that are competing with European flora and fauna. Furthermore, in this compe-
tition for survival, native species are losing their place. One example is the European
mink (Mustela lutreola) in Spain. These animals have always been heavily perse-
cuted for their fur, and in the 1990s, their population declined significantly. Currently,
the introduction of the American mink (Neovison vison) has led the European mink
to be included in the list of endangered species in Europe, as it is suffering rapid
decline and is prone to extinction. These animals were introduced for fur produc-
tion, but accidental escapes or intentional releases of individuals caused them to
affect the native fauna (Fasola et al., 2010; Jaksic et al., 2002; Lizarralde & Escobar,
2000). The introduced mink is a very opportunistic animal. In addition, coupled
with the ability to compete for food and territory, the American mink is much more
resistant to some diseases and has therefore been able to invade European mink
habitats easily (Pavés., 2021). Mink constitutes a significant threat to native rodents
and birds. This species of mink has also been introduced in the Southern Hemisphere
for the same purpose. In Argentina, it has significantly reduced native avifauna,
mainly the hooded grebe (Podiceps gallardoi) (Roesler et al., 2012).
Next, we will refer to other specific cases of native animals and plants that were
displaced by introduced exotics and, in many cases, led to their extinction.

Animals

Cats and dogs have been domesticated for thousands of years, and they now play an
important role in human society. In areas where predation is not a major threat and
adequate prey is available, some abandoned cats and dogs manage to survive and
form feral populations. This phenomenon is common on oceanic islands in Australia
and New Zealand (Van't Woudt, 1990). However, outside of oceanic islands and
desert regions, where their impact on native animals can be devastating (Medina
et al., 2011), feral cats can play a useful role in controlling small vermin popula-
tions. Nevertheless, their presence can also harm wildlife, particularly lizards, small
marsupials, and certain bird species (Kauhala et al., 2015). The need for control of
roaming, stray, or feral cats in rural areas is not entirely clear-cut, as their potential
7.3 Human-Induced R-E Changes over Nature 437

benefits in managing vermin populations need to be weighed against the damage

they may cause to native wildlife.
In contrast, dogs, whether roaming, stray, or feral, can be potentially destructive
animals and demand strict control measures to mitigate their impact on both wild-
life and human communities (Banks & Bryant, 2007; Zapata-Ríos & Branch, 2016).
We have already discussed the introduction of rabbits in Australia and their effects
on this new environment. Since the end of the nineteenth century, when rabbits
began to cause damage to vegetation in Australia, it became clear that introduced
species were potentially harmful (Enserink, 1999). Rabbits destroy natural vegeta-
tion, grasses, and small shrubs and are responsible for erosion problems as they
expose topsoil. This damage is devastating, as this layer of soil takes hundreds of
years to regenerate (Cooke, 2012).
One of the most critical environmental risks is introducing exotic aquatic species
due to the modification they cause to aquatic habitats and biodiversity (Hopkins,
2001). The introduction of exotic species has been associated with the extinction of
54% of the world’s native aquatic fauna (Harrison & Stiassny, 1999), 70% of North
American fish (Lassuy, 1995), and 60% of Mexican fish (Contreras-Balderas, 1999).
An example of this phenomenon is the common carp (Cyprinus carpio), which
wreaks havoc on populations and natural environments. It was introduced from
Asia, and its method of feeding removes sediment from the river bottom, reducing
water quality, generating turbidity, and destroying aquatic plants. It also reduces the
abundance of aquatic invertebrates, alters the spawning habitats of other species,
competes ecologically with other species, and reduces native biodiversity. It has
been responsible for the decline of native fish species, amphibians, reptiles, and
birds in various aquatic ecosystems worldwide (Rauque Perez et al., 2017). The
painted turtle (Trachemys scripta) is also one of the 100 most detrimental invasive
alien species (Seburn et al., 2023). It was introduced into Europe from the United
States and competes with Iberian turtles, as it is better adapted to polluted environ-
ments and human presence.
Many animals were also introduced for petting, as is the case of the monk para-
keet (Myiopsitta monachus) in Spain. This species competes with and displaces
native species, such as the spring blackbird (Turdus migratorius) or the magpie
(Pica pica). In addition, it is a dominant and aggressive species in artificial feeders
(Muñoz-Jiménez & Alcántara-Carbajal, 2017) and affects the flora through its nest-­
building activity (Gallego, 2019). Additionally, as a pet, the raccoon (Procyon lotor)
has been introduced to Europe from North America, affecting many native species
through competition and predation of fish, amphibians, mollusks, and birds, among
others (García et al., 2012). Raccoons are voracious and opportunistic animals that
can typically hunt and prey on bird nests. They compete intensely with aquatic
medium carnivores, such as otters (Lutra lutra), European mink (Mustela lutreola),
or polecats (Mustela putorius), for diet or territory overlap (Salgado, 2015).
All these cases demonstrate that species introduced for a particular purpose that
favors human activities can end up harming native species. Thus, native species that
were the rule in their distribution can become mere exceptions when displaced by
exotic species and all as a consequence of human influence on nature.
438 7 Focusing on Dynamics: When a Rule Becomes an Exception

Plants

The plants introduced for forestation, landscaping, and cultivation may displace
other native plants until they are significantly reduced. Many species colonized new
sites through agriculture. Some of these species, such as maize (Zea mays), wheat
(Triticum spp.), soy (Glycine max), or rice (Oryza sativa), have been beneficial
because they facilitate food supply. However, they also cause economic losses and
ecological impacts (Pimentel et al., 2001). Indeed, when plants are introduced for
agricultural production, the soil’s physical, chemical, and biological characteristics
are modified, which can take years to recover and stabilize (Okada & Harada, 2007;
Villenave et al., 2001), but this modification helps the establishment of invasive spe-
cies. Sorghum (Sorghum halepense), an African crop with vegetative reproduction
facilitated by soil tillage, was introduced in Argentina. Spreading the rhizomes
favors their establishment, proliferation, and dominance (Radosevich et al., 2007).
For landscaping and gardening purposes, the ash-leaved maple (Acer negundo),
native to North America, has been introduced to many continents. This species is
highly invasive and forms a dense layer of foliage that hinders or prevents the
growth of other native species. The behavior of foliage allocation in response to the
availability of light and nutrients allows this species to outcompete native tree spe-
cies. This characteristic threatens biodiversity and ecosystem functioning (Porté
et al., 2011). Another case is that of dandelion (Taraxacum officinale), a perennial
herbaceous plant native to the temperate zones of the northern hemisphere, which is
now widespread in the temperate zones of almost the entire world, except Africa
(Holm et al., 1997). This plant species has apomictic reproduction and can grow in
contrasting climates and disturbance regimes. In some parts of the world, these
plants are considered weeds and can reduce the pollination and reproduction of
native grasses (Kandori et al., 2009; Molina-Montenegro et al., 2010; Muñoz &
Cavieres, 2008). Another example of an introduced species is Banksia ericifolia,
which produces thousands of seeds at an earlier age in southern Africa, where it is
exotic. At the same time, in its native environment, Australia, it only begins its
reproductive cycle much later, at 25 years of age (Crawley, 1997). This characteris-
tic causes its proliferation to be much more significant and can displace native
African species, such as the proteaceous shrub Leucadendron laureolum. Both spe-
cies are killed by fire and rely on stored seeds for recovery. Banksia ericifolia pro-
duces an average of 16,500 seeds per plant, approximately 30 times more than
L. laureolum, giving the latter a considerable disadvantage in recovery compared to
the invasive potential of the exotic B. ericifolia (Honig et al., 1992).
An invasive species spreading uncontrollably in Argentina is the broad-leaf
privet (Ligustrum lucidum). Also introduced for landscaping, this tree, originally
from China, is one of the 100 most invasive species in the world. It grows by tak-
ing water away from other native species, occupies their space, and generates
biodiversity loss, creating a less conducive habitat for fauna (Ayup et al., 2014).
These trees limit the diversity of native birds, such as the black-backed grosbeak
(Pheucticus aureoventris), the dark-billed cuckoo (Coccyzus melacoryphus), and
the scimitar-­billed woodcreeper (Drymornis bridgesii). In addition, they favor the
proliferation of exotic generalist birds such as pigeons (Leptotila verreauxi,
7.3 Human-Induced R-E Changes over Nature 439

Patagioenas picazuro, P. maculosa) or parrots (Myiopsitta monachus) (Bellis

et al., 2021). However, due to high growth and reproduction rates, this tree also
represents an essential change agent in native Tala (Celtis tala) forests (Delucchi
& Torres Robles, 2009; Fernandez et al., 2020; Morello et al., 2012). The intro-
duction of all these plants by man, for different purposes, and without planning,
causes uncontrolled growth to damage the native flora in the same way that hap-
pens with animals. Thus, native species that were common are diminished in their
growth, reproduction, and distribution until remaining as exceptions in their origi-
nal environment.

7.3.3.3 On Secondary Extinctions of Biodiversity

In the context of transitioning from rule to exception, it is intriguing to examine

extinctions caused by human activity on a global scale. These extinctions demon-
strate how “indirect” actions, such as hunting, can be as impactful as direct actions
in causing the extinction of a species. We use the term “secondary extinctions” to
describe situations where a species becomes extinct indirectly due to human actions
that lead to the elimination of another species with which it had interactions (please
refer to Fig. 1 of Brodie et al., 2014). This dynamic is highly intriguing, as it goes
beyond solely considering the direct impact of human actions and introduces the
additional factor of eliminating one or more interacting species.
Some relationships between species are highly dependent on each other, highly
specialized, and have a higher probability of ending in a secondary extinction, as
well as between species that evolve more slowly. These are more vulnerable interac-
tions. An example is black-footed ferrets (Mustela nigripes), which came to the
brink of extinction when the abundance of their only prey, the prairie dog (Cynomys
spp.), declined alarmingly (Miller et al., 1994). This reduction occurred due to erad-
ication programs by the U.S. government to favor the cattle industry. Actions are
now being taken to recover these populations, which are essential to maintaining
diversity (Miller et al., 1990). Here, we can see that the indirect action of man to
favor the economy puts biodiversity at risk, not only by eliminating one species but
also a second species with which it necessarily interacts.
Sometimes, species vulnerability also depends on their resistance to human
impacts. If a species is a generalist but all interacting species are affected by the
impact of anthropization, that species may also be at risk of extinction. Conversely,
specialist species that depend on others very resistant to human-induced change
may not be affected (Rezende et al., 2007). This is the case, for example, for the
passenger pigeon chewing louse (Columbicola extinctus), for which its host species
(Patagioenas fasciata) is not vulnerable to human impacts (Colwell et al., 2012).
Therefore, this specialist species is not affected, thanks to the resistance offered by
the primary interacting species, in this case the host.
In the framework of this book, secondary extinctions could be seen as the pas-
sage from rule to exception, not only of a species affected by human actions but also
as a chain that begins with these actions, turning more than one species into an
exception and affecting the natural regulation of populations.
440 7 Focusing on Dynamics: When a Rule Becomes an Exception

However, the type of dependence between species will also be a determining fac-
tor in secondary extinctions. Most of the time, dependence is linked to food.
However, there is also dependence on mutualistic species, for example, in the case
of pollination. However, in some cases, such dependence does not usually determine
the species’ survival, so the reduction of the pollinator by man does not always have
consequences on the affected species (Brodie et al., 2014). For example, as we
already saw, sometimes the elimination of pollinators due to human action causes
some pollinator-dependent populations to be reduced. However, it can also cause
self-pollination capacity to develop within a few generations, such as in monkey-
flower (Erythranthe guttata). In this species, populations without pollinators had
significantly reduced fitness in the first few generations but recovered as they devel-
oped an improved ability to self-fertilize (Roels & Kelly, 2011). As we saw in the
previous chapter, evolution toward self-pollination is a typical response to pollinator
removal, as is the shift toward pollination by other species or by the wind in other
cases (Costa & Machado, 2012; Kalisz et al., 2004; Yamasaki & Sakai, 2013). In
any case, humans negatively affect species by interfering with the interaction among
them, which could eventually lead them to face a high extinction risk.
However, external factors can also lead to secondary extinction. For example,
this occurs when multiple anthropogenic stressors act on species interactions, exac-
erbating the risk of secondary extinction (Didham et al., 2007). If humans disturb
the habitat, this can increase the impact of exotic species on native species, generat-
ing an unfavorable chain effect (Didham et al., 2007). However, related to the loss
of pollinators, species that respond to climate change may also become incompati-
ble with their pollinators (Memmott et al., 2007), and the loss of native pollinators
could be severe for some species (Cox, 1983). If new associations between species
are generated, in some cases, the probability of secondary extinctions may be
reduced (Brodie et al., 2014).
All these possibilities highlight the significant impact of human actions on both
primary extinctions, as discussed in the previous sections, and secondary extinc-
tions of numerous species, as presented here. These actions not only lead to a loss
of biodiversity but also trigger shifts in the abundance of species, both directly and
indirectly affected. The increasing trend of common species becoming rare or dis-
appearing due to human activities is altering abundance patterns. By addressing the
loss of species interactions, we can potentially reduce the risk of secondary extinc-
tions. Therefore, it becomes imperative to consider the number of human-­induced
secondary extinctions in conservation planning (Brodie et al., 2014).

7.3.4 Climate Change and its Effect on the Dynamics of R to E

We might ask, Climate change again? It is a recurring theme, but it is true that the
change in climatic conditions linked to human activity clearly shows constant tran-
sitions from rules to exceptions and vice versa. Indeed, in the previous chapter, we
discussed how the phenomenon went from being exceptional to escalating and
7.3 Human-Induced R-E Changes over Nature 441

becoming commonplace and dangerous. In the present chapter, we will analyze the
phenomenon from another point of view. We will analyze in case of studies the
effects of climate change on different systems and how this influence results in a
transition from rule to exception.

7.3.4.1 Effect of Global Warming on Organisms

Changes in the Distribution, Hybridization Processes, and Interactions of

Animal Species

Temperature strongly influences numerous characteristics of living organisms,

ranging from the maturation of plants and insects to the dynamics of prey appear-
ance in ecosystems. Even slight changes in the planet’s temperature can signifi-
cantly impact various biological relationships and timings. Considering the
accelerated rates of current climate change compared to natural occurrences
(Solomon et al., 2007), the effects become even more pronounced. For example,
severe climate change can modify organisms’ natural spring and winter (Peñuelas
& Filella, 2009). As we will see below, this phenomenon can have adverse effects
on organisms and populations. Climate change causes phenology variations, which
are living organisms’ reactions to seasonal and climatic changes in their environ-
ment. This phenomenon is widespread in many species distributed across different
taxa (Visser & Both, 2005). For instance, a temperature increase of just 1 °C can
advance the initial emergence and peak emergence of certain butterflies by
2–10 days. Although climate change has been shown to alter insect phenology, the
relationships can sometimes be complex and even counterintuitive (Forrest, 2016).
Future climate scenarios show that we should expect species range to vary in
size, shrink or increase, or cause species shifts in altitude, longitude, or both (see
Gómez-Ruiz & Lacher Jr, 2019). One consequence that the planet has experienced
in recent decades due to climate change is expanding species ranges into new areas
(Crowley & North, 1988). When an invasive species expands its range and overlaps
with the distribution of native species, it can lead to mating between different spe-
cies and even hybridization (Coyne & Orr, 2004; Rhymer & Simberloff, 1996). The
explanation for these phenomena is that when two sister species evolve in the exact
location, they may partially or completely lose the ability to discriminate against the
other species. Thus, interspecies mating and hybridization occur when sister species
come into secondary contact (reviewed by Coyne & Orr, 2004; Sánchez-Guillén
et al., 2016). One example is posited by Wellenreuther et al. (2010) with damsel-
flies, Calopteryx splendens, and C. virgo. These authors documented a loss in the
ability to discern the same species’ mating partner from the sister species in allopat-
ric populations in northern Europe. However, how frequently hybridization occurs
is an underexplored topic (see Sánchez-Guillén et al., 2016).
In four major taxa, including fruit flies of the genus Drosophila (Coyne & Orr,
1989, 1997), salamanders (Tilley et al., 1990), frogs and toads (Sasa et al., 1998),
butterflies (Presgraves, 2002), and gymnosperm plants (Lowry et al., 2008), the
442 7 Focusing on Dynamics: When a Rule Becomes an Exception

degree of reproductive isolation has been shown to correlate directly with Nei’s
genetic distance (Nei, 1972) between species pairs. Thus, those species pairs at dif-
ferent genetic distances show different levels of speciation. Based on this principle,
we can predict which pairs of species may hybridize with invasive species when
they come into contact within their range in response to climate change. In this case,
climate change affects the distribution of species, modifying their natural or normal
range, and this change allows species to come into contact. Encounters between
closely related species do not typically occur in the absence of climate change.
However, with climate change-induced range expansions, these encounters can lead
to hybridizations and cause confusion between mating pairs, resulting in lost copu-
lation opportunities (pseudocopulation). In addition, this encounter can even gener-
ate more significant investment in reproduction to compete with an individual of
another species (e.g., Naretto et al., 2016; Vrech et al., 2018). All of these factors are
detrimental to the maintenance of the species. These disruptions are rare and may
become common in the future with potential adverse outcomes for populations.
Modifications in Predator–Prey Interaction: A Witness Case. Climate change-­
induced changes in phenology or in migration patterns can disrupt the interactions
between predators and prey. There is a possibility that the predator and the prey (or
its food source) may no longer synchronize their encounters due to these shifts. We
will leave aside predator-plant interactions, which are also altered by changes in the
distribution of one of the organisms or the phenology of plants. Instead, we will
analyze a slightly more complex example of interactions. It is the one described by
Lee Cooper (see Lovejoy & Hannah, 2019) in the Bering Sea. In this sea, the shal-
low shelf can be divided into two well-defined ecosystems. To the south, a pelagic
system (in the water column) is dominated by fishes that partition the water column.
To the northwest, waters with freezing temperatures do not allow the development
of fish. However, they do allow the development of marine macroinvertebrates such
as mollusks, annelids, or crustaceans that feed birds and large mammals such as
walruses, seals, or some whales. In the northern system, the ice cover has been sig-
nificantly reduced over the last 30 years. In this area, the increase in temperature
caused a noticeable change to a more pelagic ecosystem (Grebmeier et al., 2006).
Thus, mammals such as walruses, which depend on benthic organisms (seabed), are
severely affected. Ice sheet retreat means that they have to swim a long distance,
beyond their standard swimming capabilities, to find food. In turn, food is also
diminishing, causing a double ecological problem for these organisms. In typical
situations, such as those at the beginning of the twentieth century, the ice sheet was
present from November to June. Above it, ice-dependent species such as large ter-
restrial mammals and birds dominated. Below this point, bottom-associated animal
(benthic) production was more significant than water column production. In con-
trast, the change brought about by the increase in temperature causes less ice to
exist. The ice retreats earlier and appears after the periods where it usually did.
However, here, the dominant organisms on the ice sheet decreased significantly
(e.g., walruses and polar bears), and there was a significant increase in seasonal
migrants, such as cetaceans. Finally, there is an increased production of organisms
in the water column. This example demonstrates how the change brought about by
7.3 Human-Induced R-E Changes over Nature 443

global warming is detrimental to the feeding of some species, producing situations

that were previously exceptional or appeared in another area of the ecosystem and
became the norm at the expense of the organisms that make up the ecosystem.

Pollinators and Plants: Phenological and Distributional Changes That Result in

Mutualistic Interaction Interference

As we saw in the previous chapter, the relationship between plants and pollinators
generates globally essential ecosystem services. This balance between the two
groups can be disturbed by global warming, which can modify the phenology of
plants, pollinators, or both, generating interaction mismatches (Bartomeus et al.,
2013). Spatial mismatches can cause associated problems due to changes in the
distribution of involved species or by changes in phenology, as we have seen in the
previous paragraph. Displacements can also occur even when the species are in
contact. In this case, morphological changes may appear or changes in interaction
behaviors. These changes can generate new scaffolds in the community (Gérard
et al., 2020). Perhaps the species most likely to be affected are plants associated
with specialist pollinators and those that flower in early spring (Gérard et al., 2020;
Willmer, 2014).
An Example of Phenological Changes in Pollinator-Plant Interactions.
Temperature can differentially affect the flight period of pollinators and plant flow-
ering times (Willmer, 2014). Let us take as an example the interaction between
orchids and bees, something we already saw in the previous chapter. Combined
studies between herbaria, museums, and field data indicate that bee flight initiation
dates are moving ahead of orchid flowering time. This behavior may lead to a future
mismatch in the interaction (Willmer, 2014). Specifically, in the case of the orchid
Ophrys sphegodes, flowering is delayed relative to the emergence of the bee species
Andrena nigroaenea, and the misalignment is predicted to be total if current high
rates of warming continue. This relationship is under a deceive system (see Chap. 6)
where flowers are not typical, and male pollinators appear early in the season, before
females. These males are easily cheated because they have no females to interact
with and take for reference. Instead, they perform false copulations with flowers that
mimic the females of the species, as detailed in Chap. 6.
With the warming effect, an increase of only 2 °C makes males appear much
earlier. However, this is not the only thing; female bees also appear earlier in the
population, favored by the increase in temperature. For example, in a warm spring,
we will find male and female bees flying in the population, but the flowers would
not be open yet. The orchid’s deception system is conditioned in this situation by
having male and female pollinators interact. The chances of deceiving male pol-
linators are severely diminished as temperature increases (Willmer, 2014). Here,
again, the shift from rule to exception due to global warming is clear and is
reflected in that the orchid’s deception system would not function properly due to
the subtle change in the phenology of the pollinator and its interaction with the
female of its species.
444 7 Focusing on Dynamics: When a Rule Becomes an Exception

An Example of Range Shift and Change in Pollinator-Plant Relationship. Agaves

(Agave spp.) are plants that develop flowers pollinated by bats (Fenster et al., 2004).
The most important are the long-nosed bats of the genus Leptonycteris spp. (Gómez-­
Ruiz & Lacher Jr, 2019). These bats migrate, and their migration is considered
endangered due to their complexity (Arita & Santos-del-Prado, 1999). The loss of
this interaction would have catastrophic results ecologically but also economically,
socially, and culturally, since, among other things, agave is the source of tequila and
mezcal (Colunga-García et al., 2007; Gentry, 1982). The study by Gómez-Ruiz &
Lacher Jr. (2019) shows that the overlap of agave and pollinating bat areas will be
reduced by approximately 75%. The lack of pollinator foraging zones generates a
threat to its survival and, in return, a drop in agave pollination service. Thus, the
extinction of the pollinator would generate problems at the genetic and reproductive
levels that would make it more vulnerable to future environmental changes.
Something similar has been observed in invertebrates. Evidence shows that some
invertebrate species cannot cope with phenological changes in the plant species they
pollinate (Hegland et al., 2009; Root et al., 2003). Hence, if pollinators rely on
plants for their development and the occurrence of plants is delayed due to tempera-
ture increases, it can pose significant problems for pollinators (Durant et al., 2007).
This effect is accentuated in specialized mutualistic relationships (Schweiger et al.,
2012). Nevertheless, it is essential to note that not all outcomes are negative. As
ongoing studies reveal, in certain cases, phenological changes in plants may not
have a significant impact on the insects that rely on them. For example, high levels
of biodiversity can balance the adverse effects of dyssynchrony at the community
level (Bartomeus et al., 2013). However, at the same time, we must remember that
overall biodiversity levels in many parts of the planet are being seriously decimated
by climate change and environmental pollution. This is a controversial issue, but
with a solid scientific base. In this context, a recent study shows how some 700 spe-
cies are affected by climate change (Wessel, 2017). Therefore, we should not take
for granted that if plants lose their pollinators, there will be another pollinator to
fulfill the task (Burkle & Alarcón, 2011; Hegland et al., 2009).

7.3.4.2 Modification or Disappearance of Water Sources

and Watercourses

Lakes, Rivers, and Permanent or Seasonal Ice

It is not only living organisms that suffer from temperature increases. Geographical
agents, such as watercourses and hydrology, may also be affected (Solomon et al.,
2007). Climate change will impact river courses and directly affect associated eco-
systems (Thompson et al., 2021). Many changes in hydrological systems are linked
to the escalating global temperatures caused by human activities. One noticeable
effect is the alteration in precipitation patterns and their seasonal distribution. While
average precipitation is increasing due to climate change, a substantial portion of it
falls over the sea. Consequently, numerous continental regions are projected to
experience a reduction in precipitation (Arnell, 1999).
7.3 Human-Induced R-E Changes over Nature 445

There are also changes in the balance between snow and rain. These changes
cause ice to retreat because of an imbalance between snow flow and melting. This
imbalance contributes to the retreat of diverse ice masses such as glaciers, snow, or
permanent ice (large ice masses). In fact, mountainous permafrost, glaciers, and
large continental masses are constantly fighting against their disappearance due to
the increase in temperature and the change in the type of precipitation. Water in the
area can change from snow to rain or a mixed situation, resulting in the loss or
retreat of the ice sheet. This mismatch in precipitation and the rate of ice generation
and retreat has a profound impact on the flow of watercourses, including rivers,
lakes, and even the ocean itself.
In addition, the increase in evapotranspiration and loss of soil moisture generates
desertification, large-scale droughts, and vegetation cover changes linked to modifi-
cations in temperature and precipitation. In addition, this moisture loss increases the
risk of flooding by losing a natural shield against the advance of water and increases
the risk of fires as droughts become more extreme. Temperatures rise in areas with
high plant fuel, and the drop in precipitation means that water does not help to miti-
gate fires (Goudie, 2006). Regional precipitation and temperature patterns are pro-
jected to change, affecting natural stream flows (Palmer et al., 2009). In fact, due to
projected changes in CO2 concentration and their resulting change in temperature
and precipitation, river discharges are believed to continue to change in many
regions much faster than they have historically (Alcamo et al., 2003; Lettenmaier
et al., 1994; Vörösmarty et al., 2000).
Thus, climate change is a process that generates many geological changes from
rule to exception. This dynamic may be caused by disappearing systems such as the
retreat and melting of ice sheets or the decline of water resources such as rivers or
lakes. Additionally, by generating a change in the functioning of some systems,
such as a change in the evapotranspiration system that triggers problems previously
less frequent or less “apocalyptic” (e.g., floods, fires, and other natural disasters).
However, we should also know that climate change is not the only risk for many
watercourses, as they are also affected by pollution generated by human activities,
as we saw in the previous chapter (see also Palmer et al., 2009).
As an illustrative example, let us consider a study conducted on the rivers of the
Himalayas, one of the most significant mountain ranges in the world. The research
focused on the dynamics of four rivers in the northwestern Himalayas over various
periods of the twentieth century (Bhutiyani et al., 2008). In the last decades of the
century, a decline in discharge was observed in the Beas and Ravi rivers, with a less
pronounced trend in the latter. Both watercourses share similarities in having lim-
ited glaciers within their basins and receive minimal contributions from snowmelt.
Instead, they primarily depend on monsoon winds for their water supply. However,
the Satluj and Chenab rivers are primarily sustained by glaciers, which have acted
as buffers, regulating discharge. However, the accelerated retreat of the glacier asso-
ciated with the Satluj River accounts for the decline in discharge observed during
the period from 1991 to 2004. This illustrates the substantial impact on the water-
sheds, leading to a transition from rule to exception. In this example, long-­established
watercourses may face the risk of disappearing or undergoing significant modifica-
tions due to the influence of climate change on underlying processes.
446 7 Focusing on Dynamics: When a Rule Becomes an Exception

Oceans and Their Communities

The oceans, along with lentic and lotic watercourses, are experiencing significant
modifications due to climate change. The melting of polar ice caps results in the
introduction of large amounts of freshwater into marine systems, altering the water’s
salinity and causing sea levels to rise. This has well-established direct and indirect
impacts on the ecosystem. Furthermore, the rise in temperature and changes in pH
significantly affect marine ecosystems, leading to alterations and even the disap-
pearance of many organisms. In the following sections, we will examine two cases
related to two crucial components of the oceans: plankton and coral reefs.
Plankton: Change in Ecological Function. Plankton is an essential requirement
for maintaining the ocean’s biological network, being the axis of primary produc-
tion and the basis of many aquatic trophic chains, transferring biomass to other
trophic levels (Murphy et al., 2020). They feed many other organisms and are the
basis of critical biogeochemical processes such as carbon cycling in the ecosystem
(Doney, 2006). The rule up to this point is that plankton biomass varies within
acceptable ranges. These variations are caused by interannual changes in climate
and the upwelling of nutrient-filled cold ocean waters (Dugdale, 1985; Kämpf &
Chapman, 2016). Human-induced climate change generates numerous impacts on
the plankton community by decreasing productivity (Boyce et al., 2010; Murphy
et al., 2020). Climate change exerts more direct pressure because ocean tempera-
tures are increasing at a rate never seen before, generating more extended warm
periods. This disturbance directly impacts the production and recovery capacity of
plankton-forming organisms. If this is exacerbated and sustained over time, the
decline in plankton biomass could jeopardize the rest of the trophic levels that
depend on them.
The change from rule to exception in this example is that plankton may no longer
be the base of the food chain, nor can they cycle carbon and other nutrients effi-
ciently as they have been doing until now. At the same time, and more locally, we
will see a change in the diversity of organisms that make up the plankton (Ibarbalz
et al., 2019), generating the disappearance of some organisms that are now classi-
fied as common, as well as changes in their phenology.
A study by Guinder et al. (2010) shows how the base of the food chain can be
affected in the phytoplankton community of estuaries of Bahía Blanca in Argentina.
In this study, spanning many years, the researchers observed that the rule was a
single explosive appearance (blooming) of organisms between winter and early
spring. This blooming was the main pattern from 1978 to 2002. From 2006 onward,
some changes were detected. For example, there was an absence of some organ-
isms, changes in their phenology, replacement of dominant species in the blooms,
and new species that were previously absent. Nonseasonal blooms were also
observed, with short-lived diatoms throughout the year. In addition, large species
were replaced by comparatively smaller species. All these changes are due to the
region’s progressively warmer winters and drier climate.
In this example, the change from rule to the exception is evident, with changes in
phenological patterns, abundance, presence, and replacement of organisms in a
7.3 Human-Induced R-E Changes over Nature 447

population, a change directly attributable to the increase in temperature due to

human activity.
Coral Reef: Bleaching, Pale Corals. Corals are beautiful organisms. They repre-
sent the most beautiful postcards of any trip to the beach. The so-called stony corals
(Anthozoa, Scleractinia) are generally colonial organisms, relatives of jellyfish,
which form calcium carbonate external skeletons and are capable of generating
coral reefs. The most extensive reefs are found in the Great Barrier Reef of Australia,
followed by the Belize coral reefs in Central America, in areas close to the equator.
A small polyp with tentacles forms the living part of the coral, similar to a small
anemone. Inside it forms a symbiotic association with microorganisms called zoo-
xanthellae (Dinoflagellata) that provide food. Coral reefs are currently experiencing
a high burden of human-generated stress (Carpenter et al., 2008; Hoegh-Guldberg,
2011; Hoegh-Guldberg et al., 2007). Corals are affected by several factors, some of
which are more local, such as eutrophication, offshore development, resource
exploitation, or overfishing (Hughes, 1994; Hughes & Connell, 1999). However,
one of the significant global culprits responsible for the decline in coral health is
human-generated climate change (Eakin et al., 2009; Hoegh-Guldberg, 1999).
There is a phenomenon of great concern to researchers called coral bleaching
(Fig. 7.4a-d). This phenomenon causes corals to expel the symbiont zooxanthellae
and lose their coloration, becoming pale and eventually dying. It is a reaction to
environmental stress. Susceptibility to bleaching varies according to species, depths,

a b

c d

Fig. 7.4 Real-life examples of coral bleaching. (a) Stag coral bleaching from the center to the
sides (Credits: Gavin Bain). (b) Bleached branching coral (foreground) and normal branching
coral (background) (Credits: Acropora). (c) Bleached brain coral (Credits: NOAA National Ocean
Service, 2005). (d) A partially bleached coral colony (Credits: National Marine Sanctuaries)
https://commons.wikimedia.org/wiki/File:NMSAS_coral_bleaching_(27416199680).jpg
448 7 Focusing on Dynamics: When a Rule Becomes an Exception

and location (Grottoli et al., 2014) and is influenced by the endosymbiont (Howells
et al., 2016; Warner et al., 1999). Corals can recover from a bleaching event, but
recurrent annual bleaching and recovery events will generate intense selection and
a decrease in coral diversity in the future, as well as an overall decline in reefs in the
Caribbean (Grottoli et al., 2014). If bleaching becomes a recurring annual event,
more than 90% of coral reefs will be at risk of degradation (Grottoli et al., 2014).
Supporting our discussion of the transition from rule to exception, some models
project that reefs, as we know them today, will exist as relics in isolated locations
(Hoegh-Guldberg et al., 2007). In retrospect, it would be regrettable to lose coral
reefs due to our actions and management of ecosystems, becoming an exception,
something very rare.

7.4 R-E Changes Due to Modifications

in Scientific Interpretations

As seen in science history, there has been a constant evolution in the view of the
natural phenomena investigated. These changes may be due to several reasons, such
as insufficient knowledge, over-reliance on a single animal model and the assump-
tion of uniform behavior across species, or the use of inadequate techniques, equip-
ment, technology, and the influence of paradigm biases. Inadequate technology,
limited information, and geographic, taxonomic, or theoretical bias are variables
that can act alone or in combination to erroneously transform an observation into a
generalized rule or norm when it should be more restricted than initially assumed.
These three scenarios are not as sharp or delimited from each other. There has been
a combination of at least two for changing a rule into something admitted only as an
exception. For example, a bias in the school of thought and using a model organism,
from which data were then extrapolated to many other organisms. Therefore, we can
mention some scenarios or areas, as we did in the previous chapter, fully applicable
to the present chapter. We will begin with the one referring to theoretical or meth-
odological biases in research.

7.4.1 Key Factors Linked to Change

7.4.1.1 Biases in Study Approaches

Strong theoretical biases during experimental design and interpretation of results

have significant consequences on the robustness and future liability to the perma-
nence of a rule for any aspect of biology. In other words, rules may include biases
imposed by a prevailing paradigm or idea. Interpreting data beyond the confines of
our theoretical framework, in which we are directly or indirectly immersed, can be
challenging. Scientific “inertia” may set in if we solely pursue established ideas
7.4 R-E Changes Due to Modifications in Scientific Interpretations 449

without engaging in critical thinking. As we discussed in Chap. 1 on rules, distanc-

ing ourselves partially or entirely from traditional explanations has always demanded
courage and creativity. Within this context, let us consider two situations as exam-
ples. The first involves focusing on specific organisms to make progress in experi-
mental topics while neglecting diversity. The second situation pertains to
evolutionary biology, particularly sexual selection, where significant changes have
occurred in recent years, especially regarding the use of model species and
extrapolations.
In the subsequent chapters, we will delve deeper into these topics to explore the
challenges and opportunities they present in scientific research.

Use of “Model Species” and Generalized Extrapolation

First, let us clarify what we mean by model species. Model species are those that are
studied and analyzed in depth to know and understand different biological processes
and apply them to other species (Ankeny & Leonelli, 2011). The projection of
knowledge obtained from a particular model species can go to just one species of
interest, a family, or even all organisms (Ankeny & Leonelli, 2011). Most, if not all
fields of biology use model species to test hypotheses since it is unlikely that we can
know everything about every nonmodel species (Kunkel, 2006; Zuk et al., 2014).
Some of the most notable model species are, for example, the yeast Saccharomyces
cerevisiae, the bacterium Escherichia coli, and the nematode worm Caenorhabditis
elegans. Among insects, the yellow mealworm beetle Tenebrio molitor, the com-
mon honeybee Apis mellifera, and the fruit fly Drosophila melanogaster give some
examples in this order. Additionally, in vertebrates, rodents such as the mouse Mus
musculus, the domestic rooster, Gallus gallus, and the zebrafish Danio rerio. Many
of these models have significantly increased our scientific knowledge in various
fields, such as systematics, evolution, physiology, genetics, and behavior (Ankeny
& Leonelli, 2011; Zuk et al., 2014), in addition to the use of some in biomedical
research. Model species present characteristics that make them advantageous for
their choice and use. For example, they are easy to collect, maintain, and manipulate
in the laboratory and are generally small in size (both physical and genomic), with
relatively short generation times and high fertility and mating rates, among other
traits (Alber, 2009; Ankeny & Leonelli, 2011; Zuk et al., 2014).
Indeed, much of our current understanding of cellular processes, such as growth,
division, and gene expression, has been made possible thanks to model species
(Fields & Johnston, 2005). The use of model species is beneficial when the research
goes beyond the characteristics that involve the natural history of a particular spe-
cies, as in the case of the use of Drosophila melanogaster to identify and understand
in detail mechanisms of inheritance and development (Fields & Johnston, 2005).
Similarly, the use of rats (Rattus norvegicus) and common pigeons (Columba livia)
was vital to develop theories of how the mind works, later extrapolated to other
animals (Zuk et al., 2014). Model species play a crucial role in advancing knowl-
edge across various research areas. However, a challenge arises when extrapolating
450 7 Focusing on Dynamics: When a Rule Becomes an Exception

data from these species to other organisms without considering their specific bio-
logical characteristics and phylogenetic distances. This requires careful consider-
ation to ensure reliability and applicability to different species.

A Witness Field: Sexual Selection

The use of model species in the field of sexual selection is a clear example where
the results of studies oriented to test hypotheses only in them were later generalized
to the rest of the species, thus incurring significant errors in many cases (Zuk et al.,
2014). Let us examine specific examples. Bateman’s principle, which suggests that
males benefit from a higher number of matings, while females gain significant
reproductive benefits from only a few matings, was initially proposed based on data
from D. melanogaster (Bateman, 1948; Zuk et al., 2014). However, if we set aside
the model and consider particular characteristics of the species we are analyzing,
such as mating system, mate guarding, and offspring care, perhaps this principle is
not the one that best applies (Eberhard, 1996; Edvardsson & Canal, 2006; Tang-
Martínez, 2016).
The fly D. melanogaster has also been a model species for studies on sexual
conflict (Chapman et al., 1995; Holland & Rice, 1999). In this species, males trans-
fer proteins in the ejaculate that reduce longevity and receptivity to future mating in
females. This behavior is beneficial to the male as, for example, they decrease the
likelihood of sperm competition, but not beneficial to the female because it reduces
her level of polyandry (Chapman et al., 1995; Harshman & Prout, 1994; Manier
et al., 2010; Wigby & Chapman, 2005; Zuk et al., 2014). This finding led to studies
in numerous species that focused on sexual conflict, assuming in advance that mat-
ings are detrimental to females (Zuk et al., 2014). However, what if, in most cases,
the male does not transfer some toxic substance along with the ejaculate in mating?
What about thinking that females may benefit from the substances transferred along
with the male ejaculate and by receiving stimulation or nurturing behaviors? What
if we think that not everything is negative for females in sexual interactions?
(Eberhard, 1985, 1996). In this sense, there are studies on the benefits that females
gain with the transferred fluids and behaviors of males during mating (Simmons,
2001; Zuk et al., 2014). For example, in some insect species, seminal fluid trans-
ferred by males has been found to increase not only fecundity but also female sur-
vival (Edvardsson & Canal, 2006; García-Gonzalez & Simmons, 2010).
Another example of a model species in the field of sexual selection is the yellow
dung fly Scathophaga stercoraria, where male behaviors in sexual interactions have
been deeply analyzed and gave rise to the idea of sperm competition (Parker, 1970a,
1970b, 1970c, 1978). Here, particular interest was placed on the avoidance of sperm
competition in a framework of postcopulatory sexual selection, with associated
behaviors, such as prolonged copulation and postcopulatory mate care, among other
behaviors associated with males. Clearly, the focus was on the males, their behavior,
and their interests. This was the norm at the time, relegating the role of the female
in mating (Ah-King, 2023). In this sense, the theory of sperm competition was
7.4 R-E Changes Due to Modifications in Scientific Interpretations 451

considered a generalized process that occurred in different taxa and through which
explanations were sought regarding reproductive behavior, physiology, and mor-
phology (Smith, 1984; Zuk et al., 2014).
After several years, research began to take females into account. Indeed, with the
development of studies on cryptic female choice, in the framework of postcopula-
tory sexual selection, females were no longer considered odd in terms of the active
role they play in intersexual interactions (Eberhard, 1985, 1996, 2015). The idea of
the female possibility of choosing which male to copulate with and the sperm used
to fertilize eggs went from first being accepted as a rare phenomenon to becoming
a rule in many taxa (Eberhard, 1996, 2015).
In recent years, sexual selection studies have witnessed a rise in the diversity of
taxa employed for research. However, there remains a noticeable bias toward using
model species of insects and birds and, to a lesser extent, arachnids, amphibians,
and other groups (Zuk et al., 2014). It is worth acknowledging that model species
have undeniably contributed significantly to advancing scientific knowledge across
various disciplines. However, the big question is to what extent we can generalize
knowledge between different taxa without making mistakes. Using only a limited
number of species to explain a wide range of phenomena can lead to a problem: It
prevents us from truly understanding the actual diversity present in nature. This
limitation arises because there may be a tendency to overlook the importance of
replicating studies in different groups. Researchers might assume that they already
possess “generalizable” results derived from a few model species, leading many to
view studying other groups as unnecessary or even a “waste of time.” Consequently,
such attitudes can hinder originality in research and potentially impede a compre-
hensive understanding of the natural world.
However, as we said above, the use of model species can lead to what is known
as “confirmation bias,” i.e., expecting to find what we want to find and not being
open to the fact that our findings may differ from the prevailing patterns. This prac-
tice goes hand in hand with what we said about forcing generalizations from a few
groups and thus potentially running the risk of continuing with scientific “inertia”
when providing explanations for our results without exercising open and critical
thinking.
In conclusion, it is vital to increase studies on other species beyond those taken
as models (useful only in the first stage), for which knowledge of diversity is an
essential point, an aspect that we will analyze below from a historical and evolution-
ary perspective.

7.4.1.2 Knowledge of Biodiversity and Evolutionary Framework

Biodiversity is understood as the different forms of life present on Earth at all levels,
from genes to ecosystems, including ecological and evolutionary processes that take
place within them (Risser, 1995). The scientific community now widely accepts the
biological evolution of species over time. However, this was not always the case.
For example, in the seventeenth and eighteenth centuries, the Creationist view of
452 7 Focusing on Dynamics: When a Rule Becomes an Exception

nature was deeply rooted. It is not surprising, then, that biological explanations of
that time were mainly restricted to descriptions of plant and animal species, mag-
nificently detailed in some cases, but without explaining how they came to be that
way (in form and function). In this sense, Karl von Linné, in the middle of the eigh-
teenth century, wrote numerous books with exhaustive descriptions of species based
on their morphology and reproduction methods, which, according to the prevailing
dogma of the time, were species created by God. However, von Linné’s most signifi-
cant contribution was his classification system for living beings, which he presented
in his book published in 1735, Systema Naturae. He used a binomial nomenclature
to name each organism, assigned to a genus and a species. This classification system
is still used today.
At the end of the eighteenth century, some scientists, perhaps the most challeng-
ing to the established dogmas, began to debate the idea that the forms of life as we
see them are not fixed but are changing over time. The current of thought known as
Lamarckism, a theory of evolution proposed by the French naturalist Jean-Baptiste
Lamarck, stood out at that time. In 1809, he published his book “Zoological
Philosophy,” in which he proposed that the different forms of life did not remain
unchanged over time but evolved from simpler forms of life. The large number of
species and their adaptations to the environment led Lamarck to think that species
had evolved to adapt to changes in their home environments. The theory that
Lamarck proposed was that individuals evolve by adapting to the changing condi-
tions of habitats, where fossils were intermediate forms between present and past
forms of life. Lamarck formulated two laws in his theory, which today is known as
the theory of the “inheritance of acquired characters.” In the first law, he states that
it is the sustained and constant use of an organ or structure of an organism that
maintains it. The disuse of such an organ or structure leads to its eventual disappear-
ance. In the second law, he proposes that changes in the structures of organisms,
acquired or lost, as a result of having been subjected to changes in their habitat for
a prolonged period of time, are maintained in the following generations (Lamarck,
1809). In other words, what has been acquired can be inherited. Therefore, it would
be the capacity of individuals to adapt to changing environments that would have
produced evolution and the great diversity of species.
Let us think that Lamarck developed his theory of evolution in a context where
what was accepted was religious dogma, with the spontaneous generation of species
and where fossils, for example, were considered as different forms of life, without
any connection with current species. Already here we could have an example where
thanks to a greater knowledge of diversity, of its biology, of its nature, there is a
progressive pressure to think differently from the predominant dogma; even more so
in this case where the preconceived idea had no scientific basis. However, these new
ideas were not immediately accepted by other scientists. Lamarck’s postulates were
not discussed in depth until approximately 50 years later, when Charles Darwin
published his famous book “The Origin of Species” in 1859. In it, Darwin again
takes up several of the concepts that had been treated by the French naturalist (e.g.,
use-disuse of traits, adaptation, inheritance) to explain the great variability on which
natural selection would act. However, he does not consider the mechanism of
7.4 R-E Changes Due to Modifications in Scientific Interpretations 453

inheritance of acquired characters proposed by Lamarck to be the driving force for

the evolution of organisms. Darwin proposed, without the knowledge of genetics
yet available, that during the process of reproduction of living beings, “errors”
occurred, and this led to the offspring not being equal to their parents. This is what
leads to the creation of new species, which, as the generations go by, develop differ-
ent characteristics so that those that show more suitable characteristics are the ones
that will be better able to adapt to the habitat where they live, the widely known,
accepted, and spread the theory of natural selection. It is worth noting here how the
voyages to numerous places where nature had been little or not explored until then,
such as those made by Darwin on the Beagle, were key to a better understanding of
the existing biodiversity. Indeed, they were key to the formulation of theories linked
to ecology and evolution (Andersson & Iwasa, 1996; Kuijper et al., 2012).
During the twentieth century, in the 1930s, what is known as neo-Darwinism
emerged. Dobzhansky, Mayr, and Simpson were among its initiators. This renewed
vision of classical Darwinism proposes that the evolution of organisms is the prod-
uct of a combination of processes such as those proposed by Darwin’s theory of
evolution through natural selection, Mendel’s theory of genetic inheritance, and
random DNA mutations as the basis of variation (Mayr & Provine, 1980). This
combined theory is the one that has been the most widely accepted, in general, to
explain biological evolution. However, it has been expanded and extended more
recently due to advances in molecular biology, phenotypic plasticity, and epigenetic
inheritance. Furthermore, it left some room for other alternatives, such as those
proposed by the theory of symbiogenesis and a specific enduring framework of
neolamarkism (see also Chap. 6). In all these frameworks, evolutionary theories
changed as knowledge and interpretation of biodiversity increased from an evolu-
tionary and phylogenetic point of view. It is a process of constant feedback.
We see that it is clear that to establish accurate patterns or rules, it is vital to have
extensive knowledge of biodiversity. However, the knowledge of new information
does not necessarily mean that the patterns or rules already stated are incorrect.
Perhaps they should be revised and discussed according to specific organisms,
regions, or both (Peretti, 2014). Moreover, knowledge of biodiversity does not end
with its evolution. However, it is also helpful in many aspects of our lives, such as
those associated with obtaining food, fuel, shelter, and medicines (Risser, 1995),
aspects mentioned in various parts of this book.
In conclusion, regarding the passage of specific preestablished patterns or norms
to become rarities or exceptions and the reverse in various fields, we could say that
they are products of at least three aspects: (1) a strong theoretical bias prevailing at
the time of interpretation of the data obtained, such as that which framed the pre-
dominant evolutionary concepts of each epoch; (2) rules or patterns established
from partial data or information, not sufficiently representative, as, for example,
what was already mentioned for model species (and see below geographical insuf-
ficiency and phylogenetic insufficiency); and (3) the availability of limited techno-
logical resources at the time when such pattern or rule was proposed (e.g., see item
7.4.1.3) (Peretti, 2014). For the rules established based on partial data, studies that
include a great diversity of organisms, preferably from different regions of the
454 7 Focusing on Dynamics: When a Rule Becomes an Exception

planet, are essential. As mentioned above, the change from rule to exception due to
insufficient data could be linked to two nonmutually exclusive processes, geo-
graphic inadequacies and phylogenetic inadequacies, concepts that we will
review below.

Geographic (Intraspecific) Inadequacy

Inadequacy occurs when we extend the study area to unexplored regions for a par-
ticular species and find that a traditional rule is an exception in new places. For
example, when we find that populations inhabiting distinct elevational or climatic
zones exhibit eco-behavioral patterns that are very different from those previously
described for “the species.” In this sense, the case of the Neotropics is a clear exam-
ple of how a region with different climatic conditions and vegetation types can dif-
ferentially influence, for example, the sexual traits of species. If we only know a part
of the distribution range, we may say that a given character has a particular mor-
phology/behavior for a species, but this may not be the case (Macías-Ordóñez et al.,
2013). In this sense, Blanckenhorn et al. (2006) and Macías-Ordóñez et al. (2013)
make a fascinating analysis of how different ecological patterns could influence
sexual traits. For example, patterns associated with Bergmann’s rule, mentioned
before, and Rensch’s rule, which proposes that the size of males varies more than
that of females, could influence traits associated with sexual dimorphism in both
vertebrate and invertebrate species.
Not only abiotic factors to which individuals are exposed, but also a combination
of biotic factors such as parasitism and predation can influence the differential
development of morphological and behavioral characters of a species inhabiting
different areas (Chown & Nicolson, 2004; Macías-Ordóñez et al., 2013; Schemske,
2009). An interesting concept to include is that of plasticity that individuals may
have, which is linked to the extent of an ecological niche that different species popu-
lations may inhabit (Donohue et al., 2001). Effective plastic behavioral responses,
for example, allow individuals of different populations to adapt to environmental
variations (Donohue et al., 2001), which inevitably generates variations among
populations of the same species. In this same framework, stating that certain behav-
ioral or morphological traits are of a particular type without knowing the true geo-
graphic distribution of the species is tricky. This may lead us to mistakes similar to
those we discussed regarding using model species to describe certain characters
(see the development of the use of model species in item 7.4.1.1).
There are many examples of species with distribution ranges that cover areas
with different altitudes and latitudes and that show interpopulation variation in cer-
tain characteristics. These cases remind us that if we do not know the species’ real
distribution, we can establish specific rules that are truly not generalizable. Among
plants, some studies show an association between morphological variations accord-
ing to the geographic regions where the species are located. In the case of Quercus
rugosa, variations in leaf size have been reported. These show smaller sizes in the
7.4 R-E Changes Due to Modifications in Scientific Interpretations 455

range of its distribution from south to north, a fact associated with precipitation
levels (Rubio-Licona et al., 2011; Uribe Salas, 2009).
Another example is the significant variations among populations of Arabidopsis
thaliana along climatic and elevation gradients in variables such as their ability to
survive and recover from heat stress (Wolfe & Tonsor, 2014; Zhang et al., 2015).
Thus, different populations of this species inhabiting areas with different tempera-
tures and altitudes show differences in traits such as biomass allocation, fecundity,
dormancy, and seed germination (Montesinos-Navarro et al., 2012; Zhang et al.,
2015). This is one more example of how ignoring the distribution range of a particu-
lar species can lead us to say that some traits are the rule when, in fact, they are not.
Among animals, an example of a behavioral variation of different species popu-
lations with different distribution ranges is shown by the Mediterranean fruit fly,
Ceratitis capitata. Here, males form aggregations and emit pheromones to attract
females during the reproductive season (Diamantidis et al., 2008; Whittier et al.,
1992). Although the male behavior of this species has been extensively analyzed in
recent years (Eberhard, 1999; Yuval & Hendrichs, 1999; Diamantidis et al., 2008),
comparative studies between populations with different geographic distributions
remain limited (Diamantidis et al., 2008). In particular, this species has consider-
ably increased its distribution range, encompassing a wide variety of environmental
conditions (Diamantidis et al., 2008). Thus, a combination of different abiotic and
biotic factors to which different populations are exposed is likely to cause different
selective pressures. In turn, these selective pressures lead to a differentiation in the
evolution of mating systems of individuals from different populations of the species
with different distribution ranges (Briceño et al., 2007; Lux et al., 2003; Diamantidis
et al., 2008). In this chapter, we discussed an example involving crickets, where
natural circumstances led to a shift from a commonly observed rule to an exception.
Specifically, the songs produced by male crickets to attract females for reproduction
were found to have an unintended consequence—they also attracted predators and
parasitoids (see 7.2.1.2). This illustrates how the complexities of nature can result in
unexpected outcomes, altering the conventional understanding of certain behaviors
or patterns in the animal kingdom. Thus, certain areas of a species’ distribution can
lead to differential selection pressure on this trait in populations with a higher risk
of predation or parasitism (Zuk & Kolluru, 1998; Lehmann, 2003; Hedrick &
Kortet, 2006). Thus, among populations of a species with different distribution
ranges, there may be variations in male behavior, leading to male cricket singing in
some populations and not in others, as well as variations in song duration to avoid
predation (Hedrick, 2000; Hedrick & Kortet, 2006). For example, in populations of
Teleogryllus oceanicus that inhabit ranges with intense predation pressure from
bats, males emit their song from their roosts to avoid being attacked (Bailey &
Haythornthwaite, 1998).
In vertebrates, we have the example of anurans, where phenotypic differences
between populations of the same species inhabiting isolated geographic areas are
common (Baraquet et al., 2012). For example, in the species Hypsiboas cordobae,
it has been reported that certain morphometric variables are positively associated
456 7 Focusing on Dynamics: When a Rule Becomes an Exception

with the levels of altitude or latitude of the geographic area that the population has
(Baraquet et al., 2012; Laugen et al., 2002).
A valid question arises: How many species and what distribution ranges are nec-
essary to establish specific rules or patterns, ensuring that the discovery of new
species with distinct characteristics does not invalidate them? This presents a bio-
logical paradox, as discussed in Chap. 1, regarding the challenge of finding rules
applicable to a broad range of organisms at an intermediate or lower level. Exceptions
will inevitably arise, except for laws or rules at a higher level (I or II). Nonetheless,
caution should prevail when extrapolating concepts studied solely in specific organ-
isms or environmental conditions to other groups or conditions.

Phylogenetic (Interspecific) Inadequacy

Phylogenetic inadequacy is the most common cause that determines the passage
from rule to exception. This phenomenon occurs when, as the diversity of lineages
included in our analysis increases, a rule initially applied to certain groups is now
only an exception for the majority. In other words, in some examples, the discovery
of new species and missing links, either living or fossil, changed the concept of their
evolutionary relationships. In this sense, many preestablished patterns were pro-
posed using model species from the Nearctic region, with distributions closer to the
research centers. This highlights a significant risk of unintentional bias when apply-
ing a rule to organisms with different distributions (Peretti, 2014). For instance,
numerous studies utilizing species from the Neotropics encounter the challenge of
overcoming preconceived notions. This is largely influenced not only by the inher-
ent partial knowledge of biodiversity, which is inevitable but also by insufficient
taxonomic and phylogenetic studies that hinder a more comprehensive understand-
ing of biodiversity in certain regions of the planet (Arnold, 2003; Dayton & Sala,
2001). In this sense, access to complete and updated biotic inventories that provide
systematic, ecological, and biogeographic information on the species inhabiting a
given area (Dennis & Ruggiero, 1996; Stork et al., 1996) is fundamental when try-
ing to determine any kind of patterns or norms in the different species (Cotterill &
Foissner, 2010).
In addition to establishing that natural selection is the mechanism by which spe-
cies evolve, Darwin emphasized that species descend from common ancestors and
that the figure of a tree could represent the phylogenetic relationships between
them, the tree of life (Salvetti, 2019; Zardoya, 2010). Understanding the phyloge-
netic relationships between species is essential not only for their proper classifica-
tion but also for establishing reliable and far-reaching rules or patterns. The
naturalists of the time accepted the idea of the “tree of life” proposed by Darwin.
Dedicated to observing, comparing, and classifying, according to morphological
characteristics, they knew that each new species should be linked to other species
(Salvetti, 2019). Currently, scientists no longer use morphological descriptions of
species as a method of classification, but to reconstruct phylogenetic relationships,
7.4 R-E Changes Due to Modifications in Scientific Interpretations 457

they rely on nucleotide or amino acid sequence data and statistical inference meth-
ods (Salvetti, 2019; Zardoya, 2010).

7.4.1.3 Linked to Current Equipment and Methodologies

The lack of availability of technological resources and adequate methodology has

been and will continue to be a problem from which we will not be able to “escape”
when identifying patterns to establish rules in biology. In other words, when they
are proposed based on insufficient technology, it is to be expected that changes in
conceptions and approaches will occur later. Over the years, these rules will cease
to be valid and become, perhaps, just rarities or even disappear from knowledge. In
the following, we will visualize this through some interesting examples to illustrate
this point.

Monogamy in Sensu Stricto in Birds

A classic example of how a preestablished rule ceases to be accurate, mainly due to

advances in available equipment and techniques, is the case of monogamy in birds
(Bennett & Owens, 2002; Petrie & Kempenaers, 1998). Until a few decades ago, a
monogamous mating system was the rule for 90% of birds (Lack, 1968). With the
advancement of studies in the field of sexual selection, monogamy gradually became
restricted to specific groups, such as gulls and other seabirds (Birkhead, 2000; Ismar
et al., 2010). Progressively, with the development of novel molecular techniques, it
was discovered that monogamy in birds was not the rule at all. Therefore, assigning
100% paternity to a single male was gradually taken as a mere rarity. Indeed, new
studies based on genetic analyses of paternity clearly show that only 25% of bird
species are monogamous, so this mating system has gone from being considered the
norm to becoming the exception (Griffith et al., 2002). We can emphasize that this
idea has changed with advances in genetic techniques, such as molecular finger-
printing. Today, monogamy in birds is considered an exception instead of a rule. In
fact, when it occurs, it is more of a “social” type. That is, it does not prevent cases
of infidelity and the litter of multiple parents.
However, the initial perception of monogamy as a widespread mating system in
birds may have been indirectly influenced by human society’s perspective on this
matter. Essentially, the societal tendency to view monogamy as acceptable and pro-
miscuity as punishable might have contributed to the unquestioned acceptance of a
rule regarding avian monogamy. This bias by the prevailing human social paradigm
in each historical epoch could undoubtedly be permeating other similar cases in
biology. It is important to acknowledge that even the most serious and dedicated
scientists may be influenced by prevailing human moral norms (e.g., concepts of
“right and wrong”) during foundational research on a particular subject. Therefore,
we cannot dismiss the possibility of such influences shaping their perspectives.
458 7 Focusing on Dynamics: When a Rule Becomes an Exception

Fortunately, technological, and methodological advances generally challenge dog-

matic ideas and preconceived canons.

Thermoregulation in Ectothermic Animals

Thermoregulation refers to the capacity of organisms to actively control their tem-

perature even when the temperature of the environment may be different.
Homeothermic organisms, such as bird and mammal species, can control their body
temperatures. However, ectothermic organisms are those that do not have such abil-
ity, and their temperature varies with the temperature of the environment, such as
reptiles, amphibians, fish, and invertebrates (Cowles, 1962; Jarošík et al., 2004;
Cowles & Bogert, 1944; Lara-Resendiz et al., 2013). This definition follows what
was traditionally considered a rule. However, thanks to advances in temperature
measurement methodologies, it has been possible to determine that animals tradi-
tionally considered ectotherms can maintain their temperature stability through not
only behavioral but also physiological mechanisms (Hitchcock & McBrayer, 2006;
Kearney & Predavec, 2000).
The behavioral mechanisms of what are considered ectothermic organisms, such
as changes in body position, daily and seasonal activity patterns, and microclimate
selection, arguably still “fit” somehow with the traditional definition. We can also
name what happens in several species of insects and reptiles where their behavior is
of great importance to regulate their temperature efficiently and obtain optimal met-
abolic performance (Casey, 1981; Huey, 1982; Kiefer et al., 2007). For example,
butterflies regulate the opening angle between the wings and the body to regulate
heat absorption (Kemp & Krockenberger, 2002; Barton et al., 2014), and among
reptiles, the wood turtle Glyptemys insculpta moves to forest clearings to bask in the
sun and raise its temperature (Dubois et al., 2009). Examples such as these show
that some ectothermic animals would not be at the mercy of the climate but can
actually modify their temperature to some extent.
However, in some cases, several species no longer fit the traditional definition of
ectothermic organisms. Among the physiological mechanisms related to thermo-
regulation, the dark-light color change in reptile species regulates the absorption of
solar radiation (Clusella-Trullas et al., 2009). For example, it has been seen in the
desert iguana Dipsosaurus dorsalis that they can absorb more than 70% of the radi-
ation when they have a darker coloration. In comparison, when individuals have a
lighter coloration, this absorption drops to 60% (Norris, 1967). Another case we can
name is the regulation of peripheral blood flow. Various animal species can control
their temperature by controlling blood flow through vasodilation or vasoconstric-
tion, modifying the diameter of blood vessels. For example, the marine iguana
Amblyrhynchus cristatus is a species accustomed to living in warm areas but forag-
ing in cold water currents. During this search, it can reduce its heart rate and blood
flow to surface tissues to reduce heat loss (Willmer et al., 2009).
The analysis of thermal biology in reptiles is essential for studying their physiol-
ogy and ecology (Lara-Resendiz et al., 2013), made possible by developing and
7.4 R-E Changes Due to Modifications in Scientific Interpretations 459

using new technologies such as precision digital thermometers (Kearney &

Predavec, 2000; Lara-Resendiz et al., 2013). However, endothermy has evolved in
some species of teleost fishes and sharks of the family Lamnidae. Here, a counter-
current exchange of heat occurs, where heat passes from the venous blood, which
is heated by muscle metabolism, to the cold blood in the arteries. Because heat
passes between blood vessels carrying blood in different directions, it is retained in
the muscles, allowing the organisms to have a higher temperature than the tempera-
ture of the water. The evolution of such mechanisms is attributed to the evolution of
heat retention to have the ability to explore colder areas (Block & Finnerty, 1994).
Among insects, species of various orders (e.g., Odonata, Diptera, Hymenoptera,
Coleoptera, and Lepidoptera) can raise their body temperature by contracting tho-
racic flight muscles prior to flight (Heinrich, 1974; Heinrich, 1987). These species
have a countercurrent hemolymph heat exchange system, where cold hemolymph
enters the thorax from the abdomen, and warm hemolymph moves from the thorax
to the abdomen. For example, during flight, moths of the genus Eupsilia reach their
thoracic temperature of approximately 30°C even when the ambient temperature is
much lower (Heinrich, 1987). This type of thermoregulation has also been detected
in bees during foraging behaviors, so the higher the thoracic temperature they can
reach, the greater the number of flowers they can visit per unit of time
(Heinrich, 1987).
Although the examples found thus far differ from the traditional definition of
ectothermic organisms, it is perhaps too early to say that we are facing a change
from rule to exception. However, we believe that, with the study of a more signifi-
cant number of species and greater technological advances, we will be able to find
numerous examples showing that ectothermic organisms can regulate their body
temperature in some way. Thus, this rule will no longer be valid.

Sexual Cannibalism: From Conjecture to Reality in Scorpions

Let us start by defining female sexual cannibalism behavior. This behavior refers to
when, in general, females kill and consume the male before, during, or after mating
(Elgar, 1992; Schneider & Elgar, 2001; Elgar & Schneider, 2004; Prenter et al.,
2006). Thus, depending on when sexual cannibalism occurs, we can classify it as
precopulatory and postcopulatory, depending on whether it occurs before or after
insemination. Clearly, the costs and benefits for both females and males differ
depending on whether sexual cannibalism occurs precopulatory or postcopulatory
(Elgar, 1992; Elgar & Schneider, 2004). Therefore, the timing of sexual cannibalism
is essential in determining whether it can be considered a reproductive strategy. If it
occurs before insemination, i.e., precopulatory sexual cannibalism, it is definitely
not beneficial for males and may be beneficial for females. However, if it occurs
after insemination, postcopulatory sexual cannibalism, we can say that this behavior
can be beneficial for one or both sexes (Andrade, 1996; Elgar & Schneider, 2004;
Vahed, 1998).
460 7 Focusing on Dynamics: When a Rule Becomes an Exception

In addition, some hypotheses have been proposed to explain the occurrence and
evolution of this behavior. For example, the adaptive foraging hypothesis proposes
that in a precopulatory instance, females evaluate the nutritional value of a male
against his value as a mate (Andrade, 1998; Barry et al., 2008a; Blamires, 2011).
Another hypothesis is the aggressive spillover hypothesis, which suggests that
females that are more aggressive toward prey will also be more aggressive toward
males in sexual interactions (Arnqvist, 1992; Barry et al., 2008b; Johnson, 2001;
Polis, 1981). There is also the mate choice hypothesis, in which if a female rejects
a male as a mate, then she cannibalizes him (Gatz, 1981; Persons & Uetz, 2005).
Additionally, there is the mistaken identity hypothesis, which suggests that sexual
cannibalism occurs when females fail to identify males as potential mates (Aisenberg
& Peretti, 2011).
Sexual cannibalism is widely distributed among invertebrates, e.g., in gastropod,
copepod, insect, and arachnid species (Bilde et al., 2006; Elgar, 1992). Among
insects, there are numerous examples among the mantids. In Pseudomantis albofim-
briata, although sexual cannibalism begins before sexual interaction, males can ini-
tiate copulation and sperm transfer, while females consume them. Here, sexual
cannibalism is linked, e.g., with a better fecundity rate in males (Birkhead & Møller,
1998; Barry, 2004; Barry et al., 2008a; Barry et al., 2008b; Lelito & Brown, 2006).
In Tenodera sinensis, the sexual cannibalism behavior of females to males was also
recorded. In this case, egg analyses showed that eggs contained more amino acids
derived from males when cannibalism occurred. Thus, males provide resources
directly to the eggs, which offsets the cost of losing future matings (Brown & Barry,
2016). In the mantid T. aridifolia, there are also frequent records of sexual cannibal-
ism (Watanabe & Yano, 2012). Another insect group where sexual cannibalism
behaviors are widespread is water striders, e.g., Gerris odontogaster (Arnqvist,
1994; Spence & Cárcamo, 1991).
In spiders, there are also several cases of sexual cannibalism. In the spider
Araneus diadematus, sexual cannibalism can occur before or after insemination
(Elgar, 1989; Elgar & Schneider, 2004; Schneider & Elgar, 2001). In other spider
species, the cannibalism observed is postcopulatory, as in the case of Argiope bru-
ennichi, as females attack males after insemination (Elgar et al., 2000; Elgar &
Schneider, 2004; Fromhage et al., 2003). In addition, an iconic example is what
happens in the species Latrodectus hasselti, where males, during copulation, can
turn their abdomen 180°, being very close to the mouthparts of females and can be
consumed by them (Andrade, 1996, 1998; Elgar & Schneider, 2004). Possibly in
this species, cannibalism occurs as there is a low probability of recopulation for
males, and they increase their fertilization success when they “offer” their bodies
for females to consume them (Andrade, 1996; Andrade & Banta, 2002; Peretti, 2014).
While numerous examples of sexual cannibalism occur among spiders, in another
order of arachnids, scorpions, females were long considered to eat males immedi-
ately after mating. Indeed, this was considered the generalized pattern for the order
(Polis & Sissom, 1990), particularly in books referring to sexual cannibalism (Elgar,
1992). In this sense, species such as Bothriurus bonariensis, Urophonius jheringii,
7.4 R-E Changes Due to Modifications in Scientific Interpretations 461

U. brachycentrus, and Leiurus quinquestriatus were included by Polis and Sissom

(1990) among the species where postcopulatory sexual cannibalism was present.
However, thanks to the advance of technology and a design of experiments more in
line with the nature of this type of species, it was possible to prove that this behavior
among scorpion species was far from being a rule (Elgar, 1992; Elgar & Schneider,
2004; Peretti et al., 1999). Several factors contribute to this misconception, includ-
ing the oversight of the minimal space needed for a couple in the laboratory terrar-
ium, insufficient field observations, and limited understanding of the ethological
basis of sexual behavior (Peretti, 2014). Moreover, what distinguished these new
analyses was the seemingly simple yet crucial aspect of ensuring adequate mini-
mum distances between individuals. Indeed, the observations reporting the occur-
rence of postcopulatory sexual cannibalism were predominantly conducted in
captivity, where males and females were confined in small habitats not only for
mating but also for an extended period after copulation (Elgar & Schneider, 2004;
Peretti et al., 1999). Thus, new observations have shown that sexual cannibalism, if
it exists, could be more of a precopulatory than a postcopulatory type (Peretti, 2014;
Peretti et al., 1999). It is not currently denied that postcopulatory sexual cannibal-
ism may exist in scorpions. However, it is no longer considered the rule for the
whole order as previously assumed, but in any case, an exception.

7.4.2 With “Potential” of R-E by the Change in Interpretations

7.4.2.1 Is Life Confined to Earth?

How can life be interpreted? Are we talking about a rule or an exception? The
answer may lie in the level of interpretation we are assuming. For example, when
we discussed life in the previous chapter, we did so from the perspective of the
Earth. On Earth, life clearly went from being something rare in its beginnings (mil-
lions of years ago) to a common phenomenon in almost every corner, even in very
hostile environments (Rothschild & Mancinelli, 2001). However, what happens if
we take the universe as the focus? The view here changes. At this moment (the year
2022), life is confined only to the Earth, and we can safely say that life in the uni-
verse is rare. In fact, a theory called the rare Earth hypothesis postulates that while
Earth-like planets exist, conditions such as those necessary to generate life are rare
or perhaps even unique (Forgan & Rice, 2010; Ward & Brownlee, 2000). Earth-like
planets or the conditions to harbor life are not rare; what is rare is life itself and the
conditions that aided its emergence. Some researchers soften this last postulate by
suggesting that in the universe, life in the form of bacteria or microorganisms would
not be rare (Chela-Flores, 1998; Cockell, 2016; Rampelotto, 2010; Westall, 1999).
However, uncertainty increases when talking about complex life, such as plants or
animals, and even worse, intelligent life (Barnes, 2012; Chyba & Hand, 2005;
Hoyle, 1983). Thinking a bit, the conditions shown by the Earth to harbor life are
462 7 Focusing on Dynamics: When a Rule Becomes an Exception

unique and rare. A combination of distance from the sun, type of sun star, size of the
Earth, eccentricity of the orbit, presence and proximity of the Moon, atmosphere,
plate tectonics, and volcanic activity make the Earth a complex and rare system in
the universe. However, we must keep in mind that the universe is monstrously enor-
mous (Levin et al., 1998), and some suggest it is even infinite (Teerikorpi et al.,
2019). There are an estimated 8–10% of G-type stars similar to our sun (yellow
dwarf star) in our galaxy alone (Stardate, Universe Guide; Ledrew, 2001). These
stars are included in systems with several planets orbiting them (Gurumath, 2019).
Thus, statistically, there should be a chance that at least one situation exactly like
that of the Earth has occurred somewhere in the vast universe, something rare but
not impossible. Calculations estimate that 6 trillion Earth-like planets exist in the
Milky Way (Gough, 2020). We know, for example, that there are extrasolar Earth-
like planets that are similar in mass, size, and temperature to the Earth. In addition,
there are also “terrestrial twins” that are similar to the Earth, with liquid water in
oceans and continental water masses (Seager, 2003). Between 3000 and 5000 poten-
tial exoplanets (Han et al., 2014) with interesting characteristics to resemble Earth
or harbor minimal conditions for the emergence and maintenance of life have been
studied (Han et al., 2014).
Among the many candidates with different interesting characteristics, we can
discuss Kepler—452B and Trappist 1e as examples. The first presents a relationship
with the star it orbits, similar to that of the Earth with the sun. The star is of the same
type as the sun (G-type star) with a larger diameter. Similarly, the planet is rocky
and 60% larger than the Earth. It is within the habitable area (zone where water
remains liquid on the surface). It takes 385 days to complete orbit (Davachi, 2017;
Jenkins et al., 2015). However, much attention has recently been given to the
Trappist-1 system. Trappist-1 is a dwarf star that has seven orbiting rocky planets
similar in size to Earth, and three of them would be in the habitability zone (Van
Grootel et al., 2018) and could harbor life (Lingam & Loeb, 2017). Studies suggest
that the planet Trappist-1e could harbor more water than terrestrial oceans (Bourrier
et al., 2017) and possibly a planetary atmosphere (Acuña et al., 2021; Turbet et al.,
2020), with the potential for the development of life.
Similarly, but closer to the solar system, we see potential candidates for harbor-
ing life (Chyba & Hand, 2005; Shapiro & Schulze-Makuch, 2009), but perhaps
primitive and very different from what we are used to seeing here on Earth. This is
the example of Europa, one of Jupiter’s moons. Jupiter is a gas giant planet with a
very powerful electromagnetic field (Khurana et al., 2002). That gravitational force
is thought to cause ice to melt beneath Europa’s permanent surface ice sheet, gener-
ating oceans of liquid water in the interior (Kivelson et al., 2009). It is speculated,
still without concrete evidence, that these waters could contain even a primitive
ecosystem under the ice sheet (Hiscox, 2000). There are also studies suggesting that
in the not-so-distant past, both Venus and Mars may have harbored some form of
life (Chyba & Hand, 2005). In fact, it is believed that Mars may have had liquid
water running on the surface (Nazari-Sharabian et al., 2020). Similar cases of
changes in primitive atmospheres have been evaluated on Earth-like exoplanets
7.4 R-E Changes Due to Modifications in Scientific Interpretations 463

(Seager, 2003). However, imagine if we have litimations analyzing nearby planets,

anything beyond those has even more difficulties. It is important to recognize that
even if conditions for life are present, the emergence of life is not a guaranteed out-
come. While favorable conditions increase the likelihood of life, various factors and
complexities may still prevent its appearance. Apart from all the planetary charac-
teristics for harboring life, we also have the triggers for the appearance of life or its
entry into the system, perhaps from space (see Chap. 6 on the origin of life for more
details).
Indeed, at present, life in the universe appears to be an exceptional occurrence
limited to Earth. However, it is essential to acknowledge that our exploration of the
cosmos is still in its early stages, and despite significant advancements in technol-
ogy (Seager, 2003), our current methods for detecting life might still be relatively
primitive. When delving into the scientific papers concerning these discoveries, one
can appreciate the significant advancements in indirectly detecting variables and
constructing models to assess the suitability of planets. However, it is evident that
we are still far from determining specific critical criteria for identifying pathways to
life on these exoplanets.
Here, we see how solar system-like systems are not rare. In addition, planets with
Earth-like characteristics are common. In fact, their presence in the universe would
be a rule or a statistical consequence. However, we see that the presence of life
would be the rare variable. Nevertheless, let us remember that the lack of life on
them currently falls at an equal distance between the total absence and the techno-
logical inability to detect it. Thus, the dilemma that is very common in biology
appears: What we are looking for does not exist, or we cannot find it?
The rule, at least on Earth, is that carbon is the ideal basis for life, just as water
is the ideal solvent. However, again, is this true in the universe, or are we biased by
what we know on Earth? We have heard much about the possibility of other life-­
based molecules based on other atoms and with other solvents. The most cited
examples of alternative chemistry for life are silicon as a backbone and as an alter-
native to the solvents ammonium or benzene (Cockell, 2020). Silicon does not have
the advantages of carbon bonding with other molecules, chirality, and abundance,
so lately, the idea has been discarded (Jacob, 2016). Moreover, imagining organisms
that respond or have adapted physically, chemically, and physiologically to these
compounds becomes difficult. Carbon is more stable, does not produce such inert
structures in its interaction with oxygen, and is found ten times more in the universe
than silicon (Cockell, 2020). However, water is the most abundant solvent in the
universe, meets the requirements to be a suitable solvent perfectly, and is perhaps
the only solvent with this characteristic (Pohorille & Pratt, 2012). We see that car-
bon and water are, thus far, the rule of life because their characteristics are not
matched by any other element or compound. However, we need more information
on alternatives, including other atoms and solvents or a mixture of compounds, to
dismiss other possibilities (Pohorille & Pratt, 2012).
As we move up the biological scale, thinking that life is common in the universe
becomes much more complicated. We suggest that it is easy to talk about life in the
464 7 Focusing on Dynamics: When a Rule Becomes an Exception

universe in the form of microorganisms. However, when we move to more complex,

multicellular organisms, the chances of their existence in the universe diminish.
Chances go down even more when we talk about intelligent life. Indeed, the ques-
tion persists: whether the rule is the existence of life on other planets beyond Earth
(within the same or different galaxies), while intelligent life remains confined solely
to our planet. In simpler terms, this idea allows for the possibility that while life
could be widespread in the universe, intelligent beings might be unique to Earth,
making it an exception in that aspect. There are many hypotheses and interpreta-
tions regarding intelligent life in the galaxy, and many say that we are very likely
alone (Smith, 2011). Others say that while there are potentially millions of civiliza-
tions (Kerr, 2005), we have physical constraints that do not allow us to contact,
which, by the way, may be quite dangerous (Michael, 2011). Thus, other hypotheses
suggest the presence of hidden, undetected life in the universe. The dark forest
hypothesis would solve the Fermi paradox and states that each civilization would be
like a hunter who hides in the jungle to avoid being detected and hunted. Then, none
of the civilizations give signals to go unnoticed (Yu, 2015).
However, perhaps their technological level is similar to ours, just enabling us to
explore neighboring planets. We do not yet have the technological level to explore
the universe in greater detail (Kurzgesagt, 2015; Webb, 2002). It is also thought that
the duration of civilizations may be short, so we never get to explore space in detail
before we perish as a civilization. Finally, a hypothesis speaks of a large filter that
eliminates the possibility of civilizations reaching an advanced level (Peacock, 2018).
With these hypotheses in mind, we can understand that it would become quite
rare and exceptional contact between possible galactic civilizations, assuming they
existed. In this context, it is helpful to look at “local universes” that have been
explored over the years on our own planet that generate ideas of what life might be
like in other star systems and where to look for it. For example, exploring the depths
of the oceans is an excellent starting point for analysis. The discovery of the first
animals inhabiting these depths, represented by abyssal fish (Hoyt, 2014), was a
remarkable event. However, this discovery did not imply that the idea of finding life
in such extreme environments was exceptional. Instead, it opened up the possibility
that life might thrive in diverse and challenging conditions, including the deep
ocean, which was previously considered exceptional. That may be so in several
places, but in others, the rule of the “absence or scarcity” of life, or animals punctu-
ally, has changed toward a rule that life is present in diverse forms, many micro-
scopic. As Dr. Ian Malcom would say in the movie Jurassic Park from 1993,
“Because the history of evolution is that life escapes all barriers. Life breaks free.
Life expands to new territories. Painfully, perhaps even dangerously. But life finds a
way.” Here, in the case concerning the exploration of ocean depths, we observe how
technological advancements greatly facilitated this paradigm shift regarding life in
such environments (Danovaro et al., 2014).
The reader may question why these examples appear in this item. They seem
more like changes due to modifications in our knowledge or understanding of biol-
ogy, Earth, and the universe than changes in the universe itself. It is a mixed situa-
tion. Certainly, our evolving understanding of ideas, access to data, and improved
7.5 Key Concepts and Ideas in this Chapter 465

technology have significantly enhanced our knowledge of the universe and the
ocean floor. As a result, we have gained valuable insights into the colonization of
these spaces over time by various groups of living beings. This understanding has
shed light on how certain organisms came to populate regions where they were
previously absent. Exploring these aspects has led to fascinating discoveries about
the dynamic processes of life dispersal and adaptation to new environments, pro-
viding a deeper understanding of the complexities of life’s distribution and
evolution.
In the ocean floor example, it could be asked whether the expansion of animals
began from the depths to the surface or the other way around. Paleontological data
based on traces (marks left by organisms in the sediment) suggest that organisms
evolved in the late Precambrian, mainly in shallow water. Then, in the Cambrian,
these forms would have moved to depth (Crimes & Fedonkin, 1994). Of course, this
is the story the fossils tell us, but it may not be the whole story, or we may be miss-
ing an essential part of it, the part that was not left in the record. In any case, the
compromise solution could come from the in-between. From there, the bottom of
the oceans, sea surface, coast, and even the terrestrial environment were colonized.
So yes, we have a situation strictly of the behavior of biology from being nothing at
the bottom of the ocean or very rare to at least not so rare.
In the case of exobiology, the situation is, as of today, unknown. First, we discuss
a conjecture. However, if we consider the possibility that life does exist beyond
Earth, it opens up intriguing questions about its origin and distribution. We would
need to investigate where it began, whether it emerged simultaneously in different
locations (either strictly or over extended periods), or if it appeared sequentially
throughout the universe. Additionally, we must consider the direction of its expan-
sion, whether it originated from Earth and spread outward or originated elsewhere
and potentially reached our planet, as suggested in some hypotheses (e.g., Lingam
& Loeb, 2017). The exploration of these questions is fundamental to understanding
the broader context of life’s existence in the cosmos and how it may have evolved
and dispersed throughout the universe. Again, beyond directionality, the example
also applies to this item in that it alludes to biology. Thus, like others, we have
“mixed” situations in this type of example.

7.5 Key Concepts and Ideas in this Chapter

• We have seen multiple examples of transitions from rules to exceptions in biol-

ogy. Evolutionary causes such as natural selection, competition between species
and between organisms within a species, and biotic and abiotic factors can cause
certain traits or structures to have an obsolete function and eventually be lost, to
be considered exceptions when they occur.
• Some factors, such as the decline or disappearance of a species, can produce
changes in the interactions with other species, leaving a pattern as a rarity and
sometimes having a drastic effect on the life of one of the interacting species.
466 7 Focusing on Dynamics: When a Rule Becomes an Exception

• Species distribution patterns evolve along with relief, soil, climate, and relation-
ships between organisms or human activity. Thus, some species are common in
some areas but rare in others. Because of their more significant genetic variation,
species with a broad global distribution can adapt better to environmental
gradients.
• Cities profoundly modify natural habitats and create their microclimate, increase
the average temperature, and offer shelter in their buildings and varied feeding
possibilities. However, they are an inhospitable habitat for most species. Less
adaptable species will become rare as environments become increasingly
anthropized.
• Sometimes climate change causes specific populations to become isolated in cli-
matic relicts, which can be very useful for studying the interactions between
species and how these interactions can affect communities and the ecosystem.
There are relictual species that are representatives of groups that have partially
disappeared. These species have remained exceptions and give us information on
the diversity of the past and existing groups in terms of ancestral species.
• On Earth, there were six great mass extinctions, in which more than half of the
species that existed at that time disappeared without leaving descendants. These
extinctions marked a turning point in species community composition that inhab-
ited the earth, either by disappearance of some or by evolution of others.
• Some species survived the mass extinctions and evolved very slowly, resembling
their ancestors in their general phenotype. Living fossils are unique lineages
characterized by stable morphology, low taxonomic diversity, and a particular
rarity. They can therefore be used as evidence of long-term evolution.
• The human being, through many factors such as artificial selection, the use of
genetics, manipulation of races, or activities such as hunting or fishing, limits the
possibility of evolution to continue its course in living beings. Thus, the original
species that were the rule at the beginning of nature declined in abundance or
ceased to exist and sometimes even gave rise to new species or varieties.
• Many times, the alterations that have occurred in the climate due to global warm-
ing favor species that have been introduced voluntarily or involuntarily by human
action and can expand into new areas. This causes extinctions of native species,
making them exceptions.
• The availability of technological resources and adequate methodology is essen-
tial to identify patterns and establish rules in biology. With insufficient technol-
ogy, it is expected that changes in conceptions and approaches will occur, and
often the established rules may cease to be valid, become rarities, or disappear
from knowledge.
• Life can be a rule or an exception depending on the level of analysis. It is a rule
on Earth but seems to be an exception throughout the universe. Life can be absent
from everywhere else or just difficult to detect.
• Carbon and water are the rule for life as we know it. Other atoms and solvents
theoretically could work, but it seems that carbon and water are truly a rule
for life.
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Chapter 8
Beyond Biology

There are no laws, no traditions, and no rules that can be

universally applied, including this one
— Anonymous

Contents
8.1 Introduction 490
8.2 R&E in Sciences More Closely Related to Biology 491
8.2.1 Medicine and Related Sciences 491
8.2.1.1 Rare Diseases: A Way to Better Understand Common Patterns? 492
8.2.1.2 Exceptions that are Becoming More Common in Medicine 496
A Case in Point: Autism, Real Increase or Revision of Diagnostic
Parameters? 496
Immune Boosters: Who Says Vaccines Do Not Work? 497
Human Enhancement: “Pimp My Body” 498
8.2.1.3 On Changing Conceptions in Medicine 498
Changing Perceptions of Fatness/Obesity 499
From the Prescription of Cigarettes to the Use of Medical Cannabis 500
Maternity and Childbirth 501
8.2.2 Physics Miscellaneous 502
8.2.2.1 Triple Point in Thermodynamics 502
8.2.2.2 The Direction of Time 502
8.2.2.3 Newton’s Laws and the Motion of Bodies 503
8.2.3 Chemical Miscellanea 503
8.2.3.1 A “Macropattern” of Diversity: The Periodic Table 503
Exceptions in the Chemical Elements 504
8.2.3.2 Witness Case: Octet Rule 505
8.2.3.3 An Example of a “Duality” Rule and Exception 505
8.2.4 Geological and Related Notes 506
8.2.4.1 The First Law of Stratigraphy 506
8.2.4.2 The Age of Fossils and Strata 506
8.2.5 Astronomy Miscellany 507
8.2.5.1 Some Dynamics between Rules and Exceptions in Astronomy 509

© Springer Nature Switzerland AG 2024 489

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_8
490 8 Beyond Biology

8.3  &E in Other Knowledge Disciplines

R 511
8.3.1 Social and Related Sciences 511
8.3.1.1 On Native Cultures and Concepts of Family 511
8.3.1.2 Something that is an “Exception” Among Human Societies 512
8.4 R&E Search on Subjective/Controversial Topics 514
8.4.1 Art and Culture 514
8.4.1.1 Image and Painting 514
8.4.1.2 Music 518
8.4.1.3 Literature 518
8.4.1.4 Calligraphy 519
8.4.2 Sports 520
8.4.3 Religions and Beliefs 521
8.5 Key Concepts and Ideas in this Chapter 522
References 523

Abstract In chapter 8, we focus on the dynamics of changes between rules and

exceptions in sciences linked to biology and in other sciences further removed from
it. Within the sciences related to biology, we can name changes in medicine such as
the interpretations of rare diseases and changes in the conception of diseases such
as autism and obesity. Changes also occur in the fields of physics, chemistry, geol-
ogy, and astronomy. In sciences further removed from biology, we also find exam-
ples of a dynamic between rules and exceptions. Within the social sciences, changes
in interpretations linked, for example, to original culturfes and the concept of fam-
ily; in the field linked to art with changes about painting, music, literature, and cal-
ligraphy, for example, and changes in the interpretations of themes associated with
sports and religion where knowledge and interpretations are also changing through-
out the time.

8.1 Introduction

In this chapter, we will move beyond the exploration of rules and exceptions solely
in biology and extend the scope to other branches of science that are interconnected
with biology. By doing so, we will uncover that the perception and analysis of rules
and exceptions extend far beyond the realm of biology. In contrast, it is a more glo-
balizing phenomenon, as it was exposed at the beginning of this book. Moreover,
this chapter also includes other sciences and disciplines less related to biology,
which are present in our daily lives. We intend to mention some cases to illustrate
that there are many options and situations beyond the focus of this book that is cen-
tered on biology.
8.2 R&E in Sciences More Closely Related to Biology 491

8.2 R&E in Sciences More Closely Related to Biology

8.2.1 Medicine and Related Sciences

Indeed, the evolution of medicine over time has been remarkable, leading to signifi-
cant changes in its norms and rules. When we look back to ancient Greece, we can
imagine how primitive and limited the facilities for caring for the sick were in com-
parison to modern healthcare settings. Despite the challenges of the past, ancient
civilizations contributed valuable knowledge to medicine that has endured through
the ages. For example, in the Temple of Kom Ombo in Egypt, carved hieroglyphs
show medical instruments very similar to those still used in hospitals today, which
are thought to have been used for cataract surgery (Butrous et al., 2020; Dobanovacki
et al., 2012). They used honey as a natural antiseptic (Kuropatnicki et al., 2018),
prepared medicines, and even practiced various surgeries (Raudvere, 2020). Thus,
like these stories, we could cite many throughout history and civilizations.
Over centuries, medicine has experienced incredible advancements in under-
standing the human body’s functions, diagnostics, and treatment techniques. Today,
we benefit from a deeper comprehension of diseases, cutting-edge technologies, and
refined medical practices, allowing for more precise and effective healthcare inter-
ventions. Currently, the already massive presence of specialized technology in
health centers is an implicit rule in diagnosing and treating diseases. We now have
monitoring devices, lasers, magnetic resonance devices with unimaginable resolu-
tions, increasingly precise ultrasound scanners, and machines that aid rehabilitation.
Today, it is a rule that medicine is a therapeutic and prophylactic practice. In daily
medical practice, the physician examines the patient, orders tests, diagnoses, and
medicates, if necessary, in general with synthetic drugs.
Western medicine is the most widespread and is the worldwide rule even in coun-
tries where alternative medicine is widely practiced. The so-called alternative treat-
ments come from the oldest treatments based mainly on plant properties, meditation,
and other ancient techniques. They are treatments that were perhaps the norm in
other times and never disappeared, remaining as exceptions. Due to fashion or the
failure of synthetic drugs, they often come back and become more common. In fact,
in Latin America, multiculturalism and pluri-ethnicity show diverse medical sys-
tems (Duarte-Gómez, 2003). Examples include indigenous medicine, home medi-
cine, yoga for stress relief, herbal teas for various conditions, acupuncture, and
cannabis for pain relief.
Beyond the fact that almost half of the world’s population does not have access
to essential health services, the exceptions in medicine can be clearly seen in dis-
eases. First, let us talk about a group collectively referred to as “rare” diseases.
492 8 Beyond Biology

8.2.1.1 Rare Diseases: A Way to Better Understand Common Patterns?

When thinking about exceptions in medicine, one of the most concrete examples is
“Rare Diseases,” which involve uncommon conditions (Table 8.1). These diseases
affect the health to a greater or lesser extent of those who suffer from them. Different

Table 8.1 A list of examples of rare diseases. This table aims to understand the cause, and impact
of rare diseases on the population and the individual
Population
Rare disease Cause Effect impact Diagnosis
Consequences References
Marfan Genetic Weakness in Affects Clinical
Affects quality Dietz,
syndrome mutation connective 1 in 5000 evaluation,
of life and (1996),
tissue, affecting to 10,000 genetic
increases the Pyeritz,
the eyes, heart, people testing
risk of (2000, Du
lungs, bones, worldwide potentially et al.,
and skin fatal (2021)
complications
such as aortic
rupture
Huntington’s Genetic Degeneration of Affects Gradual loss Vonsattel
disease mutation nerve cells in 1 in of the ability &
the brain, 10,000 to control DiFiglia,
affecting people movement and (1998),
movement, worldwide cognition, Walker,
cognition, and which can (2007),
behavior lead to Ross &
disability and Tabrizi,
death (2011)
Cystic Genetic Accumulation Affects Clinical Decreased life Kock &
fibrosis mutation of thick, sticky 1 in 2500 evaluation, expectancy Hoiby,
mucus in the to 3500 sweat test, and increased (1993),
lungs and other people genetic risk of serious Hodson
organs, causing worldwide testing complications et al.,
recurrent such as (2012)
respiratory respiratory
infections, failure
digestive
problems, and
other symptoms
Williams Genetic Cognitive and Affects Clinical Can affect Morris &
syndrome deletion learning 1 in 7500 evaluation, learning Mervis,
difficulties, people genetic ability and (2000,
distinctive worldwide testing social 2021)
facial features, adaptation,
and cardiac and and increase
blood the risk of
circulation cardiac and
problems blood
circulation
problems
8.2 R&E in Sciences More Closely Related to Biology 493

Table 8.1 (continued)

Population
Rare disease Cause Effect impact Diagnosis Consequences References
Gaucher Genetic Accumulation Affects Clinical Affects quality Lee,
disease mutation of a fatty 1 in evaluation, of life and (1982),
substance in the 40,000 genetic increases the Sidransky,
organs and people testing, risk of serious (2004),
tissues of the worldwide blood complications Pastores &
body, causing analysis such as organ Hughes,
liver and spleen failure (2018)
problems, and
bone and joint
pain
Tuberous Genetic Formation of Affects Clinical Can affect Gomez
sclerosis mutation benign tumors 1 in 6000 evaluation, learning et al.,
in various people genetic ability and (1999),
organs of the worldwide testing, social Crino
body, including imaging adaptation, et al.,
the brain, analysis and increase (2006),
kidneys, and the risk of Curatolo
lungs, causing serious et al.,
seizures, complications (2008)
cognitive such as organ
problems, and failure
other symptoms
Niemann-­ Genetic Accumulation Affects Clinical Can affect Kolodny,
pick disease mutation of lipids in 1 in evaluation, quality of life (2000),
cells, causing 150,000 genetic and increase Vanier,
neurological people testing, the risk of (2013)
and hepatic worldwide blood serious
problems, and analysis complications
pulmonary such as
dysfunction respiratory
Pompe Genetic Inability to Affects failure Mellies &
disease mutation fully 1 in Lofaso,
breakdown 40,000 (2009),
glycogen, people Kroos
causing worldwide et al.,
progressive (2012),
muscle Leslie &
weakness, Bailey,
respiratory and (1993)
cardiac
problems
(continued)
494 8 Beyond Biology

Table 8.1 (continued)

Population
Rare disease Cause Effect impact Diagnosis Consequences References
Tay–Sachs Genetic Accumulation It mainly Clinical It can affect Gravel
disease mutation of a fatty affects evaluation, the quality of et al.,
substance in the people of genetic life and (1991),
brain, causing Ashkenazi testing increase the Fernandes-­
progressive Jewish risk of serious Filho &
neurological descent complications Shapiro,
problems and and other such as (2004)
pulmonary rare ethnic respiratory
dysfunction groups failure
Rett Genetic Progressive Affects It can Hagberg
syndrome mutation neurological mainly significantly et al.,
problems, girls and is impact quality (1985),
including caused by of life and Smeets
motor, a mutation increase the et al.,
cognitive, and in the risk of serious (2012)
communication MECP2 complications
issues gene such as
cognitive and
physical
disability

countries and organizations have approximations for considering a disease rare (see
Richter et al., 2015). However, in general, it ranges from 5 to 86 per 100,000 people
(Nguengang Wakap et al., 2020; Richter et al., 2015). The approximate number of
rare diseases is not well defined, especially for their rarity, but ranges between
5000–8000 rare diseases. New rare diseases are discovered every year, and the truth
is that being exceptions as such, they do not have the entire research interest of
pharmaceutical companies or governments. This lack of interest arises mainly
because there is no business behind them due to the low sales of potential drugs
(Drummond et al., 2007). New drugs are being added to treat some of them (e.g.,
560 new drugs in 2015) (Phrma.org, 2021).
Rare diseases include Mendelian, infectious, or rare cancers (Haendel et al.,
2020). We can mention numerous possibilities resulting from viral or bacterial infec-
tions, allergies, degenerative diseases, and chromosomal disorders, among others
(Haendel et al., 2020; National Center for Advancing Translational Sciences, 2022;
Zhu et al., 2020). Mendelian diseases are somewhat easier to detect, as they appear
in the family in predictable proportions, do not appear in in-laws, and manifest at
approximately the same age (Buchanan et al., 2006). In contrast, complex diseases
are the most common diseases affecting the population. The cause is multifactorial
and depends on a combination of genetics, environment, and lifestyle factors, among
other factors (Craig, 2008). Examples of the latter are complex chronic diseases
such as cardiovascular conditions, asthma, diabetes, Alzheimer’s disease, cancer,
and psychiatric diseases that have become the focus of attention of epidemiologists
and geneticists as they are more prevalent in health importance (Hunter, 2005).
8.2 R&E in Sciences More Closely Related to Biology 495

Despite investment in research, the causes of these diseases remain poorly under-
stood (Buchanan et al., 2006). Here, it is evident from the book’s point of view that
rare diseases are the exception in medicine, and complex diseases are the rule.
Nevertheless, we should focus on the fact that the method of diagnosis and the fea-
sibility of obtaining economic benefits for pharmaceutical companies are closely
linked to labeling diseases as one or the other. We should not be surprised to find in
the future that the casuistry of rare diseases is not as low as we think (McMaster,
2021), similar to what we will discuss with autism spectrum diseases later on.
From a scientific point of view, these diseases can often be the gateway to under-
standing poorly understood biological and physiological pathways. This process is
similar to the study of teratologies to better understand some ontogenetic develop-
mental processes, as discussed in Chap. 5. Here, we highlight what has been com-
mented on in some journals and blogs (Craig, 2008; Peltonen & Uusitalo, 1997;
Reid, 2016). The study of the molecular biology underlying “Rare Diseases” helps
detect dysfunctions and novel biochemical pathways, which indirectly contributes
to a better understanding of biological processes in general (Berman, 2014; Griggs
et al., 2009). Many important discoveries arising from the study of rare diseases
often contribute to a better understanding of more common conditions (Griggs et al.,
2009). In his popular science blog, J. Reid (2016) highlights the benefits of these
studies, particularly in clarifying the normal functioning of biochemical patterns.
For example, the study of mutations on the ob gene encoding leptin. This dys-
function produces insulin resistance and endocrine abnormalities. The study of con-
genital leptin deficiency and other Mendelian obesity disorders has taught much
about the processes that generate overweight and obesity, such as those associated
with insulin (Blüher & Mantzoros, 2009; Fatima et al., 2011; Reid, 2016). Thanks to
advances in technology and molecular analyses, studies of rare diseases have been
favored by advances in genetic labeling techniques, such as labeling with microR-
NAs (miRs). Recently, the expression of miR patterns in body fluids demonstrated
their importance as noninvasive biomarkers for different diseases (Salvatore et al.,
2011). The human genome project demonstrated that RNA transcripts are more
numerous than protein-coding genes. This fact has generated a paradigm shift where
the rule was that one RNA produced one protein (Hanna et al., 2019). The miRs are
regulated and transcribed in the same manner as protein-coding genes. miR biogen-
esis involves separate transduction and processing steps in which the active site of
20–22 nucleotides is extracted from a longer hairpin RNA precursor. These 20–22
nucleotides are fused into partial duplexes between the short RNAs and the untrans-
lated regions (UTRs) of targeted mRNAs, leading to silencing mRNA translation in
mammals (Salvatore et al., 2011). miRs regulate gene expression and are related to
many biological activities, such as tumorigenesis, immune response, neurotransmit-
ter synthesis, insulin secretion, and even circadian rhythm (Zhou & Yang, 2012).
Identifying these disease-linked mRNAs is crucial to understanding disease patho-
genesis at the molecular level and helps design molecular tools for prevention, diag-
nosis, and treatment (Salvatore et al., 2011; Zhou & Yang, 2012).
Outside the technicalities, it is interesting to see that some diseases are rare in
some regions but not others. For example, Tay–Sachs is rare in the general
496 8 Beyond Biology

population but very common in the Ashkenazi Jewish group (Charrow, 2004;
Myerowitz & Costigan, 1988). Tuberculosis is rare in developed societies such as
the United States but is in the top 10 most frequent causes of death worldwide
(Harding, 2020). Another example is Zika or Malaria, which are rare in Europe or
the USA but very common in South America, Africa, or Southeast Asia (Beier et al.,
1999; CDC, 2022a; Kazmi et al., 2020; Kumar et al., 2012; Yakob & Walker, 2016).
Something similar is true for thalassemia. Thalassemia is an inherited blood disor-
der characterized by insufficient production of hemoglobin in red blood cells, which
is responsible for transporting oxygen to all cells. The severity of the condition can
vary, ranging from no symptoms or mild anemia to cases requiring blood transfu-
sions (CDC, 2022b). Between its two forms, the beta form prevails punctually
among the Mediterranean population (Greer et al., 2013), being relatively rare in the
rest of the world, except in the Maldives, where the highest concentration of affected
individuals is found (Waheed et al., 2016). With these examples, we see that the
rarity of a disease can also be contextual (Haendel et al., 2020).

8.2.1.2 Exceptions that are Becoming More Common in Medicine

Next, let us discuss some examples of exceptions that become progressively more
common in medicine. This shift includes certain diseases, medical conditions, and
the use of specific biomedical tools.

A Case in Point: Autism, Real Increase or Revision of Diagnostic Parameters?

In recent decades, there has been a noticeable rise in the diagnosis and prevalence of
disorders associated with autism spectrum disorders (Fombonne, 2009; Zeidan
et al., 2022). It is estimated that the worldwide prevalence escalated from 1/5000
cases (0.02%) in the 1970s to the current data, which is approximately 1/100 chil-
dren (1%) (Isaksen et al., 2013; Zeidan et al., 2022), a 50-fold increase. Even so, the
prevalence is still believed to be quite underestimated (Fombonne, 2003). However,
the question that quickly arises is why this increase occurred. Is it real? It is a subject
of heated debate, and although there are different hypotheses, most of them largely
point to methodological factors (Fombonne, 2009). The identification of cases has
been facilitated by the expanded concept of the autism spectrum, which now includes
individuals who do not exhibit apparent intellectual impairments. In addition, diag-
nostic criteria were expanded, and specialized services were developed to better
understand the pathology (Fombonne, 2001, 2003; Isaksen et al., 2013; Infobae, 2015).
Nevertheless, it is not ruled out that the condition has indeed escalated and that
environmental factors are causing this increase (Isaksen et al., 2013). Here, we see
that the disease is perhaps not more common; it did not go from being the exception
to the rule, but it did change the diagnostic paradigm and is now detected much
more frequently. The same can happen with many rare diseases that can change
their status from rare to more common as the diagnostic criteria are expanded, or
there are ways to identify the disease better.
8.2 R&E in Sciences More Closely Related to Biology 497

Immune Boosters: Who Says Vaccines Do Not Work?

Since the twentieth century, we have become accustomed to vaccines as an immune

booster that has saved countless lives (Kayser & Ramzan, 2021). This practice has
helped life expectancy grow and move beyond critical moments in early life where
death from infectious diseases was very high (Okwo-Bele, 2015; WHO, 2019). The
immunization schedule is estimated to save approximately three million lives
worldwide annually (WHO, 2019). We have seen that some diseases, such as
Smallpox caused by the Variola virus (Ray & Ryan, 2004), have been totally eradi-
cated, and others are almost totally controlled thanks to the herd immunity that
vaccines provide (Orenstein & Ahmed, 2017) (Fig. 8.1a–d). Methods of immuniza-
tion by inoculation are older than we think. In ancient times, different people around
the world used techniques to boost immunity (Kayser & Ramzan, 2021). Thus, the
attempts of humans to boost immunity are not a rare action but rather a rule, and
currently, vaccines are an essential part of our lives.Unlike the artificial processes of
immunization that have accompanied us in our history, gene therapy is writing the
history of medicine into the future (Sayed et al., 2022). We had already mentioned an
example of gene therapy in the section on rare diseases when we discussed
mRNA. This type of therapy is considered to be a paradigm shift in treating diseases
because of its precision in targeting treatment. Although there is much talk about it,
it is still in experimental stages, and there is still a long way to go. There are at least
two perspectives linked to our book on this subject. The first is that gene therapies

a b

c d

Fig. 8.1 Disease behavior after the development and introduction of vaccines in the UK. After the
introduction of vaccines, the diseases decrease their incidence and may have some breakouts but
not at the level seen before the development of the treatment. (a). Diphtheria. (b) Polio. (c)
Measles. (d) Pertussis. Credits: Creazilla (NA). (License: Public domain. https://creazilla.com/
nodes/19975-how-vaccines-work-vector)
498 8 Beyond Biology

will move from being rare or disease-­oriented treatments to becoming a regular part
of medical treatment and perhaps with room to expand to treating other diseases. The
other perspective is to see viral vectors as something valuable and good that does not
generate a disease (the rule until now) but, on the contrary, treats it and sometimes
even cures it. This change that leads to the use of this type of therapy responds, of
course, to the change in the use of technology and the advance of the same that makes
the identification, replacement, or arrangement of genetic sequences a daily work and
not confined to a “gloomy macabre” laboratory. We also must think that there will be
a radical change in disease treatment and precision medicine (Kosorok & Laber,
2019; Mirnezami et al., 2012). In the current paradigm, the rule is a kind of “one size
fits all approach” where the disease is considered, and standard patient treatment is
applied. In the future, medicine aims to generate a health system where conditions
are treated considering individual differences shown as genes, environment, and life-
styles that the patient has and thus adjust the therapeutic precision (Ashley, 2016). As
precision therapy proves to be more effective, broad-spectrum medication may
become increasingly rare. Alternatively, at the beginning, the cost of precision ther-
apy will be high, remaining a rarity for most people.

Human Enhancement: “Pimp My Body”

Human enhancement is a discipline of medicine and bioengineering that seeks to

develop techniques and technologies to enhance and surpass normal or diminished
physical and intellectual capacities due to some conditions (Brey, 2009). It combines
disciplines such as biotechnology, nanotechnology, genetic engineering, and pharma-
cology. This possibility of altering human capacities deserves a rethinking of the objec-
tives of medicine. Many transhumanists believe this would generate a new race of
posthumans with above-­average characteristics. However, if we think about it, is a
human being with an artificial organ or a robotic prosthesis much different from a per-
son with an immune system boosted by a vaccine or someone who boosts their eye-
sight with glasses? Everything indicates that clinical advances since the first half of the
last century produced accelerated progress that has led us to the formation of “super-
people,” with improvements that take us back to science fiction (Bostrom & Roache,
2008). From the point of view of the book, these “superhumans” can be considered
exceptions, but in the future, perhaps they will become the new rule. We can venture
that in the long term, they could end up outnumbering and even displacing “normal”
humans (which they would no longer be). However, for something like “superhumans”
to become the rule, human societies must overcome many legal and ethical issues, such
as identity, dignity, equality, and the psychology of people (Brey, 2009).

8.2.1.3 On Changing Conceptions in Medicine

As in the previous case, the reverse situation also occurs in medicine, where specific
patterns (or medical principles) become progressively less common and end up
being rarities or disappear. To illustrate this point, we will focus on the change in
8.2 R&E in Sciences More Closely Related to Biology 499

diagnostic criteria and medical recommendations in three common aspects of daily

life: the problem of obesity, smoking, and how childbirth is treated.

Changing Perceptions of Fatness/Obesity

The perception of overweight or obesity has a strong cultural component, but it is

thought to have varied over time in different cultures (Sobal, 2001). It is known that
in many ancient cultures, there was a preference for women with a fat or moderately
overweight phenotype (Bray, 1992). There are ancient representations of female
icons associated with fertility, such as the Venus of Willendorf, which is approxi-
mately 25,000 years old. Similarly, today, some cultures still worship figures with a
specific pattern of fatness over thin or skinny bodies, which they find even deroga-
tory (Renzaho, 2004). For example, in sub-Saharan Africa, being overweight and
obese are signs of social status. Hispanic families and families of European descent
in America tended to see a certain amount of overweight as a sign of bodily
well-being.
Obesity and being overweight have started to be seen as health problems in the
last three decades (Renzaho, 2004). However, Hippocrates, the great physician of
antiquity, already saw obesity or being overweight as a problem and identified good
nutrition, exercise, and sun exposure as solutions to that problem (Alzate-Yepes,
2019; Renzaho, 2004). However, at that time, it was not a widely contemplated
disease. Toward the beginning of the twentieth century, obesity started to attract the
attention of the medical community. Nevertheless, it was still a powerful sign of
social status in areas such as North America (Grivetti, 2001; Renzaho, 2004). The
two world wars brought much poverty, hunger, and disease, which emphasized the
relationship between fatness and health, deeply rooted in European immigrants who
escaped the war.
Suddenly, there was a marked change in conception. Fatness went from being a
common rule to being an exception and was stigmatized by society far beyond the
health problems it can cause. After the Second World War, beauty criteria changed
radically, strongly driven by the stereotypes that appeared in advertising, especially
on television. Dancers, artists, models, and sports athletes were seen there, reinforc-
ing the stereotype of the slim body (Renzaho, 2004). These stereotypes have not
changed and continue to be a source of disconformity among people (Murnen &
College, 2019). However, stereotypes have not changed in areas such as those
inhabited by sub-Saharan tribes in Africa and areas of Polynesia, among others.
These ethnicities continue to value the image of being overweight and relate it to
well-being and power. Furthermore, these stereotypes migrate with the people. This
is how in neighborhoods such as the Bronx in New York, we can see admiration for
bodies that in other cities such as Buenos Aires would be cataloged as overweight.
This is a heritage that Africans brought to America and is still reflected in their
African–American descendants. Although currently, the rule seems to be admira-
tion and reflection in thin and athletic bodies, there are many exceptions in groups
that continue to see this type of physiognomy as derogatory.
500 8 Beyond Biology

From the Prescription of Cigarettes to the Use of Medical Cannabis

Many drugs, such as cocaine, nonmedical marijuana, ecstasy, and opium, are illegal,
and their eradication is an issue on the agenda of the governments of almost all coun-
tries. Nevertheless, we have “legal drugs” such as cigarettes and alcohol. History
shows a substantial shift from rule to exceptions in the use of cigarettes and other
compounds such as cannabis. Today, smoking has a rather negative connotation in the
general public. However, there was a time when doctors recommended smoking
(Little, 2019). As much as this may seem like negligence, it was a move by the skillful
marketing minds of the tobacco companies. In the first half of the twentieth century,
smoking was seen as a sign of status and elegance and was often recommended for
health (Martí, 2016). Between 1920 and 1950, it was common for doctors to prescribe
smoking to reduce stress, throat conditions, cancer, and halitosis and even to improve
the appearance of teeth (Martí, 2016; Seoane, 2017). Tobacco companies drove the
business and used these practices to their advantage by using health professionals in
advertisements, studies, and totally manipulated surveys (Seoane, 2017) (Fig. 8.2a–d).
By 1950, studies were accumulating, suggesting tobacco’s harmful effects on
health. In response, tobacco companies started fierce campaigns where not only
health professionals appeared but also showbiz stars, children, and even babies talk-
ing about the benefits of cigarettes smoked by their parents. In 1939, Franz Hermann
Muller warned that most lung cancer patients were smokers. This observation was
joined by epidemiologists Richard Doll and Bradford Hill, who in 1951 published a
study showing that 99.5% of lung cancer patients were smokers. Although tobacco
is still consumed, the perception has changed substantially. Currently, apart from
changing the consumption of cigarettes to electronic cigarettes, patches, or chewing
gum, smoking has decreased thanks to restrictions in different countries, but tobacco
is still consumed, and many are addicted.

a c d

Fig. 8.2 Some old cigarette advertisements in which doctors or athletes encouraged smoking. (a)
Advertisement for Piccadilly cigarettes featuring a doctor, a figure skater, and two trapeze artists
(Credits: Wellcome Images). (b) Image of a cigarettes ad, showing the many “benefits of smok-
ing.” (c) Another advertisement suggesting that athletes and doctors prefer smoking a particular
brand of cigarettes (Credits: Don O’Brien). (d) The advertisement claims that the doctor’s choice
is the American choice (Credits: Joe Haupt)
8.2 R&E in Sciences More Closely Related to Biology 501

Cannabis has been consumed by humans for 4000 years. It has been a therapeutic
agent for different conditions, as with many other natural products used in tradi-
tional medicine. In the nineteenth century, cannabis extracts were used in Europe
and the United States for myalgias and nausea (Quiñones-Laveriano & Catacora-­
Villasante, 2019). Cannabis was vetoed by the United Nations Single Convention
on Narcotic Drugs in 1961 (Lande, 1962). Relatively recently, there has been a
resurgence of general interest in cannabinoids to treat neurological conditions and
especially chronic pain (Hill et al., 2017; Leonard, 2022). Thus, we see how can-
nabis has been a rule of use in the East (Brand & Zhao, 2017) but a rarity in the
West. It then moved from more widespread use to a new exception by being vetoed
and is now gaining momentum globally to perhaps become normal or a rule in pain
management. While its reported efficacy is mixed, many patients claim it has been
a major therapeutic game changer that has improved their lives.

Maternity and Childbirth

Some examples linked to motherhood show a change from rule to exception. First,
new generations in developed countries tend not to have many children or not to
have them at all. This idea arises because raising a child is too costly, and people are
encouraged to reach projected goals efficiently and not to meet the standards needed
by society (Hoffower, 2022; Jagannathan, 2021). This conception is responsible for
the birth rate drop in many countries (Nargund, 2009). It is clear that in the last
century, the idea reigned that to comply with the precepts of society, a person had to
get a partner, get married, buy a house, have a child, and maybe buy a dog. This
conception has been changing considerably, and today singlehood or the desire not
to be a parent is much more common or not so negatively viewed than it was a few
years ago.
The way of being born has also undergone changes with the new perceptions of
parenthood. Before, births were natural except in situations where the child or the
mother was in danger. Today, there is a tendency for deliveries to be by cesarean
section and already scheduled in advance by the doctor. In fact, cesarean delivery
rates have increased from 12% of total deliveries to 21% by 2015, reaching 44% in
the Latin American region (Sandall et al., 2018). This change has advantages and
disadvantages. On the one hand, if natural childbirth is opted for, the mother has
labor that can extend for long hours and often ends in the same way in a cesarean
section. If a cesarean section is chosen, at the moment, there is no pain, and the
delivery is fast. However, the postoperative period is usually long and slightly pain-
ful. It has been seen that babies born from cesarean sections may have subtle health
alterations resulting from abnormal exposures to hormones and bacteria during
delivery (Sandall et al., 2018). Regardless of the method of birth, the perception of
how to feed them has also changed. The rule used to be that you could feed pro-
fusely without too much of a set schedule. Today, specialists suggest a progression
of foods to avoid problems in the digestive system, allergies, or intolerance to cer-
tain foods. These are everyday examples of changes from rule to exception in the
health field.
502 8 Beyond Biology

8.2.2 Physics Miscellaneous

As we saw at the beginning of the book, we are generally accustomed to believing

that over time, there are no exceptions to the theories and rules that are proposed in
exact sciences. Although we know that theories can be modified or discoveries can
be made, we tend to think these rules are a pattern that will not change and remain
static. In biology, we saw countless exceptions to the patterns we thought were rules
throughout this book. Although exceptions may be less likely in harder sciences,
such as mathematics and physics, this does not mean that there are none, and this is
what we will try to explain below concerning physics.

8.2.2.1 Triple Point in Thermodynamics

In the 1870s, physicist Josiah Gibbs found that a substance in thermodynamic equi-
librium can be found simultaneously in three phases. This phenomenon can be
observed in water, for example, which, upon reaching its “triple point” at a given
combination of pressure and temperature, can exist as a solid, liquid, and gas simul-
taneously, a kind of “physical Schrödinger’s Cat.” These so-called triple points also
occur in other substances, such as solids with different stable crystalline structures.
The premise is that they always exhibit at most three phases simultaneously. Even
in liquid crystals, for which it is known that they can adopt several phases depend-
ing on the arrangement of their molecules, never more than three phases were
observed simultaneously (Cemič, 2005; Dehoff, 2005; Preston-Thomas, 1990).
However, this rule is now being considered based on new findings. Published results
show a system consisting of a mixture of elongated molecules and spheres of a
polymer that are dissolved in a liquid. Because of this combination, the elongated
molecules behave like liquid crystals. Furthermore, when there are sufficient elon-
gated molecules in the solution, they are arranged parallel. However, since there are
also spheres in the polymer, when the shrinkage of elongated molecules increases,
they constrict the spheres. Therefore, two new liquid phases associated with the
elongated molecules appear, and two solid phases with different crystalline struc-
tures are added. This dynamic results in a “quintuple point.” Although it exists only
as a simulated system, scientists believe it should be possible to reproduce it in the
laboratory (Peters et al., 2020). This discovery calls into question one of the laws of
thermodynamics, which could be transformed from a rule to an approximation.

8.2.2.2 The Direction of Time

Continuing with the laws of thermodynamics, the second law states that entropy can
only increase and never decrease (Wark & Richards, 2001). Moreover, from this state-
ment, it is understood that time moves in only one direction, the direction in which
entropy increases. However, it should be noted that the laws of thermodynamics were
established during the industrial revolution when work was being done on
8.2 R&E in Sciences More Closely Related to Biology 503

manufacturing steam engines that could be more efficient in energy use. Currently, the
British scientist John Barbour questions this premise of time moving in one direction
and suggests a new conception of time in his book “The Janus Point: A New Theory of
Time,” where he explains how time could move in two directions (Barbour, 2020).
For Barbour, the second law of thermodynamics was thought for machines where
energy and heat were confined in a bounded space. However, in an unbounded
space, particles can continue to travel and join others to form more complex struc-
tures, which will grow in all directions of space and time. That is, the passage of
time would not be an increase in entropy but an increase in complexity, without
limits. Confirming this hypothesis would represent an exception in the traditional
vision of physics. It would show an increasingly complex, structured universe that
is growing without borders.

8.2.2.3 Newton’s Laws and the Motion of Bodies

At present, we consider that the laws formulated by Newton provide answers to most
of the problems related to moving bodies, but there are also exceptions. On the one
hand, they allow us to explain the motion of stars, for example, or of projectiles created
by man or the mechanics of machine operation. However, classical dynamics is only
valid for inertial systems, i.e., systems that move at a constant velocity and whose
velocity is far from the speed of light (Serway & Jewett, 2009). An example of this
type of system could be the earth, which, despite being under translational and rota-
tional accelerations, can be considered for an observer as an inertial reference system
due to the magnitude of these forces (Sears et al., 2013). The truth is that, in reality,
there is always some force acting on bodies. Therefore, finding a system that can be
treated as an inertial system is challenging. These facts show that although Newton’s
laws are rules, they are based on models where certain variables are taken into account,
as in this case of motion. If those variables are not fulfilled, the motion of the bodies
will not be governed by that rule either. Therefore, they could be seen as exceptions to
it. Once again, we can see that every general rule has its exception and is not fulfilled
on certain occasions since the given conditions are outside those necessary for this to
occur. Although they are universal rules postulated long ago and that cannot be dis-
proved, there will always be something that they cannot explain: the exceptions to
the rule.

8.2.3 Chemical Miscellanea

8.2.3.1 A “Macropattern” of Diversity: The Periodic Table

The history of the discovery of chemical elements and the periodic table represents
the quest for a universal language, enabling us to comprehend the composition of
everything that exists and is known today. It is the search for the creation of a rule
that made it possible to order so we can understand new discoveries. The story
504 8 Beyond Biology

begins with the Greeks, who proposed the existence of the essential components of
everything, proposing the four elements as the primary builders of everything:
water, earth, fire, and air. From this first theory, which at that time could be consid-
ered a rule, in the Middle Ages, alchemists became interested in the mixture and
transformation of elements to obtain the most precious metal: gold. In the search
for gold, the alchemists identified up to 13 elements known today, such as tin,
arsenic, and silver. Moreover, most known chemical elements were discovered dur-
ing the Industrial Revolution due to the need for metal extraction methods
(Santos, 2010).
The periodic table we have today comes from the table devised by the chemist
Dimitri Mendeleev, based on Dalton’s atomic theory, who published the atomic
masses of certain elements. Mendeleev’s periodic table orders the chemical ele-
ments according to their atomic weight and valence, which defines the combining
power of the atoms. We now use a more extended version of the periodic table,
where the elements are arranged according to atomic number, electron configura-
tion, and chemical properties. The distribution of the elements horizontally in peri-
ods responds to the energy level of the atoms. Groups of elements of equal valence
(corresponding to the number of outermost electrons) are arranged vertically, as
proposed by Mendeleev, which has been a rule for the arrangement of elements
according to their properties (Garbayo & Fernández, 2012).

Exceptions in the Chemical Elements

The Bohr model of the atom describes the atom as having a nucleus composed of
protons and neutrons, with circular electron shells, similar to the orbits of planets.
Each electron shell’s energy level increases as they move away from the nucleus. To
have the most stable and lowest energy configuration, the electrons fill the shells
inside out. The number of electrons in the outermost shell is known as the valence
shell. As a general rule, atoms are most stable when their outermost face is com-
plete, with the most essential elements needing eight electrons in this shell to be
stable (Lewis, 1916). This is known as the octet rule, which we will mention in the
next item. However, there are exceptions for some elements in the table where this
order of filling orbitals with increasing energy is not fulfilled. This exception is
because the attractive forces of protons and electrons are added to the interference
of the lower electron shells that cause energy deviation. The most stable configura-
tion differs from the expected configuration (Ule, 2019). These elements are differ-
ent from the rest, and we can observe an exception to the configuration described in
general (the “rule”) that is needed for the stability of the elements. Therefore,
although the model described by Bohr and the ordering in the periodic table follow
a specific pattern, sometimes these general patterns also have exceptions or oddities
that are out of the ordinary. This example makes us wonder whether there truly is a
general pattern that encompasses a totality or whether these patterns are always
generalities that group the majority but from which something different always
escapes.
8.2 R&E in Sciences More Closely Related to Biology 505

8.2.3.2 Witness Case: Octet Rule

This rule mentioned above was proposed by Gilbert Newton Lewis in 1916 and
explains how the atoms of chemical elements combine. The atoms of the different
elements tend to maintain a stable electronic configuration by locating 8 electrons
in their last energy levels. Therefore, elements with high electronegativity tend to
gain electrons until they reach the octet, while those with low electronegativity tend
to lose them for the same reason. Due to this phenomenon, molecules can acquire a
stability similar to that of noble gases (elements located at the right end of the peri-
odic table). This rule makes it possible to understand how atoms form their bonds
and the behavior and chemical properties of the resulting molecules (Lewis, 1916).
Although it predicts the behavior of many substances, the octet rule has several
exceptions in compounds that can reach stability without the need to have eight elec-
trons in their last energy level. Phosphorus (P), sulfur (S), selenium (Se), silicon (Si), or
helium (He) are hypervalent elements, i.e., they can accommodate more electrons. On
the other hand, hydrogen (H) can accept a maximum of two electrons in a chemical
bond. Beryllium (Be) is stable with four electrons, and boron (B) is stable with six
electrons (Myers, 2003). As mentioned above, these exceptions demonstrate once again
that the rules try to group or encompass, in this case, most of the chemical elements.
However, it cannot capture the totality of the cases because most of the chemical ele-
ments respond to that pattern or rule. There will always appear exceptions that make us
go out of the common and that are not part of the majority. In this chapter, we see that
these exceptions occur not only in biology but also in other sciences, such as chemistry.

8.2.3.3 An Example of a “Duality” Rule and Exception

Hydrogen is the simplest of the atoms, since it has only one proton, electron, and its
most common isotope, protium, unlike other isotopes, does not have any neutrons in the
nucleus. It cannot be framed in any periodic table group, but it is often placed in group
1 (or family 1A) because it has only one electron in the valence shell. It is interesting to
note that six elements (C, H, O, N, P, and S) make up 99% of all living matter. The atoms
of these elements are tiny and form strong, stable covalent bonds. Except for hydrogen,
they can all form covalent bonds with two or more atoms, giving rise to the complex
molecules that characterize living systems (Curtis et al., 2008). However, hydrogen is
the most abundant chemical element in the universe, appearing in more than 75% of
matter mass and representing more than 90% of the atoms. Although it is not very reac-
tive under normal conditions, it forms a multitude of compounds with most chemical
elements. Because it has a relatively simple atomic structure, with a single proton and a
single electron in its most abundant isotope (protium), the absorption spectrum of this
atom could be explained quantitatively. This fact was the central point of Bohr’s atomic
model, a fact of great importance in developing the theory of atomic structure (Thomas
Jefferson National Accelerator Facility — Office of Science Education).
What we want to call attention here is that we have a unique chemical element,
not classifiable like the others in the table. Due to its notorious simplicity, it does not
506 8 Beyond Biology

behave like other elements essential for life but is the most abundant and can form
multiple compounds. In other words, from chemistry, we have in this element the
“duality” of something unique, different from all the rest (everything is unique, but
this element stands out) but at the same time common: “Rarity from the qualitative
(i.e., simple), but pattern from the quantitative (i.e., abundance).” This example
shows us again that something can be pattern and rarity simultaneously, depending
on the variables or the focus we are concentrating on.

8.2.4 Geological and Related Notes

8.2.4.1 The First Law of Stratigraphy

This law was first postulated in the seventeenth century by the father of geology,
Nicholas Steno, who stated that every rock stratum is older than that which overlies it
and younger than that which underlies it. It responds to the process by which the
eroded materials of already existing rocks will be deposited on each other over time.
It is a law or rule that allows us to think and reconstruct the landscape and its history
from the occurrence of changes and deformations of the rock structure. However,
many situations showed that the strata did not respect a consecutive order according
to what would correspond to their relative ages. These situations were exceptions to
the general rule, which had not been considered previously. In some circumstances,
tectonic deformations after the deposition of the substrate may cause the position of
the observed layers to be somewhat reversed. Therefore, they could not be explained
by this phenomenon in the same way as in other cases. Because of this fact, the first
law of stratigraphy had to be modified to include exceptions not considered before.
Thus, the law now postulates that “every stratum is older than the one overlying it and
younger than the one below it, as long as no tectonic deformations have taken place
after the deposition of the strata” (Press & Siever, 2000). Here, the general rule has
exceptions. Although they were somehow considered in the statement of the law, they
are situations that are far from what could be the pattern in an ideal condition or model.

8.2.4.2 The Age of Fossils and Strata

Biostratigraphy is the science that studies the distribution of fossils in rocks, allow-
ing us to assign an age to them according to the evolutionary degree of the fossilifer-
ous assemblages. The oldest living communities are arranged in lower strata and
usually represent a lower diversity than the most modern ones, showing correspon-
dence with biotic succession (Cabrera et al., 2018). Currently, geologists and pale-
ontologists are guided by the international chronostratigraphic table, a permanently
updated resource that contains all the necessary geochronological information and
rock succession worldwide (Cohen et al., 2013). As living beings evolve, the ages of
the successive layers of the Earth’s crust can be perceived according to the associa-
tions with the fossils found there. However, in this rule, we also find exceptions. In
8.2 R&E in Sciences More Closely Related to Biology 507

this case, they are given by organisms that have persisted for a long time without
changes, and some still exist today (Beierkuhnlein, 2007; Lomolino et al., 2006).
These are the so-called “living fossils” we have already mentioned in previous chap-
ters. Let us recall the ginkgo tree among plants and the nautilus in the group of
invertebrates dating from the Paleozoic. Among the vertebrates, coelacanths (with
much diversity between the Paleozoic and Mesozoic) and tuatara (recorded from the
Jurassic and now confined to New Zealand), among others, remain (Ward, 1984;
Werth & Shear, 2014). These “living fossils” would represent an exception to the
rule of biostratigraphy and a problem since, by remaining unchanged, they give no
possibility of knowing the age of the stratum in which they are found. Here, we have
one more example that every rule can have its exception and that the rules are never
100% accurate in regard to covering all known cases in the different sciences.

8.2.5 Astronomy Miscellany

The influence of celestial bodies on the earth is undeniable. The sun gives us light
and warmth that allows plants to grow and gives us a sense of security about the
night, just as the moon influences the tides and eclipses that generate changes in the
behavior of animals. With these basic premises, our ancestors assumed that the posi-
tion and relationship between the sun, the moon, and the other planets (Luminaries
sensu Kunth & Zarka, 2005) would influence various terrestrial events, human psy-
chology, and the destiny of people (Zarka, 2009). The position of these luminaries
at a particular point in time and space could be calculated, and their graphical rep-
resentation produces the horoscope (Greek hora+skopein = hour+examine). Both
astrology (the study of the heavens) and astronomy (the writing of the heavens) have
a shared history from antiquity to the Renaissance (Zarka, 2009). The Renaissance
saw the appearance of telescopes and the adoption of more scientific study param-
eters over preconceived esoteric ideas. Thus, astrology was left aside, and astron-
omy became much more robust. We see how astrology was the rule in ancient times,
with the lack of 100% scientific studies. In fact, many courts and kings had their
own astrologers who advised them in decisions on social, economic, harvest, and
war matters. Such is the case of the German astronomer and mathematician Johannes
Kepler, who, even without being totally convinced of the discipline, was an astrolo-
ger to the court of Emperor Rudolf II in Prague (Field, 1984; Zarka, 2009).
Moreover, physicians of antiquity diagnosed and prescribed remedies for ill-
nesses based exclusively on the person’s horoscope. At that time, astronomy, medi-
cine, and astrology went hand in hand. Today, those rules have changed, and
astronomy and medicine are strong scientific disciplines that are totally separate
from astrology, which has been relegated to pseudoscience. However, for ordinary
people, reading the horoscope in newspapers is still helpful, and many people still
trust the predictions of an astrologer to make essential decisions in their lives.
The universe is not exempt from laws, rules, exceptions, and changes from one
to another due to scientific advances. Physics in the universe was, is, and probably
will always be the same. Many phenomena can be described with Newton’s
508 8 Beyond Biology

equations. Other more complex phenomena escape the analysis of Newton’s laws
but are addressed by Einstein’s theory of relativity, which in simpler processes is
equated with Newton’s laws. If we look for rules toward the beginning of the cre-
ation of the universe, we will see that at the beginning, it was a chaotic furnace of
space, mass, and energy condensed in an infinitesimal point. Obviously, there were
no galaxies, stars, or planets (Ratra & Vogeley, 2008). After the Big Bang, the uni-
verse began to expand and cool. That is still the rule, and it is thought that the uni-
verse could expand infinitely at a slow speed. Another rule in the universe is the
presence of hydrogen clouds, which have been noted to exist everywhere. As we
said, hydrogen is ubiquitous in the universe, and helium and lithium are the main
atoms formed in the Big Bang (Turner, 2009). Let us remember that hydrogen is a
very reactive gas. However, the hydrogen nucleus of Jupiter behaves like a semiliq-
uid metal, creating a substantial electromagnetic field (Nellis, 2000). This phenom-
enon, among other things, is the cause of very particular features in some of its
moons where we see that this influence generates the melting of ice sheets forming
subterranean seas (Chap. 7) or volcanic activity by melting deep rocks.
What about the other atoms that we know of the periodic table? They form in the
heart of stars and, as a rule, are scattered across the universe when they explode
(Cox, 1989). Another singular rule that often goes unnoticed is that in the universe,
spheres are the natural rule (Cain, 2014; Tyson, 2019). Gravity is responsible for
molding objects into this shape. Low gravity causes the shapes to deviate from a
sphere for objects with more irregular shapes, such as the moons of Mars, Phobos,
and Deimos (Tyson, 2019). Seems that flat planets should be an exception to this
premise. Masses of gas can also coalesce into spheres of gas that form stars.
If we think of exceptions or oddities in the history of the Universe, perhaps the
most obvious one is that at the beginning, after the Big Bang, all the cosmic struc-
tures that we study today did not exist. We know that it was because it started from
the subatomic particles, a path that led to galaxies, stars, planets, and everything that
exists today in the Universe, whether we can measure, identify, or not. We can also
cite as an oddity the double star systems where one sphere exerts a significant gravi-
tational force and the other sphere is distorted by it (Tohline, 2002).
Another rule that appears in the Universe is the gravitational influence of dark
matter (Tucker & Wang, 1998). We do not know what it is, but we know its influ-
ence from gravitational effects. It does not influence at the planetary level, for exam-
ple, but it influences the stars’ motion at the galaxy’s center (Pitjev & Pitjeva, 2013a,
2013b; Tyson, 2019). On the other hand, it is known that the force of gravity
decreases its effect with distance. As an exception, we see that stars at the edges of
galaxies move fast despite the greater distance to the galaxy’s center (Tyson, 2019).
Here, the dark matter would be involved, which is not identified, but its influence is
measured.
We all know or think we know that the speed of light is constant. At least, it is
strongly suggested. However, there are less common theoretical circumstances
where the speed of light varies and therefore is not a constant (Farrell & Dunning-­
Davies, 2004) and is proposed as an alternative solution to some theoretical equa-
tions (Ellis & Uzan, 2005). A rare coincidence is that the Sun, Moon, and Earth have
8.2 R&E in Sciences More Closely Related to Biology 509

a very particular combination of size and distance that allows total eclipses to be
seen. This combination, at the moment, is almost unique in the Universe (Tyson,
2019). These were scattered examples that show rules and exceptions at the astro-
nomical level. These examples show how we can find rules and exceptions
everywhere.

8.2.5.1 Some Dynamics between Rules and Exceptions in Astronomy

It is possible to appreciate many changes from rule to exception and vice versa
regarding our knowledge of the Universe. Perhaps not because of a radical change
in the natural behavior of the Universe but rather because of changes due to scien-
tific and technological progress from antiquity to the present.
To cite an example of a change from rule to rarity or exception of nature, we can
comment on the collisions of asteroids or other celestial bodies. Five hundred mil-
lion years ago, after the formation of the solar system, the Earth was continuously
bombarded by space debris still wandering in space. In fact, the Earth raised its
temperature by friction as chunks of material entering the atmosphere generated
heat and then fused with the crust, forming complex molecules (Tyson, 2019). The
presence of an atmosphere counteracts to some extent the impact of a meteorite.
However, if this is at least 1 km in diameter, the result can be very significant.
Indeed, the history of the Earth confirms this. These phenomena, called, as we saw
in the first chapters, contingency phenomena, have had a radical influence on evolu-
tionary processes. For example, the tremendous collision of an asteroid toward the
end of the Mesozoic era (Chicxulub event 65 mya) in the area comprised today by
the Gulf of Mexico and its drastic effect on the atmosphere, solar irradiation, and the
direct impact of the explosion annihilating 70% of all species, including dinosaurs
(Chiarenza et al., 2020; Pope et al., 1997). The extinction of groups such as the
major dinosaurs was accelerated by this event, perhaps already affected by other
causes such as climatic cooling and the decline in herbivore diversity (Condamine
et al., 2021).
We can see then that this topic of asteroid collisions in magnitude can be consid-
ered from the perspective of our book as (1) a phenomenon that was possibly the
rule at the beginning of the Solar System, to become not an exception, but at least a
relatively rare type of event. (2) From the perspective of what concerns the planet
Earth and the evolutionary history of its life forms, it has been an exception to the
times it has occurred. However, when it happened, the result was fundamental, as a
contingency, for what would happen later with many animal and plant groups. This
is an indirect but crucial extraplanetary abiotic artificer in the direction of evolution
(Alvarez et al., 1980; Martin & Livio, 2022; Sleep et al., 1989). Concerning the lat-
ter, the idea that Jupiter had played a significant role in the development of life by
acting as a sizable gravitational shield that would deflect Earth-bound objects was
well established (Ward & Brownlee, 2000). However, in recent years, this idea has
been rigorously evaluated. While popular science still suggests that idea, there is
evidence that this is not the case with most bodies that can collide with the Earth
510 8 Beyond Biology

(Grazier, 2016; Horner et al., 2010; Horner & Jones, 2008, 2009, 2010). An excep-
tion is long-orbiting comets (Grazier, 2016).
In the latter context, currently, with the advancement of orbit detection tech-
niques, extraplanetary body directions, and mathematical models, a collision of the
asteroid named 99,942 Apophis with our planet is predicted approximately 2029
(Giorgini et al., 2005; Hirabayashi et al., 2021; Yoshida et al., 2021). It is speculated
that, depending on the collision angle, whether it disintegrates in part upon entering
the atmosphere, the results could be devastating. Perhaps a new contingency for
new directions in biological evolution? Much of this is not discussed or worried
about, but alarms sound on the effect on the human species (Morais et al., 2021).
The efforts to detect with precision aspects referred to this future impact and, even-
tually, to destroy it beforehand with weapons at the service of extraplanetary science
are the object of current research (Cheng, 2021; Maltagliati, 2022). Time is press-
ing. There are other potential collision cases cataloged as potentially hazardous
asteroids and comets (Petrov et al., 2018; Trigo-Rodríguez, 2022), some of which
may be in line with any of the inner planets of the solar system (Devyatkin
et al., 2022).
Returning to our topic of interest, there are many cases in astronomy of transi-
tions from rule to exception and vice versa due to changes in scientific conception
and technological progress. For example, we know of paradigm shifts concerning
the position of where we live (e.g., Kragh, 2006). Therefore, our planet was unique
at the beginning of our history as human beings. Then, in antiquity, other planets
were discovered, so the Earth went from being an exception (or something extraor-
dinary) to being a rule in the then-known universe. Thus, the geocentric theory was
created where it was postulated that although the Earth was not unique, it was the
center of the known universe, and the planets and the sun revolved around it. Then,
this changed once again, and it became known that the Earth and the other planets
revolved around the sun. The sun was considered unique, and then it was realized
that it was just another star in the universe. Thus far, the known universe was per-
haps the Milky Way, and then it was known that the Milky Way was a galaxy like
many others scattered throughout the universe. Finally, it is believed that there is
one universe, but there are theories that speak of multiple universes, which would
again take us out of our comfort zone. Although this was a crude and general account
that seeks to quickly show how changes in conceptions of nature cause a paradigm
shift of what is rule or exception, there are also more concrete examples.
In Einstein’s time, the rule was that the universe was static (Hoyle et al., 2000;
Sen, 1957). In fact, he developed a constant to fit within the statics paradigm (Harvey
& Schucking, 2000; Straumann, 2002). Hubble realized that the universe was
dynamic and expanding (Freedman, 2000), and Einstein regretted having generated
the constant to fit the paradigm. In fact, he called it “his biggest mistake.” However,
in recent years, Einstein’s cosmological constant has been used again in cosmic
acceleration studies (Barrow & Shaw, 2011a, 2011b; Peebles & Ratra, 2003).
Another rule is that galaxies are generally large clusters of stars. However, there
are galaxies called dwarf galaxies (Hodge, 1971; Mateo, 1998). They are natural
laboratories where galactic evolution models and paradigms can be evaluated
8.3 R&E in Other Knowledge Disciplines 511

(Haynes, 2018). Tyson (2019) suggests that the rule is the presence of dwarf galax-
ies in the universe due to the amount that exists, which is clearly much larger than
the so-called “normal” galaxies.
Astrophysics and cosmology are exciting fields that pose a significant challenge
to understanding nature’s workings. As we said at the beginning, the magnitudes are
titanic and challenge the mind. There is much room for the emergence of exceptions
and paradigm shifts, both associated with the progress of science and technology for
measuring phenomena. The rules are strong, perhaps because phenomena are gov-
erned by well-established laws such as those of physics. These laws, at least, have
been seen to work well in this universe. Interpretations could change a lot in the
future with the unification of the fields into a theory of everything and the discovery
of other universes where the laws we now use and know may vary (Halpern, 2004;
Tegmark, 1998).

8.3 R&E in Other Knowledge Disciplines

8.3.1 Social and Related Sciences

In the vast field of social sciences, we will focus on two examples, native cultures
and family conceptions, to show some cases of how social changes over time have
modified what was once common to new conceptions. Sometimes this dynamic
leaves the dominant patterns of the past as mere exceptions.

8.3.1.1 On Native Cultures and Concepts of Family

Native cultures are a clear example of how knowledge, including the ancestral wis-
dom of many peoples, has been lost over time and with them, at the cultural level,
patterns of tradition. Let us consider how the original cultures native to each region
have been modified over time. We can mention, for example, what we said about
ancestral medicine based on the use of plants or the modification of each tribe’s own
beliefs about nature. Additionally, the habits of life as the way of obtaining food, the
accepted clothing, beliefs, and festivities, to name some traditional practices of each
social group that have been lost over time. The arrival of new beliefs and customs
has caused many original cultures to be lost. Added to this are the racial and social
prejudices that native cultures have suffered and which, even today, with all the
progress in accepting the “different,” still continue to suffer, perhaps transforming
what were once rules into only exceptions. Native cultures have also been lost, not
only by the mixture of the new cultures that were able to arrive but also, for exam-
ple, by factors of migration of the youngest to large cities, loss of territories, and
modes of exploitation of natural resources (Porcel Moscoso, 2018). The point is that
traditions of different kinds that used to be the most frequent are no longer so or are
only maintained by the older generations. Of course, this loss of native culture
512 8 Beyond Biology

eventually leads to the loss of the cultural heritage of each place (Porcel
Moscoso, 2018).
On the other hand, the traditional family conformation pattern considered the
formation of monogamous marriage as what was accepted as valid in Western soci-
ety. It was considered the only moral and legal way to establish that type of relation-
ship. Marriage had to be socially recognized as such, and there was a sexual division
of labor (Manrique, 1996). The “high society” families married their children based
on economic and social interests, and it was typical that the first male-born child
received the family inheritance (Freijo et al., 2004; Manrique, 1996). However, over
time, the conception of the family has undergone a period of change. The two-­
parent, monogamous marriage model, considered the standard, has been adapting to
a new social structure. It is now coexisting with other forms of familiar assem-
blages, such as single-parent homes, extended families, families resulting from
assisted reproduction, families with adopted children, and homoparental families
(Meler, 2008).
What is different today is that family models are beginning to be decided by
individuals, and different behaviors are becoming increasingly frequent. For exam-
ple, some couples do not get married. Some couples remarry, and some couples are
open or exchange partners. There are homosexual couples and couples who live
apart. Many of these behaviors in the past were absolute rarities and even morally
condemned by society. Today, they are becoming increasingly frequent and
accepted.
The change in the conception of family is closely linked to the advance and
development of technology in several aspects (Manrique, 1996). Let us consider
prenatal diagnosis, which has transformed pregnancy into a family project, chang-
ing it from a natural occurrence to a planned event in many cases (Manrique, 1996).
Initially, this practice was almost inconceivable and remained exceptional. However,
over time, advancements in more precise and commonly used techniques have led
to its widespread adoption. Another significant change that took place, which is
involved in family development, is that women began to work outside the home in
paid jobs, something previously almost exclusive to men. This exception has
become a pattern in much of the world. Women no longer only take care of the chil-
dren and the housework but also “go out” to work, which granted them economic
independence and influenced their role in society.

8.3.1.2 Something that is an “Exception” Among Human Societies

What is considered acceptable among human behaviors varies among different

cultures, as norms are a social construct, and the meaning of what is right or wrong
differs from one society to another (Vera et al., 2012). Each culture establishes
different patterns of behaviors that may vary among members of society, consider-
ing, for example, children and adults or men and women (Maldonado, 2017). For
instance, certain behaviors that deviate from societal norms may be tolerated when
8.3 R&E in Other Knowledge Disciplines 513

displayed by a child. However, the same behaviors would be deemed unacceptable

if exhibited by an adult with fully developed psychological capacities. Although in
the world numerous cultures vary in the behavioral patterns accepted as valid,
behaviors such as rape, incest, theft, and murder are not considered acceptable for
any member of that society. These are conducts that threaten the social, legal and
political balance (Maldonado, 2017; Vera et al., 2012). Consequently, these behav-
iors are subject to direct penalties, such as legal repercussions and fines, or indi-
rect consequences through education, such as the case of familial or
community taboos.
Let us set aside extreme and punishable behaviors. The truth is that nearly all
people, if not everyone, regardless of their honesty, have at some point in their lives
told a lie or crossed some personal boundary. For example, we put ourselves at the
supermarket express checkout with more products than allowed, cut in line, miss
work without a justified reason, get on a plane without being called, cross a red
light, to name a few cases of minor transgressions. In this sense, studies have shown
that these small transgressions to preestablished rules are not associated with intel-
ligence but with some conditions, such as certain emotional states or the degree of
people’s creativity. Individuals who are more creative can (and usually do) break the
rules more easily. Another factor that can influence transgressions is the social
group to which we belong. If our group tends to engage in rule-breaking behavior,
there is a higher likelihood that we may do the same to fit in and be accepted, even
if we would not act that way in different circumstances. Indeed, there is a positive
aspect to consider. When presented with a challenge or a “dare to push further,” we
may break some established rules, but without causing harm to others. For instance,
this could involve going beyond the usual expectations and seeking greater personal
growth, satisfaction, and benefit.
Staying with the status quo is suitable and safe, but breaking the rules and going
against the expected, allows one’s talent to emerge and develop (Buckingham &
Coffman, 2012). Just not to be misinterpreted, think about many brand advertise-
ments where the slogan invites us directly or indirectly to break the rules. Let us see
some examples: Nike: “Just do it.”, Apple: “Think different.”, Adidas: “Impossible
is nothing. “, Virgin: “Screw it, let’s do it.”, Netflix: “Watch what you want, when
you want.”, Spotify: “Listen to what you love.”, Airbnb: “Belong anywhere.”, Uber:
“The way you move.”, Levi’s: “Live outside the lines.”, Nike Golf: “Never follow.”,
Under Armour: “Rule yourself.”, Oakley: “Eye protection for those who refuse to
conform.”. These brands encourage people to think out of the box, do what they
feel, be unique (outstanding), and never conform to the status quo.
Additionally, technological development is linked to essential changes in human
behavior. Access to rapid communication (television, internet, social media) and
travel around the world has enabled wide dissemination of new fashion standards
emerging in the “more developed” cultures. It drives others to follow the same can-
ons. Clothing, food, music, issues associated with art, and lifestyles in general are
gradually changing. What was once common or seemed strange to us perhaps now
no longer (Maldonado, 2017).
514 8 Beyond Biology

8.4 R&E Search on Subjective/Controversial Topics

8.4.1 Art and Culture

8.4.1.1 Image and Painting

Art can be seen as the most subjective form of human expression, as its purpose is
to evoke emotions and convey a unique perspective of the world. This is why terms
such as “exceptional,” “monstrous,” “ugliness,” “genius,” or “beauty” are frequently
found in artistic works. These concepts can be interpreted from various angles and
hold different values based on the historical context in which the artistic representa-
tions are analyzed (Kant, 1977; Rosenkranz, 1853; Tatarkiewicz, 1970). According
to Kant (1977), artistic genius is a talent that produces original creations surpassing
nature through its expressive potential, creating, expressing, communicating, and
contemplating beauty (Flores, 2001).
However, the strange, the monstrous, the obscene, or “immoral” has always had
a marginal place in art, being the works with these characteristics repudiated by
academic or religious institutions, although widespread and in many cases claimed
in later times. From Antiquity to the Middle Ages, ugliness is related to a lack of
harmony that breaks the rules of proportion on which beauty is based (Rosenkranz,
1853). However, it is admitted that, despite the existence of beings and things con-
sidered ugly, art can represent them beautifully, and the beauty of this imitation
makes the ugly acceptable (Aristotle, fourth century B.C.; Eco, 2007). However, to
what extent does a representation of the ugly and monstrous make it somehow more
attractive? While beauty does not produce a shock or wonder in the preconceived
aesthetic pattern in the viewer, the ugly is configured as an original and shocking
experience, which can result in extreme sensitivity and intensity in the receiver of
an artistic work (Muñoz, 2017).
From ancient texts of the first centuries of the Christian Era, representations are
known where monstrous men and animals appear, which are then reproduced in
medieval encyclopedias (Bovey, 2002), giving rise to the fascination for the super-
natural and an unknown world ruled by unique and monstrous figures: “in the great
symphonic concert of cosmic harmony, the monsters themselves constitute, even if
only by contrast (…) to the beauty of the whole” (Eco, 2015). In this way, monsters
become increasingly present in literature and painting, from Dantesque descriptions
of hell to the aberrant and fascinating paintings of Bosch (Fig. 8.3a–d). In the pas-
sage to the Modern Age, the monster lost its symbolic charge. It is only considered
a mere “natural curiosity” to be studied in its anatomy more scientifically with a
naturalistic interest.
Artistic movements are extraordinary examples of the dynamism between rules
and exceptions, at the level of individual artists as exceptional geniuses admired or
wholly rejected, or of movements and conceptions of the “ugly” and “beautiful”
that were totally disruptive for their time, “revolutionary” artistic proposals or broke
with the prevailing pattern or rule at a particular historical moment. During the
8.4 R&E Search on Subjective/Controversial Topics 515

a b

c d

Fig. 8.3 Examples of illustrations of monstrosities. (a) Giovanni da Modena, The Inferno, 1410,
Basilica di San Petronio, Bologna, Italy. (b) Coppo di Malcovaldo, Inferno-part. Giudizio
Universale, c. (1260–70), mosaico. Firenze, Battistero, Italy. (c) Limbourg Brothers, Hell from the
Tres Riches Heures du Duc de Berry, (1411–1416), Musée Condé, Chantilly, France. (d) Anonimo,
Christus in de Limbus, (1575), Indianapolis Museum of Art, USA

Renaissance, artists such as Michelangelo, Raphael, and Leonardo da Vinci were

inspired by classical Roman and Greek art, taking as rules balance, naturalism, per-
spective, symmetry, and “perfect” proportions (Summers, 1990). Humanist portraits
with proportioned and anatomically correct sculptures and harmonious and sym-
metrical architecture are clear examples of the spirit of the Renaissance. The strange
for this time became the rule during the Baroque, where vivid, extravagant colors
prevailed. It became necessary to represent reality crudely, with distortion of forms
with violent and contrasting effects, a certain tendency to imbalance and exaggera-
tion, abandoning the corresponding “perfect” representations of the previous period.
For example, Caravaggio illustrated the supernatural with a very human appear-
ance, bringing man closer to the mystery of the transcendent through vulgarity and
ugliness. However, this transition would be reversed with the appearance of
Classicism during the Modern Age. Aesthetic and philosophical patterns of Classical
Antiquity would re-emerge, such as the “aurea mediocritas,” a Latin term that
alludes to the desire to reach a middle ground between extremes. This state is far
from excess through the just measure of opposites (concordia oppositorum): the
516 8 Beyond Biology

virtue is in the middle ground (Aristotle, fourth century B.C.). Classicism assumes
the ideals of romanticism and humanism, aspiring to achieve absolute perfection
through art. Nicolas Poussin, a great exponent of this movement, would say that
Baroque painters such as Caravaggio, who departed from these rules, had come to
destroy painting, qualifying them as “painters of ugliness.”
An iconic example of painters rejected and considered rare in their time can be
seen in the well-known “hall of the rejected” (Salon des Refusés) in 1863 in Paris.
This collective show brought together great painters such as Manet, McNeill
Whistler, Courbet, and Cézanne. They had been rejected from the Paris Salon exhi-
bition of the Académie des Beaux-Arts (the most important annual artistic event or
biennial in the world at the time) (Bozal, 1996; Hauptman, 1985). This fact coin-
cides with the birth of Impressionism in painting as a disruptive artistic expression
initiating the path toward avant-garde movements. Many of these artists broke aca-
demic rules by painting outdoors instead of indoors in their studios. The Salon of
the Rejected was gaining popularity in subsequent years. Those artists first margin-
alized and exceptional from a negative assessment gave way to what would become
the rule or norm in the later artistic period.
However, suppose we are discussing disruptive artistic movements. In that case,
we cannot fail to mention Surrealism, where the extraordinary, fantastic, and strange
were common currency in the leitmotiv of both pictorial and literary works (Nadeau,
1965). Surrealists often challenge perceptions and reality in their works of art. The
limits of beauty were expanded; the spectrum of combinations grew, provoking a
true creative explosion (Bigsby, 1972). In many cases, the images of pictorial space
are represented with unnatural and disproportionate shapes and sizes, with what
could be considered “technical errors,” but to create empty and suggestive spaces for
the observers to give definitive meaning to the representations. One of the precur-
sors of Surrealism, Giorgio de Chirico proclaimed: “To become immortal, a work of
art must escape all human limits: logic and common sense will only interfere (…)”.
Later, artistic movements and artists would aim to intentionally provoke rejec-
tion or strangeness, presenting unique and provocative proposals that would stand
out in some way or impose debates on the public (Gomes, 2021; Jennstål & Öberg,
2019) (Fig. 8.4a–f). “La Fontaine” (literally a signed urinal) by Marcel Duchamp
inaugurated the postmodern era, and when presented at the Society of Independent
Artists in 1917, it was not considered a work of art and was rejected (Tomkins,
1977). Although initially a joke by Duchamp to mock the artistic circle of the time
and the prevailing notion of art, this work imposed a new style known as “ready-­
made” and was voted the most influential work of art of the twentieth century
(Turner prize, Gordon’s, 2004). Duchamp’s only laws were those of exception,
those that break and question the norms, and he was the pioneer of conceptual art
(Paz, 1990). Something similar happened with Andy Warhol’s “Campbell’s Soup
Cans” (1962), a pop art icon. When it was exhibited, it caused outrage, and the
excessive questioning and criticism distinguished Warhol from other emerging pop
artists (Schroeder, 1997). Warhol’s reputation grew to become the most renowned
and quoted American pop artist (Galenson, 2021). More recently, something similar
happened with Maurizio Cattelan’s “Comedian” (2019), a banana stuck to the wall
8.4 R&E Search on Subjective/Controversial Topics 517

a b c

d e

Fig. 8.4 Exceptional artistic manifestations that received the rejection of the public or the
Academy. (a) Michelangelo Merisi da Caravaggio, Sacrifice of Isaac, 1595, Uffizi Firenze, Italy.
(b) Edouard Manet, Luncheon on the Grass (1863), Musée d’Orsay. (c) Jackson Pollock, Blue
Poles, (Number 11), 1952, National Gallery of Australia. (d) Cham, Caricature on Impressionism,
on the occasion of their first exhibit, (1874), Bibliothèque nationale de France, Paris. (e) Marcel
Duchamp, The Fountain, (1917), Original missing. (f) Tracey Emin, My Bed, 1998, Saatchi
Gallery (g) Maurizio Cattelan, Comedian (2019), Private collection, presented for the first time in
Miami Art Basel (2019), USA

with packing tape (Bryzgel, 2019) (Figure 8.4g) or “America” (2016), a fully func-
tional golden toilet (Bown, 2019). These works hide a powerful critical component
on an economic and political level but are still questioned as true “works of art”
(Celik, 2021).
This same phenomenon can be transferred to other artistic disciplines, such as
architecture and poetry, where disruptive artists have been rejected for their excep-
tional creations over time. The Eiffel Tower (1889) was considered “useless and mon-
strous” and was even ordered to be demolished, although it finally survived and today
is considered the most emblematic symbol of Paris. In poetry, the French “damned
poets” stand out (such as Corbière, Rimbaud, and Verlaine) who were talented but
misunderstood by their contemporaries, who rejected the established artistic and
social norms, developing a free and provocative art (Verlaine, 1884). This literary
style gave rise to “malditism” for those poets who transgressed the established norms,
and this nickname would end up being applied to many writers (Del Moral, 1985).
The rare or exceptional will always be judged subjectively in art. Therefore, the dyna-
mism between rules and exceptions transcends disciplines and temporality.
518 8 Beyond Biology

8.4.1.2 Music

Another aspect undoubtedly linked to art and culture is music, which has also
changed over time. Although musical notes are invariable, what has been created
and modified are musical styles. In this sense, musicology studies the phenomena
related to music, its theoretical bases, its notational systems, its history, and its
relationship with societies. It has been responsible for analyzing the musical struc-
tures consolidated throughout history (Franco, 2019; Palisca & Grout, 1996;
Reich, 2002). The history of music refers to the study of manuscripts, iconogra-
phies, the relationship between music and society, and the different musical genres
over time. For example, from the history of European classical music to rock
music, different musical styles have had their “glory” period, and their great per-
formers are considered by many true idols who left their mark on the world history
of music over time.
In early times, the different musical forms were linked to the sacred use of these.
However, they then gave way to secular music, i.e., music that is not linked to any
practice of religious origin but to different cultures and traditions with their own
rules in musical composition (Franco, 2019). Great composers such as Brahms,
Wagner, Verdi, Debussy, Rachmaninoff, and Stravinsky, among many others, were
misunderstood in some of their masterpieces for being original and “exceptional”
(Slonimsky, 1965).
Music was significantly affected at the end of the nineteenth century by the
industrial revolution, which allowed new and significant advances in various aspects
of society. For example, the mechanics of instruments mainly provide new musical
resources, giving greater creative flexibility to the compositions in their melodies
(Franco, 2019). The transformation of music from technological innovation is unde-
niable. We can consider the sophisticated “tuning” of certain instruments that
require a specific sound.

8.4.1.3 Literature

On the other hand, we can speak of the literacy process that has been gaining an
essential space within societies and where in recent decades, more attention has
been given to it (Tapia, 1994). The social phenomenon of literacy was an exclusive
skill taught only to specific people or groups. For example, in ancient times, scribes
and royal advisors, and people belonging to high society, only to the noblest fami-
lies of the place, where literate people were responsible for teaching their children
(Tapia, 1994). Even exclusive to sons, female daughters were only instructed in
Christian morals and housework and only had access to literacy if they joined the
cloistered nuns’ convents. It was not until the middle of the seventeenth century that
the literacy phenomenon became more massive with the implementation of schools.
This strategy sought, among other things, to ensure that the children of the poorest
families were not left without assigned responsibilities so that they could acquire
education and professional training (Tapia, 1994).
8.4 R&E Search on Subjective/Controversial Topics 519

Let us consider another point closely linked to literacy: access to books. Access
to books was also for a tiny part of society. It was not as common to have a library
at home as it is today, not only because of the cost of books but also because they
were not printed on a massive scale. With the passing of time, having a “library” in
every house went from being an exception to a rule. It was not strange then that
there was a minor or extensive library in every house, which also reflects the increas-
ingly preponderant role that education had. Physical libraries, then, went from being
an exception to a rule, and with the advance of technology, they went from a rule to
an exception again. Currently, how common is it to have libraries similar at home to
those of our parents or grandparents? Most likely exceptional, as with internet
access, for example, our library is already “virtual.” The form of the library has
changed from physical to virtual, but the “size” or the number of books or writings
we have access to is undoubtedly much more significant.

8.4.1.4 Calligraphy

Another subject to which we can refer, associated with culture, to see how some
patterns became exceptions with time, at least in their use, is calligraphy. According
to a classic definition, calligraphy is “the art of writing with beautiful, artistic and
well-formed handwriting according to different styles.” In this sense, the morphol-
ogy of the written letter was mainly associated with aesthetic aspects, legibility, and
economy of the substrate. Essentially, where handwriting was most used was in
religious and mercantile activities, leaving the orthographic and grammatical
aspects of writing in the background (Bello, 2016). Although in many cultures,
there has been a development of writing, and in its absence, one of its visual forms,
calligraphy, the importance attributed to it has depended on the historical and cul-
tural contexts (Gálvez Pizarro, 2004).
Calligraphy can be classified, for example, in the Latin writing system in
Carolingian, Gothic, Chancellery, English commercial, foundational, and others.
All of them are governed by different and demanding formal and aesthetic rules
(Gálvez Pizarro, 2004). However, handwriting and calligraphy are being replaced
due to technological advances and may be lost over time. Think, for example, of
Johannes Gutenberg’s creation of the printing press in the mid-fifteenth century,
which significantly reduced handwriting for copying books, with movable type
gaining ground. The printing press provided the technical conditions to ensure
equality in the reproduction of copies, which was impossible with the manual writ-
ing of texts (Bello, 2016).
On the other hand, the forms of writing were simplified. As a result, the teaching
of writing in schools was limited to letters with more cursive features, such as the
Spanish Bastarda, similar to those used today (Bello, 2016). The innovations
brought about by the development of typewriters first and computers years later
further reduced the use of calligraphy. Word processing programs speed up, facili-
tate writing, and make the correction process much more manageable. In addition,
when printing, the text will appear “clean” without amendments, as in handwritten
520 8 Beyond Biology

or typewritten texts (Ferreiro, 2006). In addition, the use of personal computers and
the Internet has produced changes in the way young people write, mainly when used
in chats, e-mails, and cell phones, for example, so that changes in the forms of writ-
ing are associated with changes in social practices (Ferreiro, 2006).
Although formal calligraphy has largely lost its original function as a daily nota-
tion tool, it has been maintained over time in search of other types of utilities more
linked to artistic expressions, with the design of advertising, logos, and labels,
among others. At the beginning of the twentieth century, modern calligraphy resur-
faced, where letters may or may not be legible (Claude et al., 1996; Mediavilla,
2005). In fact, the artistic movement called “calligraffiti” merges calligraphy with
graffiti, amalgamating the traditional with the modern.

8.4.2 Sports

Within sports activities, we also find examples of rule changes. As previously men-
tioned, sports-related activities have become increasingly important in people’s
daily lives. Many people spend many hours playing sports, assigning them positive
characteristics in terms of health and as a social, educational, moral, and cultural
factor (Garoz Puerta, 2005). In addition to the vital role in economic activities
already at the level of professional sports, sports such as Football, American
Football, Baseball, and Basketball, for example, move large amounts of money
worldwide (Triviño, 2011). An important role that sports has also had and still has is
at the sociopolitical level. A clear example is the place taken by the practice of rugby
in the unification between black and white people in South Africa (Triviño, 2011).
With sufficient evidence, sport contributes positively to the development of our lives.
Numerous sports originated in ritual, medieval, and popular games that changed
toward a sporting environment in the nineteenth century with the creation of com-
petitive sports (Garoz Puerta, 2005; Triviño, 2011). In this sense, part of the sports
study has focused on the different rules, their functions, and how they have evolved
through history (Garoz Puerta, 2005; Triviño, 2011). If we refer to particular sports,
we can say that in all of them, there are rules and that the rules serve to regulate the
competition by granting equal opportunities to all competitors and sometimes bring
safety to competitors, as in the evolution of F1 cars. Within the rules, we can dif-
ferentiate between rules that refer to equipment, players, substitutes, coaches, and
judges. Timing rules, rules that determine infractions, penalties and points, or goals,
and rules of conduct in general of the participants (Arias et al., 2011; Garoz Puerta,
2005; Sánchez, 1987; Triviño, 2011).
Knowing and following the rules is fundamental in the development of the game.
Therefore, if the aim is the modification of the conditions of the game, it is necessary
to modify its rules. We should always keep the basic rules to not significantly alter
the sport’s spirit in question and maintain interest in the original game. It is crucial
to analyze the impact that these modifications in its rules have before its definitive
implementation (Arias et al., 2011; Nevill et al., 2008). In addition, many sports have
8.4 R&E Search on Subjective/Controversial Topics 521

modifications and adaptations in their rules when, for example, they are played by
children or by people with disabilities, such as sports adapted for people in wheel-
chairs or blind people, where the rules are not the same, but the sport is the same.
Changes in the regulations of different sports are also influenced by changes in
lifestyles. In this sense, they are added to sociocultural evolution (Garoz Puerta,
2005). Let us also think about sports video games that, with technological advances,
are becoming increasingly frequent, not only those played by children or in an ama-
teur way but also large competitions worldwide (e-sports). Here, the rules can be
considered limitations on the actions of the players, whether the players can be
injured or not, or the scenarios available for the game to take place, rules that do not
exist in the “real” game (del Castillo, 2012; Gee, 2004; Juul, 2005; Prensky, 2002).
We can then understand sports rules as changing and influenced, for example, by
sociocultural evolution and by the evolution that technological advances bring with
them (Garoz Puerta, 2005).

8.4.3 Religions and Beliefs

In religion, the concept of rules, principles, norms, and above all, the idea of
“dogma” emerges strongly. According to the Dictionary of the RAE (Real Academia
Española, 2022), dogmas are concepts taken as absolute truth that cannot be
doubted. It is an undeniable principle. Religious dogmas are beliefs that define a
religion, differentiate it from other religions, and are considered truths associated
with people’s faith. In the Catholic Church, dogmas are understood as absolute
truths taught to the faithful. They are categorized into divine dogmas taught by
Jesus, apostolic dogmas taught by the Apostles, and ecclesiastical dogmas taught by
Popes. The Catholic Church takes dogmas as absolute truths, and if any doubt
arises, they reaffirm it with another dogma. For example, Christianity takes as
dogma Jesus Christ as the son of God. However, when doubt or inconsistency arose
in this dogma, they created another article of faith to reaffirm it. In Judaism, Saadia
Gaon was the one who systematized the dogmas of religion, the belief in one God,
and Israel as the guide of the world. In addition, practices such as the use of the
Talit, a fringed cloak worn by the faithful, and Tefillin, small leather boxes placed
on the head, are common among the faithful. Islam establishes for its faithful that
“There is no God, but Allah and Mohammed is his prophet.” Islam preaches that
God is merciful and all-powerful and has guided his faithful through his prophets.
Its dogmas are embodied in the Quran, which is the textual word of God (Goldman,
1995; Watt, 2003), and it is religion that has seen the most significant increase in the
number of followers in recent times.
Although religious dogmas have remained almost unchanged over time, we can
say that the practice in many religions has changed. For example, in the Catholic
Church, the mass was said in Latin, backward to the people, and facing God at the
main altar. This practice ended with the Second Vatican Council between 1962 and
1965, with a mass celebrated in vulgar language. Pope John XXIII said… “I want
522 8 Beyond Biology

to open the windows of the church so that we can see outside and the faithful can see
inside,” which initially generated a rejection by other members of the Church who
insisted on the conservation of Latin as the universal language of religion (Díaz
Patri, 1994). This is a clear example of change from rule to exception in the
Christian church.
On the other hand, common practices years ago among the faithful are now
almost a rarity, such as attending Church on Sundays, which the whole family did
as a ritual. It is increasingly common to hear from the mouths of the faithful, “I
believe in God, but not in the Church”; in this sense, numerous corruptions linked to
the Church have undoubtedly caused many of the faithful to move away from it. In
addition, in recent years, the question has also arisen: are religions necessary for the
development of a society? This question was not even asked before (Giner, 1993).
In the past, a world without religion was not imaginable.
Currently, many of these concepts have changed. In fact, in today’s societies, the
institutional and political order can be maintained without the need for religion; for
example, secular state countries do not take any religion as a state religion (Giner,
1993). The truth is that religions have lost their essential place in societies, occupied
in the preindustrial world. The secular process, the passage from a religious to a
civil sphere, of modern society led one to think that religion’s days were numbered.
Clearly, this was not the case, but it has confronted religions with significant crises
and created new religious movements (Velasco, 2006).

8.5 Key Concepts and Ideas in this Chapter

• We reviewed rules and exceptions in other branches of science related to biology

and other sciences and disciplines less related to biology.
• Advances in knowledge and technology associated with medicine lead to changes
in its rules over time. Exceptions that are now more common include diseases
such as autism, medical conditions, and biomedical tools such as vaccines, gene
therapy, and precision medicine. There have been changes in the concepts and
approaches in medicine for obesity, smoking, and parenthood.
• Although less likely to occur, exceptions are also observed in the “hard sciences,”
such as physics, chemistry, and geology. Transitions in rules and exceptions also
occur in social sciences, such as changes in conceptions about native and family
cultures as simple examples.
• Artistic movements are also clear examples of the dynamism between rules and
exceptions both at the level of individual artists and subjective conceptions of
“ugly” and “beautiful” or worthy of being called art. We review artistic proposals
that break with the current pattern or rule in certain historical moments. Changes
in rules and exceptions in music, literacy, calligraphy, sports, and religion are
linked to sociocultural evolution and technological advances.
• Everyday activities such as sports and religion may also show a clear dynamic
between Rule and Exceptions that boost its evolution.
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Chapter 9
Overview and Final Prospects

Contents
9.1 Perspectives on Potential Applications 532
9.2 On a more Theoretically Scientific Level 533
9.2.1 Strengthening Publications on Rarities 533
9.2.2 Appreciating the Dynamism Between R and E 534
9.2.3 Avoiding Bias in Scientific Education 535
9.3 On a Human–Nature Relationship Level 536
9.3.1 The Vindication of Singularity and Otherness 536
9.3.2 Direct Applications of Exceptions and R<->E Dynamism 538
9.3.3 Modifications and Environmental Risks of R<->E Dynamism 540
9.3.4 Applications of R<->E Dynamism on a more Holistic Level 541
References 543

Abstract Finally, chapter 9 is intended to be a closing section of this book, sum-

marizing in some way what has been said in the previous chapters. In this sense, we
have discussed the dynamics between rules and exceptions, taking into account dif-
ferent factors involved in such dynamics. Some changes are generated by nature
itself, and others are promoted, directly or indirectly, by human action. In addition
to the dynamics of change produced by intellectual development, changes in domi-
nant scientific paradigms, discoveries, and technological advances. We show the
potential applications and benefits of considering rules and exceptions at two main
levels: first, from a theoretical-scientific level, more directed to the scientific com-
munity, where publications that highlight different types of rarities are valued and
the dynamism between rules and exceptions is appreciated; and second, from a level
related to improving man’s relationship with nature.

© Springer Nature Switzerland AG 2024 531

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0_9
532 9 Overview and Final Prospects

9.1 Perspectives on Potential Applications

We conclude this journey with a summary of what has been presented in the vari-
ous chapters of this book. Throughout these pages, we have reviewed the theoreti-
cal aspects specific to the life sciences, their knowledge and theories, their
extensions to the daily lives of people, and their connection to biology. When ana-
lyzing rules, patterns, norms, exceptions, oddities, and anomalies, our research not
only covers purely general or “basic” aspects but also extends to areas of signifi-
cant practical relevance. Many cases are directly or indirectly related to important
applied fields, such as agricultural engineering, biomedicine, and the environment.
For example, the impact of climate change on rule-exception dynamics, biodiver-
sity conservation, and the introduction of exotic species are clear examples of this
intersection.
When talking about “applications” in science, several visions emerge. For
example, these applications can be more direct within the framework of the spe-
cific discipline or more indirect, with important theoretical connotations. The most
direct application is the one that is mainly related to a benefit for man, such as
those oriented to technologies, agriculture, livestock, industrial or service produc-
tivity, among many others. On the other hand, more indirect applications (from an
anthropocentric perspective) come from work in the social, philosophical, and
epistemological sciences. In other words, the term “application” goes beyond a
narrow anthropocentric utilitarianism, with synonyms such as “employ, use, man-
age, utilize, allocate, exploit” that should be more flexible. Whatever the type of
application, it is possible that the concepts we have seen about the dynamics
between rules and exceptions underlie and are important in these different scien-
tific aspects.
Throughout this book, we have explored and described the rule-to-exception and
exception-to-rule dynamics. In doing so, we have considered various influencing
variables that shape these dynamics. Some cases illustrate entirely natural changes,
while others reveal the active role of humans, directly or indirectly, in driving these
shifts throughout history. In addition, we have emphasized the role of intellectual
development in generating shifts between rules and exceptions that can result from
shifts in scientific paradigms, new discoveries, technological advances, and new
ideas. A key message of this book is that current situations may change in the future:
the static succumbs to change. To illustrate the potential applications and benefits of
rules and exceptions, we will organize this summary into two main levels. It is
important to note that these levels are not mutually exclusive and may not always
have clear boundaries. First, we will address a theoretical perspective aimed at sci-
entists and the scientific community itself. Second, we will explore a more practical
aspect, focusing on improving the connection between humanity and nature in vari-
ous domains.
9.2 On a more Theoretically Scientific Level 533

9.2 On a more Theoretically Scientific Level

9.2.1 Strengthening Publications on Rarities

We have emphasized the importance of exceptions, aberrations, teratologies, and

abnormalities in biology and other disciplines. These phenomena are of great
importance in studying ecological and evolutionary implications from various per-
spectives. Often, aberrant events have been overlooked in scientific reporting, but
they have proved to be valuable contributions to certain fields, such as plant physiol-
ogy, as exemplified by the study of homeotic genes and the ABC model. In addition,
exceptional cases, such as cephalopods, offer excellent potential for understanding
the evolution of intelligence in different animal groups. Taxonomic curiosities, such
as carnivorous sponges or carnivorous plants, are particularly valuable from a com-
parative standpoint, as they provide essential information for exploring potential
phylogenetic hypotheses.
However, evaluating, understanding, and comparing these examples is often
challenging, mainly due to the lack of publications or in-depth studies of these rare
phenomena. The discussion of aspects of rules and exceptions in many groups
requires more emphasis on the publication of rare cases. Without adequate represen-
tation of these rare cases or events in the literature, it becomes more difficult and
limited to share data, opinions, or engage in discussions at any level. Several factors
contribute to these omissions, including confirmation bias, underfunding of research
on rare phenomena (e.g., rare diseases), difficulties in publishing results from non-
model species, and reluctance to publish papers with rejected hypotheses. These
multifactorial reasons underscore the need for a concerted effort to promote and
include information about these rare cases or events in the scientific literature.
For example, in animal behavior studies, it is common to observe some individu-
als exhibiting behaviors that deviate from the general pattern observed in other indi-
viduals. Unfortunately, researchers often ignore these outliers when analyzing the
data, with no apparent justification. It would be interesting, however, if these data,
even if not included in the formal analyses, were presented in the study. This would
illustrate the natural variability within the population and potentially serve as a basis
for exploring new questions in the future. In morphological studies, as mentioned
earlier, teratologies or aberrations can be incredibly valuable from a comparative
standpoint, providing essential insight into potential phylogenetic and evolutionary
hypotheses. In addition, the study of endemic or locally rare organisms, especially
in underrepresented regions such as the Neotropics, can provide critical information
to address important questions. Such research can also help confirm or refute para-
digms extrapolated from primary research sites, such as the Nearctic region.
In this context, fostering a constructive habit to strengthen the dynamic relation-
ship between rules and exceptions involves incorporating more data on rare cases in
our publications. One effective approach could be to include supplementary material
annexes containing information on these cases. While these data might not be
directly relevant to the specific study, they can be immensely valuable for other
534 9 Overview and Final Prospects

researchers. Presently, there is a growing emphasis on uploading supplementary data

or original spreadsheets from publications on the web (Whitlock, 2011). With the
digital and online publishing tools available today, it becomes feasible to share and
access this type of information in a manner similar to image databases in taxonomic
collections or morphological studies across various groups. Researchers could easily
compare “rare” data with other similar information found in these appendices.
By collecting and openly sharing rare data, authors can potentially shed light on
connections between ideas, casual observations, potentially innovative strategies, or
variations in adaptive and evo-devo contexts. As responsible authors, we should
commit to providing this information, and journals should actively include such
data in the open-access databases linked to publications. This practice can be applied
to experimental, descriptive, and comparative studies and will benefit the scientific
community as a whole.

9.2.2 Appreciating the Dynamism Between R and E

This perspective is of utmost importance as it enriches us as students of life, enabling

us to advance more rapidly in scientific knowledge while avoiding dogmas, even
smaller ones. Embracing this approach entails developing a heightened critical
capacity to question concepts based on nonstatic paradigms, not only from an epis-
temological standpoint but also at a strictly biological level, encompassing evolu-
tion, ontogeny, and generational aspects.
The cultivation of critical thinking starts early, beginning in the family and ele-
mentary school, where we encourage the development of reasoning skills and
objectivity, along with a healthy dose of skepticism toward unsupported claims.
This mode of thinking involves asking questions, formulating hypotheses, consider-
ing alternative explanations, and assessing the credibility of information sources
(Halpern, 1998; Solbes-Matarredona, 2013; Vieira et al., 2010).
Indeed, there exists a close link between scientific thinking and critical thinking.
Given the ongoing social and cultural changes, it is imperative to nurture citizens
with a critical and flexible mentality capable of questioning accepted norms if they
lack sufficient evidence. Importantly, this does not imply blindly doubting or criti-
cizing established knowledge without grounds; rather, it emphasizes the importance
of not accepting something as “true” if the supporting evidence is lacking or if there
is evidence to disprove it. A well-informed, evidence-based approach is what we
strive to cultivate.
In this sense, science education extends far beyond teaching theories and laws or
conducting experiments to test hypotheses. It requires building a society that recog-
nizes and embraces the dynamic nature of scientific activity. Such a society should
be capable of evaluating, with reason and argumentation, what is currently consid-
ered true or a standard practice (Eslava, 2014). Science is not static and timeless;
rather, it is an ongoing process of knowledge construction that heavily relies on the
context in which it operates.
9.2 On a more Theoretically Scientific Level 535

As we previously mentioned, scientific knowledge evolves and undergoes grad-

ual changes based on evidence and discussions. As scientists, we should not become
disappointed or frustrated when exceptions challenge established rules. Instead, we
must take on the challenge of refining or reformulating those rules and continually
striving for improvement. It is essential to remember that scientific growth and
development often arise from breaking down dogmas that were once thought insur-
mountable. Aspiring to challenge scientific laws in a constructive manner with
responsibility and professionalism is vital for the advancement of science.

9.2.3 Avoiding Bias in Scientific Education

Indeed, a crucial aspect of science education is to adopt a more open and less dog-
matic approach. Encouraging openness and creativity in teachers can lead to the
development of critical thinking in students. This perspective should extend beyond
undergraduate education to graduate education, including Ph.D. students and
researchers in their daily scientific work. This new vision should also influence the
content of textbooks, with an emphasis on the presentation and appreciation of
exceptional cases. As we have emphasized, the study of these exceptional cases is
essential to capture the full complexity of biological systems. Consider, for exam-
ple, the negative impact of a dogmatic professor on a group of students. If a profes-
sor rigidly adheres to a single perspective that he takes to be the absolute truth and
fails to present alternative viewpoints or variants, he hinders the students’ ability to
construct knowledge independently. It also limits their ability to develop critical
thinking skills and to evaluate and choose among different explanations or
hypotheses.
To promote a more effective and enriching learning experience, we should
encourage teachers to adopt a more inclusive and open-minded approach to teach-
ing. By fostering an environment that allows for exploration, questioning, and con-
sideration of diverse viewpoints, we can empower students to develop their critical
thinking skills, enhance their ability to think independently, and prepare them to
become versatile researchers in the scientific community. In science, bias refers to
the difference between what we think we value and what we actually value (Cuéllar
Rodríguez, 2019; Rodríguez, 2020). Bias is prevalent in all areas of scientific
research. At each stage of the scientific process, from setting objectives to selecting
methodologies, study variables, and statistical analyses, researchers may introduce
bias. To ensure the integrity of research findings, it is essential to recognize and
identify these biases to minimize and correct their effects (Manterola & Otzen,
2015; Rodríguez, 2020).
While objectivity is the ideal state in science, where personal goals and motiva-
tions should not influence research activities, it is difficult to completely avoid epis-
temic biases (Biddle & Kukla, 2017; Cippitani et al., 2021; Fraedrich, 2001; Reiss
& Sprenger, 2014). The key is to acknowledge the existence of biases and work to
minimize them. One effective way to address bias is to discuss it with other
536 9 Overview and Final Prospects

researchers and subject the work to peer review (Cippitani et al., 2021). Another
type of bias in science relates to the publication of the scientific results obtained by
researchers. Here, we can distinguish two important biases.
The first bias, publication bias, refers to the selective publication of research
results, where studies with positive and statistically significant results are more
likely to be published, while nonsignificant or negative results may be overlooked.
This can result in an incomplete and biased representation of the true evidence in a
given area of research. The root of this bias may lie in editorial decisions or societal
pressure to publish “exciting” results, leading to underreporting of less favorable
findings (Rodríguez, 2020). The second bias relates to scientists’ adherence to
established explanations or data from studies in model organisms. This tendency
can inhibit the development of novel ideas or discoveries that challenge current rules
or paradigms. According to this idea, many studies do not come to light because “it
did not work the way it was supposed to.” Being more critical and constantly chal-
lenging the norms is essential for scientific progress and growth. It encourages
researchers to explore alternative hypotheses and innovative approaches, potentially
leading to breakthroughs and a deeper understanding of biological systems.
As scientists, it is crucial to recognize and actively address these biases. By pro-
moting transparency, open-mindedness, and rigorous evaluation of all research
results, we can improve the reliability and validity of scientific findings. Fostering a
culture that embraces diverse perspectives and welcomes constructive criticism is
fundamental to advancing science and achieving its ultimate goal of expanding
knowledge and improving our understanding of the world.

9.3 On a Human–Nature Relationship Level

9.3.1 The Vindication of Singularity and Otherness

As we have seen, in systems theory and holism, there is a singularity where small
changes can have significant effects due to the interconnectedness within the inte-
grated “whole.” Furthermore, exceptional cases can be linked to the concept of
uniqueness, which refers to the intrinsic value of each living being and is closely
related to the idea of “identity.” At the social level, the notion of individuality plays
a crucial role in shaping intra and interspecific relationships, social codification,
belonging, and the hierarchization of human groups. Rose (2001) underscores the
value of individuality by emphasizing that each person has his or her own life
story. In addition, identifying someone as “other” (not belonging to our group) has
significant implications for understanding social identity. The concept of “other-
ness” emerges from a philosophical, psychological, cognitive, and social process
through which a group defines and distinguishes itself from other groups
(Türkkan, 2010).
Gradually, concepts have emerged that emphasize the value of diversity and oth-
erness by recognizing and embracing differences and ensuring their equitable
9.3 On a Human–Nature Relationship Level 537

representation in political and social agendas. It is crucial to emphasize that the

emphasis on what makes individuals different and exceptional should never lead to
discriminatory practices or associate negative connotations with those who are dif-
ferent (whether those differences are real or perceived). Such negative associations
can potentially stigmatize members of other groups.
This emphasis is particularly important at a time when issues such as racial, reli-
gious, and gender discrimination, the marginalization of minorities and school bul-
lying are among the most critical social problems in the world. Not only are they
detrimental to society, but they also contribute significantly to mental health prob-
lems and suicidal behavior (Ahuja et al., 2015; Larraín, 2019). As a society, it is
crucial to increase social awareness of the uniqueness of each individual to tackle
discrimination. Achieving this goal can be challenging, especially in organizations
where negative biases are deeply ingrained from an early age. An effective approach
involves collaboration between interdisciplinary groups of scientists and educators
to ensure that topics or examples with negative societal connotations are presented
without bias from the beginning of education.
For instance, when teaching children about organisms often labeled “bad” in
biology, it is essential to provide a comprehensive understanding of their biology,
the precautions necessary when dealing with them, the benefits they offer, and how
to care for them. By doing so, people would be less likely to develop fear and aver-
sion toward creatures such as cockroaches, arachnids, snakes, or bats (among oth-
ers) if they are introduced to their value and how to coexist with them from an
early age.
To reach a wider audience and influence family perspectives, additional resources
such as television, the Internet, and social networks can be used. These platforms
can help dispel misconceptions and fears about various topics. In addition, address-
ing not only biological but also social and cultural issues in a professional manner
can foster constructive discussions. However, we must remain vigilant about the
biases mentioned in the previous section to ensure that the information presented is
objective, accurate, and unbiased. This perspective, similar to the consideration of
humans, is prominent in certain areas of research within animal behavior and biodi-
versity conservation practices. One such area of focus in animal behavior research
is the study of animal personality and the incorporation of individuality into
decision-­making rules. This highlights the importance of recognizing the unique-
ness of each organism as a critical variable (Carter et al., 2013; Schuett et al., 2010;
Stamps & Groothuis, 2010a, 2010b).
Science can benefit from exploring what rare and exceptional species can offer
to address current challenges. A notable example is the discovery of rare or relict
species that can provide valuable benefits. Historically, such species have been
instrumental in the development of biomedical compounds to combat diseases,
including cancer. However, the focus should not be solely on finding species that
offer cures for specific diseases. As we have seen, these new species have also
shown promise in addressing environmental issues, such as the treatment of waste-
water and pollutants. It is equally important to recognize and value the importance
of common species that often go unnoticed because of their familiarity while
538 9 Overview and Final Prospects

providing critical ecosystem services. A pressing concern in this regard is the pol-
linator crisis, particularly the alarming decline in bee populations. Tackling this
crisis and protecting pollinators are essential steps in preventing potential large-
scale extinctions.
In contrast, related to uniqueness but extending to other organisms, we encounter
the concept of “value” of animal and plant species that goes beyond purely eco-
nomic considerations. It is crucial to recognize and appreciate the values inherent in
species, which extend to various aspects, such as aesthetics, culture, social signifi-
cance, recreation, and beliefs (Chan et al., 2012; Díaz et al., 2018). Species have
intrinsic or inherent value independent of their usefulness to humans, often referred
to as “existence value” (Vucetich et al., 2015). In addition, species may possess
“nonuse value” simply because they contribute to the continuity of nature, allowing
future generations to benefit from them (Pearson, 2016). In essence, species often
have an intangible value that may or may not be linked to their utilitarian benefits.
Acknowledging and appreciating these diverse values can lead to more comprehen-
sive and inclusive conservation practices (Pearson, 2016).
Such practices recognize the complex relationships between humans and biodi-
versity and embrace different perspectives on valuing nature. In conclusion, each
species is a unique product of thousands or millions of years of evolution, and each
plays an important role in enabling ecosystems to function properly (Costanza et al.,
1997; Kenter et al., 2015). In this way, we also become more aware of the value of
each species, even rare ones, in ecosystems and native communities. Their disap-
pearance will have serious short- or long-term consequences in the imbalance of
biological and, ultimately, ecological interactions. We must make responsible and
strategic use of umbrella species to design conservation strategies that benefit many
groups (Roberge & Angelstam, 2004). On the other hand, in recent decades, there
has been a greater social awareness, beyond solid environmental groups, fighting
against the unscrupulous actions of humans that are detrimental to the environment,
with consequences that ultimately lead to a decrease in biodiversity.

9.3.2 Direct Applications of Exceptions and R<->E Dynamism

In addition to their contributions to theoretical, phylogenetic, and evolutionary

knowledge in biology, exceptions in nature can be of immense benefit to humans at
various levels. Specific teratologies (abnormalities) observed in fungi, pollen, or
embryos of different species and exceptional phenomena such as bioluminescence
in fungi can be valuable bioindicators of environmental pollution. Moreover, the
exceptional characteristics of certain organisms can inspire new industrial applica-
tions. For example, the remarkable abilities of tardigrades, such as anhydrobiosis
(the ability to survive extreme desiccation) and radiotolerance, hold promise for
advances in radiation protection, cryopreservation of biological material, and other
industrial applications. Furthermore, some extraordinary organisms have the poten-
tial to make significant contributions to medicine and biomedicine. For example,
9.3 On a Human–Nature Relationship Level 539

amoeboid fungi have provided valuable insights into the study of human cancer and
other diseases, aiding in drug mode of action studies and toxicological assessments.
The “rare biosphere” of microbial communities can have a disproportionate impact
on ecosystem functions, including biogeochemical cycles. Certain microbes pos-
sess essential enzymes relevant to industrial processes, such as thermophilic cellu-
lases used in biofuel applications. Conversely, the removal of rare species from soil
ecosystems can lead to an increase in undesirable pathogenic species, underscoring
the critical role of rare species in biotechnological applications such as crop
protection.
In various contexts, humans have the ability to modify or manipulate other spe-
cies for various purposes, such as increasing productivity, disease resistance, docil-
ity, or purely aesthetic reasons. Today, even genetic engineering techniques are used
to create transgenic organisms. While artificial selection can have positive results in
terms of improving food productivity, there are instances where it leads to the cre-
ation of teratologies for human benefit.
From our perspective, what humans find beautiful can sometimes promote traits
that natural selection would otherwise have eliminated, such as those associated
with difficulties in feeding, locomotion, or reproduction. Artificial selection can
also result in reduced genetic diversity within modified species, making them more
susceptible to disease and morphological problems, leading to shorter life spans
compared to their wild ancestors. Therefore, human intervention in the creation of
genetically modified individuals should be undertaken with greater control and cau-
tion. While there are potential benefits to be gained, it is essential to minimize the
adverse effects on the species and organisms created. A balance must be struck
between achieving human goals and ensuring the long-term well-being of these
modified organisms.
The interplay between rules and exceptions can extend beyond the strictly bio-
logical realm and have significant applied importance in various fields. For exam-
ple, certain rare diseases often serve as gateways to understanding poorly understood
biological and physiological pathways, proving valuable for the study and preven-
tion of more common diseases. In addition, some medical phenomena previously
perceived as rare, such as autism, have gained prominence on research and funding
agendas due to increasing prevalence. Advances in technology and changes in
symptomatology or diagnostic perceptions have led to the abandonment of certain
concepts and practices in medicine. On the other hand, preventive medicine has
witnessed the development of numerous vaccines to eradicate diseases, from a rarity
a few decades ago to the norm today, with the vast majority of individuals receiving
vaccinations. It is now rare to find individuals who have never been vaccinated. Of
course, the acceptance of vaccines may vary depending on the sociocultural context.
An alarming concern, however, is the increasing resistance of bacteria to antibiotics.
The emergence of mutant pathogens can potentially cause some diseases that were
once exceptions, to become the rule, especially if care is not taken in the use of these
products.
The field of biotechnology is pushing the boundaries of what is possible in terms
of modifying DNA configurations and the embryology of hybrid organisms.
540 9 Overview and Final Prospects

Cross-­species treatments, including those aimed at curing diseases, creating organs,

and enhancing resistance, are becoming increasingly feasible. Evolutionary con-
cepts serve as the foundation for advances in synthetic biology, robotics, and bioen-
gineering. Synthetic biology continues to be the subject of intense global debate.
While it promises many benefits, such as the creation of artificial cells, molecular-
based tissue repair, cell reprogramming, and organ bioprinting to address organ
shortages, it also raises concerns about potential drawbacks and biases. Despite
these concerns, its application in medicine has the potential to yield significant posi-
tive outcomes. As technology advances, it is becoming increasingly rare to find
individuals who are completely “natural,” with no grafts, surgeries, prostheses, or
foreign bodies inside them. Technology is advancing rapidly, allowing for proce-
dures and manipulations that were unthinkable just a few years ago.

9.3.3 Modifications and Environmental Risks of R<->E

Dynamism

Indeed, as we have observed, rarities can have multiple impacts, both positive and
negative, on the environment and human activities. Some rare events may lead to
direct applications in industry or inspire new scientific breakthroughs, while others
may have adverse effects. One discussed example of a negative impact is the
“witches’ broom” case, which is causing significant economic damage to cocoa
crops in Brazil and other regions of Latin America. However, such damaging cases
also serve as catalysts for numerous research efforts aimed at mitigating their poten-
tial economic consequences.
On the other hand, rare species in specific ecosystems may be highly vulnerable
compared to more widespread or abundant species. Despite their rarity, they may
have significant value and play a critical role in providing various ecosystem ser-
vices. For example, certain soil microorganisms act as nitrogen fixers, rare species
stabilize food webs, keystone species maintain ecosystem structure, and predatory
species have a disproportionate influence on community structure. The reckless
exploitation of species through activities such as deforestation, hunting, fishing, and
the degradation of natural environments has resulted in the transformation of once
abundant species into exceptions, or worse, their complete disappearance from vari-
ous regions of the planet. The primary cause of this mismanagement of natural
resources and the transformation of species from common to exceptional is the lack
of effective management policies and the reliance on government officials who may
not be adequately qualified to make informed decisions in this regard.
Implementing appropriate measures to address these uses is critical to slowing
the disappearance of species already threatened with extinction and possibly recov-
ering some populations. While these measures may only be partially effective in the
face of irreversible extinction, they can help reverse the damage to species that have
experienced significant declines in abundance. As a result, these currently excep-
tional species may have a chance to avoid total extinction. With all that has been
9.3 On a Human–Nature Relationship Level 541

discussed about human activity on the dynamics of rule changes and exceptions, we
need to become more aware of the implications of human action in modifying spe-
cies through artificial selection and synthetic biology. Both to see its pros and cons
at the economic level and to reintroduce nearly or completely extinct species.
Similarly, we must take better care to control the introduction of exotic organ-
isms, whether for fishing, agriculture, forestry, poaching, or pleasure. Their impact
on native organisms is severe, with cascading effects that are rarely predictable.
Exotic organisms can cause the extinction or severe reduction in abundance of sev-
eral native plant and animal species, in addition to other effects such as hybridiza-
tion, parasitism, competition for resources, altered behavior, and reproduction.
These negative effects spread, changing the structure and functioning of the envi-
ronment and altering the population dynamics of certain regions. Thus, the intro-
duction of exotic species is one of the greatest threats to biodiversity in the world.
The destruction of forests and ecosystems also has cascading effects, often leading
to catastrophes that were once exceptional but are now the norm in many parts of the
world. Often, it is not measured, but the economic gain of any activity that favors
the destruction of ecosystems is less than the material and human loss of the catas-
trophes caused directly or indirectly.

9.3.4 Applications of R<->E Dynamism on a more

Holistic Level

Linked to the conceptual frameworks of holism and singularity, we have discussed

the Gaia hypothesis (Lovelock & Margulis, 1974), in which everything is intimately
connected despite distances, and the Earth functions as a unit with living beings
interacting synergistically with their inorganic environment in a complex self-­
regulating system. In these cases, we recover the notion of the importance or value
of each species. This uniqueness is linked to the exceptional characteristics of each
living being or species, which can be translated into particularities in time and space
and critical components of the biosphere. Lovelock was struck by the radical differ-
ences between Earth and the nearest planets when NASA invited him to the first
attempt to discover the existence of life on Mars; this uniqueness of Earth’s condi-
tions led him to formulate this hypothesis (Lovelock & Margulis, 1974). The
“unique” conditions of the Earth, with a self-regulating biosphere that makes its
physical environment hospitable (complete homeostasis), allow life on our planet.
The Gaia hypothesis states that the initial conditions that made life possible have
been modified by life itself. Therefore, the resulting conditions are the consequence
and responsibility of the life that inhabits them. This hypothesis emphasizes the
Earth’s ability to “recover” to a state of equilibrium after events such as mass extinc-
tions or global climatic changes. It can help predict the history and evolution of
biota in the face of future scenarios, taking into account phenomena such as climate
change. The question of whether life on Earth is an exception or whether life as a
phenomenon can occur elsewhere in the universe is a fascinating and ongoing
542 9 Overview and Final Prospects

debate. Some scientists believe that life may be possible on other planets or galax-
ies, although it may not necessarily resemble life as we know it on Earth, a concept
consistent with the mediocrity principle extended from the Copernican principle.
Consequently, the search for life beyond Earth is one of the most important and
challenging scientific endeavors of our time (Des Marais, 2000; Des Marais et al.,
2008; Kiang et al., 2018; Race & Randolph, 2002).
In the search for potential life on other celestial bodies, such as planets, moons,
or exoplanets, scientists look for evidence of current or past life through the detec-
tion of biosignatures (Kiang et al., 2018). For example, research has suggested that
microbial life could exist in the subsurface of Mars, the atmosphere of Venus, and
the oceans of some moons of giant planets (Schulze-Makuch et al., 2005). To help
assess the evidence for life beyond Earth, a “Confidence of Life Detection” (CoLD)
scale has been proposed (Green et al., 2021). Searching for planets that closely
resemble Earth’s characteristics and may be more conducive to life is undoubtedly
a challenging task, despite the discovery of over 300 million “potentially habitable”
planets in our galaxy. Despite these discoveries, no terrestrial planets with useful
photon flux, energy, and energy efficiency comparable to Earth have been observed
(Covone et al., 2021).
The “rare earth hypothesis” proposes that multicellular life forms such as those
found on Earth are exceptional in the universe. This suggests that a large number of
specific requirements, a large number of coincidences, and improbable astrophysi-
cal and geological circumstances are necessary for complex life to emerge. This
hypothesis attempts to explain the “Fermi paradox,” which asks why, given the
potential for life to expand and occupy different niches, there is no evidence of intel-
ligent extraterrestrial life on other planets or any indication of their visits to our
own. The term “rare earth” comes from the book “Rare Earth: Why Complex Life
Is Uncommon in the Universe” (2000) by Peter Ward, a geologist and paleontolo-
gist, and Donald E. Brownlee, an astronomer and astrobiologist. In their work, they
argue that planets, planetary systems, and galactic regions capable of supporting
complex life, such as Earth, the solar system, and our galaxy, are exceptionally rare.
Concluding Words In this book, we have presented a basic theoretical framework
and provided numerous examples to stimulate reflection on the evolving concepts
and facts that underlie our understanding of rules and exceptions. It is important to
recognize that there are several viable alternatives and complementary approaches
to the issues discussed here. While our current framework may be perceived as rela-
tively simple, focusing on only two components (rules and exceptions) and direct
associations along with the sources of dynamics (nature, humanity, epistemology,
and technology), we welcome new hypotheses and perspectives to enrich and extend
this theoretical foundation, making it more complex and comprehensive.
The three-context approach (time, space, and group) that we have used, while
having its limitations, provides a necessary starting point for our discussion of rules
and exceptions. It serves as a practical basis for future research, where a wider range
of variables and a richer multidimensional analysis can be considered. In this regard,
mathematical studies involving models that explore the prediction of exceptions
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standing of the dynamics between rules and exceptions. We leave a roadmap for
further exploration in this area, trusting that it will inspire scientific research that
combines epistemological and empirical aspects, drawing from the limitless exam-
ples provided by the magnificent nature that surrounds us.

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Index

A Ananas bracteatus, pineapple, 413

Acacia, 259, 323, 324 Anas platyrhynchos, 29
Acer negundo, ash-leaved maple, 438 Andrena nigroaenea, 443
Acetobacter pomorum, 337 Angraecum sesquipedale, Darwin's orchid, 31,
Acoela, 144 168, 169
Acoelomorpha, 144 Anopheles gambiae, 275
Acritarchs, 124 Anoxypristis spp., sawfish, 434
Acropora, 447 Anthozoa, stony coral, 447
Actinia equina, 316 Antilocapra americana, American
Aegilops speltoides, 295 pronghorn, 414
Aegilops squarrosa, 296 Apankura, 249
Agaricales, 153 Apis mellifera, domestic bee, honeybee, 272,
Agave spp., agaves, 444 312, 316, 449
Agelenopsis aperta, 316 Aplysia sp., 320
Agkistrodon contortrix, eastern copperhead Apocynaceae, 350
snake, 271 Apteronotus leptorhynchus, 318
Agkistrodon piscivorus, cottonmouth Aquarius remigis, 316
snake, 271 Arabidopsis thaliana, 326, 342, 455
Ailuropoda melanoleuca, giant panda, Arachnida, arachnid, 118, 175, 179, 250, 316,
188, 427 425, 451, 460, 537
Alcanivorax, 306 Arachnids, 126, 179
Aleocharinae, 159 Araneus diadematus, 460
Allocosa senex, burrow-digging wolf Araucaria araucana, araucaria, 416
spider, 59, 60 Architeuthis, 148
Allolobophora caliginosa, 317 Argiope bruennichi, 460
Allonautilus spp, 424 Argiope radon, 316
Amaranthaceae, 129 Argonauta argo, argonaut, 29
Amblyrhynchus cristatus, marine iguana, 458 Armillaria, 152, 153, 155
Ambystoma californiense, California tiger Armillaria gallica, Oregon monster, 154
salamander, 275 Asbestopluma, 135
Ambystoma tigrinum, tiger salamander, 275 Asclepias, 350
Amoebozoa, 150 Asteraceae, 264
Amphioctopus marginatus, 314 Astyanax mexicanus, Mexican tetra, 184, 409
Amphiprion clarkii, clownfish, 178 Atkinsonia, 270

© Springer Nature Switzerland AG 2024 545

A. V. Peretti et al., Rules and Exceptions in Biology: from Fundamental
Concepts to Applications, https://doi.org/10.1007/978-3-031-55382-0
546 Index

B Convoluta paradoxa, 145

Banksia ericifolia, 438 Corallorhiza, 325
Bison bison, American bison, 426, 433 Corylus avellana, common hazel, 299
Bison bonasus, 419 Cotoneaster franchetii, cotoneaster, 277
Bison priscus, 419 Cryphonectria parasitica, 188
Biston betularia, peppered moth, 290 Cryptopsaras couesii, anglerfish, 29
Boraginaceae, 264 Cryptostylis erecta, 266
Bos primigenius, aurochs, 297 Cryptostylis leptochila, 266
Bothriurus bonariensis, 23, 128, 460 Ctenophora, 144, 245
Brassica oleracea, 296 Cucurbita foetidissima, 414
Bromeliaceae, 413 Cucurbitaceae, 414
Brosimum acutifolium, 189 Cuscuta, 25
Buchnera, 236, 269 Cycadales, 262
B. aphidicola, 269 Cylindraspis peltastes, giant tortoise, 432
Cynomys spp., prairie dog, 439
Cyprinus carpio, common carp, 437
C
Cactaceae, 103, 129
Caenorhabditis elegans, nematode worm, 313, D
320, 449 Danio rerio, zebrafish, 317, 449
Caladenia longicauda, 265 Daphnia melanica, 259
Caladenia, spider orchid, 265 Daphnia, water flea, 238
Caladium steudneriifolium, 167–168 Decodon verticillatus, 409
Calcarea, 139 Demospongiae, 135
Calopteryx splendens, 441 Dendritobilharzia pulverulenta, 146
Calopteryx virgo, 441 Diceros bicornis, black rhinoceros, 434
Calyptraeidae, 182 Dictyostelium, 151
Canis lupus familiaris, domestic dog, 296 D. discoideum, 138, 151, 152
Canis lupus, gray wolf, 296, 434 Digenea, 145
Carassius auratus, bubble eye goldfish, 298 Dinoflagellata, 447
Carduus sp., thistle, 277 Dionaea muscipula, venus flytrap, 119,
Caryophyllales, 158 155, 327
Cassia grandis, pink shower tree, 413 Dipsosaurus dorsalis, desert iguana, 458
Castanea dentata, American chestnut, 188 Diptera, 459
Casuarius casuarius, cassowary, 189 Drakaea livida, warty hammer orchid, 266
Celtis tala, tala, 439 Drosera, 155–157
Centropyge potteri, angelfish, 178 Drosophila, 123, 124, 253, 313, 316, 332, 342,
Ceratitis capitata, Mediterranean fruit fly, 455 441, 449
Chlamydomonas, 183, 245 D. hawaiana, 253
Chlorella vulgaris, 246 D. heteroneura, 253
Chondrocladia lyra, 142 D. melanogaster, fruit fly, 313, 342, 449
Chondrodactylus angulifer, 182 D. mercatorum, 253
Chorioactis geaster, devil's cigar, 154 D. silvestris, 253
Chromalveolata, 150 Dryas octopetala, shrub, 417
Chromista, 150 Drymornis bridgesii, scimitar-billed
Cladorhizidae, 135, 142 woodcreeper, 438
Cnemidophorus spp., whiptail lizard, 240, 300
Coccyzus melacoryphus, dark-billed
cuckoo, 438 E
Coleoptera, 125, 159, 459 Enhydra lutris, sea otter, 189
Columba livia, common pigeon, 297, 298, Ephedra, 262
416, 449 Epifagus americana, 25
Columbicola extinctus, passenger pigeon Eratigena atrica, giant house spider, 126
chewing louse, 439 Eriaxis rigida, 265
Index 547

Erythranthe guttata, monkeyflower, 440 Hymenoptera, 103, 104, 459

Escherichia coli, 269, 304, 449 Hypsiboas cordobae, 455
Eucestoda, 146
Eudorina, 245
Euglena, 183 I
Euplecta subdecussata, 169 Ibicella lutea, 413
Euprymna tasmanica, 316 Idotea balthica, 170
Eupsilia, 459 Illex argentinus, Argentine squid, 435
Evolvulus nummularius, 169 Ipomoea pes-caprae, 169
Extatosoma tiaratum, spiny leaf stick Ischnura, 177
insect, 271 Ithomiini, 264

F J
Foraminifera, 135 Juglans nigra, Eastern American black
walnut, 325

G
Gallus gallus, fowl, 298, 345 L
Genipa americana, 414 Lactobacillus sp., 337
Gerris odontogaster, water strider, 460 Lamellaxis gracile, 169
Ginkgo biloba, ginkgo, 424 Lamnidae, sharks, 459
Glossina, 344 Latimeria spp., coelacanth, 424
Glossinidae, tsetse flies, 181 Latrodectus hasselti, 460
Glycine max, soy, 438 Legionella pneumophila, 151
Glyptemys insculpta, wood turtle, 458 Leiurus quinquestriatus, 461
Gnathifera, 118 Lepidoptera, 290, 459
Gnathostomulida, 118 Lepidosiren paradoxa, South American
Gnetales, 262 lungfish, 117
Gnetum, 262 Lepomis gibbosus, 315
Gobiodon, gobies, 178 Leptonycteris spp., long-nosed bats, 444
Gomphotheriidae, giant elephant, 413 Leptotila verreauxi, 438
Gonium, 245 Lepus europaeus, European hare, 277
Gonodactylus smithii, 138 Leratiomyces erythrocephalus, 166, 167
Smith's mantis shrimp, 147 Leucadendron laureolum, proteaceous
Gracilaria gracilis, 170 shrub, 438
Gryllus bimaculatus, 345 Leucosolenia, 139, 140
Gryllus integer, 316 L. somesii, 140
Gymnocladus dioicus, Kentucky coffee tree, 413 Licmophora, 145
Ligustrum lucidum, broad-leaf privet, 277, 438
Linaria vulgaris, 333
H Lissopimpla excelsa, orchid wasp, 266
Haliaeetus leucocephalus, bald eagle, 188 Lumbricus terrestris, earthworm, 317
Helicobacter, 269 Lutra lutra, 437
Helicosporidium, 181 Lycaena helle, 419
Hippoboscidae, louse fly, 181
Hippoboscoidea, 181
Hofstenia miamia, 317 M
Holocnemus pluchei, 316 Macaca, 300
Holothuria glaberrima, sea cucumber, 318 Maclura pomifera, Louisiana orange tree, 413
Homo sapiens, 154, 422 Magnoliaceae, 263
Homoscleromorpha, 140, 245 Mangifera indica, mango, 413
Hydra, 143, 317 Manihot esculenta, cassava plant, 264
Hydrodamalis gigas, Steller's sea cow, 432 Mastotermes darwiniensis, 418
548 Index

Mastotermitidae, 418 O. insectifera, 265

Merluccius hubbsi, Argentine hake, 435 O. sphegodes, 443
Merostomata, horseshoe crabs, 118 Opiliones, 179
Mesonychoteuthis, 148 Opisthokonta, 150
Microstomum, 143, 144 Opuntia, 274
M. caudatum, 143 O. ficus-indica, fig cactus, 274
M. lineare, 143 Ormia ochracea, 411
Mimosa, 274, 328 Ornithorhynchus anatinus, platypus, 117, 425
M. pigra, 274 Oryctolagus cuniculus, European rabbit, 273
M. pudica, 328 Oryza sativa, rice, 438
Miracinonyx, 414 Oryzias latipes, medaka fish, 335
Mirounga angustirostris, 252 Oscarella, 140
Mollusca, 144, 315 Oscarellidae, 140
Monogenea, 145 Oxypetalinae, milkweed, 170
Monosiga brevicollis, 244 Oxypetalum solanoides, 171
Monotropa uniflora, 25
Musaceae, 296
Musa paradisiaca, banana, 296 P
Mus musculus, mouse, mice, 416, 449 Panarthropoda, 128
Mustela lutreola, European mink, 436, 437 Pandorina, 245
Mustela nigripes, black-footed ferrets, 439 Panellus stipticus, 138, 152, 153
Mustela putorius, polecats, 437 Panthera onca, jaguar, 414, 434
Mycena, 153 Paradisaea apoda, paradise bird, 29
M. mycelium, 153 Paragobiodon, gobies, 178
Mycetozoa, 150 Paramacrobiotus, 136
Myiopsitta monachus, 437, 439 Parus major, 315
Mylodon darwini, mylodon, 413 Passer domesticus, 416
Myrcianthes coquimbensis, lucumillo, 413 Passiflora, 269
Myxomycota, 150 Patagioenas fasciata, 439
Patagioenas maculosa, 439
Patagioenas picazuro, 439
N Persea americana, avocado, 413
Nautilus, 16, 148, 424, 507 Pheucticus aureoventris, black-backed
N. pompilius, nautilus, 424 grosbeak, 438
Neovison vison, American mink, 436 Phragmites australis, common reed, 416
Nepenthaceae, 155 Phyllodactylidae, African gecko, 182
Nothofagus dombeyi, coihue, 416 Physarum polycephalum, 313
Notoplana acticola, flatworm, 317 Pica pica, magpie, 437
Nycteribiidae, bat fly, 181 Pieris rapae, 345
Pinguicula sp., 158
Pinus sp.
O pine, 277
Octopus, 148, 314, 316, 325 P. sylvestris, scots pine, 418
O. cyanea, 314 Pisaura mirabilis, nursery web spider, 345
O. rubescens, 316 Plasmodium, 180
Odonata, 459 Platyhelminthes, 143, 144
Odontodactylus scyllarus, peacock mantis Pleodorina, 245
shrimp, 147 Plodia interpunctella, 345
Oleaceae, 270 Podarcis hispanica, 318
Onthophagus, dung beetle, 173 Podarcis sicula, 294
Ophioderma longicauda, serpent star, 318 Podiceps gallardoi, hooded grebe, 436
Ophrys, 265, 267 Podoctidae, harvestmen, 179
O. apifera, 265, 266 Poecilia reticulata, guppy, 296
Index 549

Polychaeta, 126 Scleractinia, 447

Populus spp., aspen, 417 Sclerocormus, 117
P. tremuloides, quaking aspen, 299 Scrophulariaceae, 270
Porifera, 139, 140, 142, 179, 244, 245, 309 Semicossyphus reticulatus, kobudai
Pouteria splendens, lucumo, 413 fish, 178
Pristis pectinata, smalltooth sawfish, 271 Sequoiadendron giganteum, giant
Pristis sawfish, 271, 434 sequoia, 188
Proclossiana eunomia, 419 Serinus canaria, Gibber Italicus, domestic
Procyon lotor, raccoon, 437 canary, 298
Proteobacteria, 269 Solenopsis invicta, 261
Protium giganteum, 189 Sorghum halepense, sorghum, 438
Protozoa, 135, 150, 233, 247, 335 Spea, 258
Pseudocorticium, 140 S. multiplicata, 258
Pseudomantis albofimbriata, 460 Sphenodon spp., tuatara, 424
Pterostylis sanguinea, 266 Sphyrna lewini, hammerhead shark, 434
Pycnogonida, sea spiders, 118 Spiculosiphon oceana, 135
Pycnogonum litorale, sea spider, 127 Stenorrhynchos speciosum, 265
Pygoscelis papua, coastal penguin, 416 Streblidae, bat flies, 181
Pyracantha angustifolia, crataegus, 276–277 Sus scrofa, wild boar, 272
Python bivittatus, Burmese python, 275 Syllidae, 126
Symbiodinium spp., 190, 191
Symsagittifera roscoffensis, 144, 145
Q
Quercus spp.
oak trees, 188 T
Q. rugosa, 454 Talobionta, 149
Tapirus terrestris, South American tapir, 434
Taraxacum officinale, dandelion, 438
R Teidae, 300
Rafflesia, 25 Teleogryllus oceanicus, 411, 455
Rana pipiens, 318 Tenebrio molitor, yellow mealworm
Raphus cucullatus, dodo, 432 beetle, 449
Rattus norvegicus, rat, 416, 449 Tenodera aridifolia, 460
Rhinanthus, 270 Tenodera sinensis, 460
Rhinella marina, cane toad, 273 Tetragnatha versicolor, long-jawed orb
Rhinoptera steindachneri, golden cownose weaver, 127
ray, 434 Tetraselmis convolutae, 144
Roeseliana roeselii, 344 Thalassia testudinum, turtle grass, 170
Rosa canina, dog rose, 277 Tityus carrilloi, 416
Rosa rubiginosa, sweet briar, 277 Trachemys scripta, painted turtle, 318, 437
Rosaceae, 271, 276 Tragelaphus strepsiceros, greater kudu, 323
Rubus ulmifolius, blackberry, 276 Trematoda, 145
Tribolium castaneum, red flour beetle, 260
Triticum spp.
S T. aestivum, common wheat, 296
Saccharomyces cerevisiae, yeast, 449 T. dicoccum, 296
Salmonella, 269 T. monococcum, 295
S. typhimurium, 151 wheat, 438
Santalaceae, 270 Trochita, Sigapatella, 182
Scathophaga stercoraria, yellow dung fly, 450 Trypanosoma brucei, 280
Sceloporus undulatus, 261 Tupaia glis, common treeshrew, 105
Schistocerca gregaria, 318 Turbellaria, 143, 145
Schistosoma mansoni, 145 Turdus migratorius, spring blackbird, 437
550 Index

U X
Urophonius brachycentrus, 461 Xanthopan morganii praedicta, 168
Urophonius jheringii, 460 Xenogryllus marmoratus, 175
Utricularia spp., 158 Xenopus laevis, 300

V Y
Vaccinium corymbosum, northern highbush Yersinia pestis, 281, 282
blueberry, 299 Yersinia pseudotuberculosis, 282
Variola virus, smallpox, 497
Vibrio, 269
Volvox, 245 Z
Vultur gryphus, Andean condor, 416 Zea mays, maize, 426, 438
Zea perennis, perennial teosinte, 426
Zegalerus, 182
W Zoochlorella, 144
Welwitschia, 262 Zooxanthellae, 447
Wolbachia, 179