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First published 2019
by Routledge
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© 2019 Francesco E. Marino
The right of Francesco E. Marino to be identified as author of this
work has been asserted by him in accordance with sections 77
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For my wonderful wife, Trish, and the three treasures
we share, Emma, Alexander and Anabel. Of all the
hominins I know, they are indeed the most infatigable.
Contents

Prefaceviii
Acknowledgementsxi

1 Evolution and natural selection in human performance,

health and disease 1

2 Safety factors, reserve and trade-offs 20

3 Not just cousins 47

4 Defining and measuring fatigue 70

5 Morphology and skeletal muscle 99

6 The brain: the emotional aspect of fatigue 121

7 The environment: temperature and the human capacity

to resist fatigue 148

8 Energy in, energy out – and fatigue 179

9 Power versus endurance 203

10 Fatigue in disease 228

Index241
Preface

There are a number of personal reasons for writing this book. First and foremost
is the challenge which comes with trying to put in writing the ideas about human
performance and fatigue which I have collected over a period of 25 years as an
academic. However, some of those ideas stretch back to my younger days of being
an avid footballer (round ball!) and what seemed to be the physical training
extremes I endured at the hands of coaches. This book represents my understand-
ing of the concept of fatigue. It is an attempt to harness much of the research
which I have been involved with over the past 25 years. Much of this research
represents human exercise performance under various conditions, including
extreme temperatures.
A second reason is the challenge of writing a book which would be informative
and provocative for my fellow exercise scientists and all those that have a love
of human performance. This particular challenge was perhaps the most difficult
since I had to make assumptions about prerequisite knowledge. A third reason
is to share the joy which comes with the appreciation of human performance.
A fourth reason, but connected with the third, is that I never had the opportu-
nity to formally study evolutionary biology, except in splashes of curriculum here
and there. For this reason, over the course of an academic career I devoured all
manner of writings in the field of evolutionary science, which has led me to the
conclusion that all observations in exercise science can be explained by evolu-
tionary theory. I even went to the extreme of a sabbatical at Harvard University
in the Department of Human Evolutionary Biology. It was during this time that
I truly understood how little I understood about evolutionary biology, but it did
confirm my view that all things in human performance and disease can poten-
tially be unravelled by evolutionary theory. So, this book is the culmination of
this journey. By the way, the journey continues! Thank you, Professor Lieberman!
One of the first studies that I had the privilege to be a part of was on the
effect of lowering body temperature for improving exercise performance in the
heat, known as precooling. At the time I was captivated by the fact that reduc-
ing body temperature by as little as 0.5°C before exercise would result in better
times or greater distances. My initial and rudimentary understanding was that
body temperature was a limiting factor for exercise – an observation that had
 Preface ix

general consensus, albeit the mechanism was unknown. Over subsequent years it
became apparent that the results from these studies were very much dependent
on the exercise protocol that was used – that is, whether the exercise was either
self-paced or fixed by the experimenter. This difference meant that experimen-
tal results had to be interpreted with some caution and contextualised against
the exercise model that was used. It also meant that time to ‘fatigue’ was highly
dependent on the exercise protocol.
A crucial question in the exercise sciences is what determines how fatigue
develops during physical performance. This question has been a central tenet of
experimental studies in elite, recreationally active, healthy and diseased individ-
uals. The reason for this is that understanding what the exercise ‘stopper’ might
be regardless of health status could mean the difference between winning and
losing, improving health or even motivating more people to partake in exercise
to gain the benefits of regular physical activity. However, fatigue is not easily
defined and requires a nuanced approach to understand how to measure it and
what the potential causes might be. The exercise sciences have attacked these
questions from many different perspectives so that there are likely to be meta-
bolic, cardiovascular, respiratory, thermoregulatory and neuromuscular answers,
all with a specific story to tell and all worthy of investigation. Although much has
been learned about these systems and their responses under different conditions
in both health and disease, a glaring omission has been why these systems work as
they do. The only way to answer this particular question is to go back in time and
understand the evolutionary path taken by our biology and that of other animals.
It would not be an understatement to suggest that exercise scientists in the main
have had little or no formal training in evolutionary biology – including me!
Why is this important? As put by (Dobzhansky 1973), the simple answer is that
“nothing in biology makes sense except in the light of evolution.” For instance,
why have mammals adopted a core temperature balance point of 37°C? Why not
25°C or 42°C? What advantages would this particular body temperature have
and what were the determining factors for its evolution and eventual adoption?
Why the erect posture and bipedal locomotion? Some of these questions have
been studied and debated, in some cases for centuries. Definitive answers to these
questions will not be found in this book, but potential explanations and proposi-
tions are provided that might cause us to think differently about our health and
performance capabilities.
The central theme of this book is that evolution played a part in how we as
humans, when compared to other mammals, in particular our non-human pri-
mates, began on a biological path eventuating in the ‘choice’ between endurance
and power. As such, the contention is that the biological machinery that provides
for endurance also improves our fatigue resistance. To make this case, Chapter 1
deals mainly with the basics of evolutionary theory. This includes the concepts of
adaptation and exaptation and their relationship to fatigue. Chapter 2 introduces
the concepts of safety factors and trade-offs in physiology. Surprisingly this is an
area that is under-appreciated in the exercise sciences given that much of the
x Preface

field attempts to explain why some of us are better than others at certain physical
feats. Chapter 3 provides physical comparisons between us and our closest living
relatives and what this means in terms of structure and function. Understanding
fatigue also requires a framework to define and measure it. Therefore, Chapter 4
deals with the framework at the cellular and organismic level and provides exam-
ples of how fatigue can be measured. Chapter 5 compares the human morphology
to that of Neanderthals and other extinct species. The reason for this comparison
is that there are striking similarities and differences between living and extinct
species which provide insight into whether endurance was a favoured adaptation
and played a part in our survival.
The human brain represents the pinnacle of human evolutionary biology.
Chapter 6 discusses the complex nature of the human brain in relation to fatigue
and its emotional construct. A striking physiological capacity of humans is our
ability to sweat profusely and thermoregulate effectively. Chapter 7 discusses
this unique ability, comparing and contrasting that of other mammals that have
chosen endurance or power. In Chapter 8 the vexing problem of energy and its
relationship to physical activity and health is discussed. The lurking problem
of energy-in and energy-out is highlighted in relation to fatigue. Chapter 9 will
provide a historical context to the concepts of endurance and power, their meas-
urement and inherent limitations. Finally, Chapter 10 utilises two pathologies
(multiple sclerosis and myasthenia gravis) to illustrate the difference between
central and peripheral fatigue and how fatigue generally manifests in these
illnesses.
A caveat: I am not an expert in all of the areas covered in this book. There are
volumes written by scholars about evolutionary biology as a stand-alone topic;
this is not an attempt to even remotely replace those writings. It is an attempt to
draw the concepts of evolutionary biology closer to human fatigue, performance
and health. Throughout the book I have needed to repeat certain concepts for
the sake of clarity. My hope is that this book will invite exercise scientists and
all those involved or interested in human performance generally to think more
broadly about our capabilities. Specifically, that human fatigue is a complex phe-
nomenon and that it cannot be unravelled merely by studying individual systems.
Evolution played a major role in achieving the human biology and form so that
all of our observations cannot be detached from the tinkering that occurred over
some 5 million years. To deny this, and not consider why we might have chosen
endurance rather than power, means that we will have missed the opportunity to
understand more fully who we are and what our strengths and frailties might be.

Reference
Dobzhansky, T., 1973. Nothing in biology makes sense except in the light of evolution.
The American Biology Teacher, 35(3), pp. 125–129.
Acknowledgements

When writing a book, it is almost impossible to acknowledge all the individuals

who have had a hand in shaping one’s thoughts and ideas about a topic. A book is
a culmination of many years of thought, discussion, reading, arguments and assis-
tance. I want to apologise upfront if I have missed anyone in this regard. I have
done my best to make mention of individuals and groups which have assisted me
in my intellectual journey.
As an undergraduate student I attended a conference where Professor Tim
Noakes from the University of Cape Town presented on the failure to thermoreg-
ulate during distance running. At one point he asked the simple question, “Why
do the majority of runners collapse only when they cross the finish line?” I was
struck by this obvious yet simple observation, perhaps not because of its scientific
merit but rather its philosophical catch. This was surely a paradox worthy of
investigation. Having completed a PhD in thermoregulation and performance,
I ventured to Cape Town and completed my sabbatical, where I was heavily influ-
enced by the way in which science was practised at this laboratory. For this oppor-
tunity I am grateful to Professor Noakes and the staff.
I am also indebted to Professor Mike Lambert, who has been a source of aca-
demic integrity and friendship for over 20 years. I am particularly grateful to Pro-
fessor Daniel Lieberman from the Department of Human Evolutionary Biology at
Harvard University. Dan took a chance to host an academic (and family) with an
interest in evolutionary biology and gave me time to discuss, critique and develop
ideas about human fatigue which might not otherwise have been possible. I want
acknowledge Professor Bob Meyenn, the individual who initially gave me a job
as an academic and has remained a valued friend. Bob taught me the true value
of education and free thinking.
Over a period of about 15 years I have had the privilege to lead a staff dedi-
cated to teaching and learning and to the pursuit of knowledge. I am indebted to
my colleagues and the many Honours and PhD students of the School of Exercise
Science, Sport & Health who have given me support and inspiration to think
differently about all things human.
xii Acknowledgements

Finally, I wish to acknowledge my parents, Francesco Snr and Raffaella, who

with a limited education understood the power that comes with thinking for
oneself.
My wife, Trish, and our beautiful children, Emma, Alexander and Anabel,
continue to indulge my many odd behaviours with good cheer. The value of your
love and support is beyond any human measure. Thank you.
Chapter 1

 volution and natural selection

E
in human performance, health
and disease

How extremely stupid not to have thought of that.

– T.H. Huxley’s reaction after reading Darwin’s The Origin of Species

Introduction
Any typical textbook dealing with the broad topic of exercise physiology or exer-
cise science will include cursory information on human evolution, if at all. This
is perhaps not surprising given that evolutionary theory is generally accepted and
that scientists have a working knowledge of the topic. On the surface this is likely
to be true, for the basic assumption is that humans, like all other living organisms,
evolved over a long period of time – evolutionary time. On this point, we take
this to signify millions of years of tinkering that eventually spawned the modern
form of Homo sapiens. One of the problems with this line of thought is that the
evolution of Homo sapiens was directional and that we are the outcome. That is,
evolution was linear and the only possible result is what we have today. This view
is so far from reality and the facts that we have typically become passive in our
understanding of evolutionary theory and how it can be applied to understand
and solve our modern-day problems. In fact, very few of us would consider evo-
lutionary theory as a means of understanding our biology as applied to human
performance and health.
In order to address this fundamental understanding of human physiology as
it pertains to performance, health and disease, this chapter introduces some of
the most fundamental concepts of evolutionary theory before venturing into
the complexities of form and function. This chapter considers the concepts first
introduced by Darwin and Huxley, along with the classic studies confirming that
evolution is something more than just a theory, but a process which is alive and
dynamic. To begin our quest in understanding the place of evolution in biology
and in human performance we need only reflect upon the reasoning given by
eminent scholars in the field.
In his highly cited 1973 paper titled “Nothing in biology makes sense except
in the light of evolution,” Theodosius Dobzhansky (1973) outlines the arguments
2 Human performance, health and disease

and counter-arguments that are typically used in the debate as to whether evo-
lution is a verifiable theory. Although this paper is usually invoked as a way
of asserting that the cornerstone of biology is in fact evolutionary theory, it is
worth reiterating the basis of Dobzhansky’s argument. In his description of life’s
remarkable diversity, Dobzhansky also notes that the unity of life is in fact no less
remarkable. That is, from the most seemingly rudimentary life, such as a virus, to
the most complex organism, the biochemistry is not only similar but also simple.
This is not to suggest that DNA and RNA are uncomplicated; on the contrary, it
is the universality of the biochemistry that is indicative that all life is intimately
connected by preserving the most basic primordial features. The classic theories
of Oparin and then Haldane (Miller 1953; Miller et al. 1997) provide the basis
from which life likely arose, whereby the Earth’s atmosphere, composed largely of
nitrogen, ammonia, methane and helium, combined in a primordial soup to form
the building blocks of life, the amino acids. The way in which amino acids con-
stitute sequences for given kinds of proteins and that vary within and between
species, along with single amino acids arising by genetic mutations, Dobzhansky
submits “that all these remarkable findings make sense in the light of evolution;
they are nonsense otherwise” (p. 128). However, the essence of Dobzhanky’s rea-
soning is as follows:

There is, of course, nothing conscious or intentional in the action of natural

selection. A biologic species does not say to itself, “Let me try tomorrow (or
a million years from now) to grow in a different soil, or use a different food,
or subsist on a different body part of a different crab.” Only a human being
could make such conscious decisions. This is why the species Homo Sapiens is
the apex of evolution. Natural selection is at one and the same time a blind
and creative process. Only a creative but blind process could produce, on the
one hand, the tremendous biologic success that is the human species and, on
the other, forms of adaptedness as narrow and as constraining as those of the
over specialised fungus, beetle, and flies.
(p. 127)

Although there are numerous texts outlining the basic tenets of evolution, the
purpose of this section is to provide what might be regarded as the fundamental
aspects of evolutionary theory thought to have a direct relationship to under-
standing human performance and our ability to live healthy lives and avoid dis-
ease. To this end, there are two terms used in the foregoing passage taken from
Dobzhansky’s paper that are fundamental to understanding evolutionary theory.
These are natural selection and adaptedness. In order to apply the principles of
both natural selection and adaptedness to any aspect of biology, especially when
attempting to understand human health and disease from an evolutionary per-
spective, we must first consider the context in which they were originally used by
Darwin in The Origin of Species (Duzdevich 2014). In articulating what Darwin
considered to be natural selection, he noted that very slight variations regardless
 Human performance, health and disease 3

of their causation would in some way benefit the individuals of a particular species
in their relationship with other living things and/or their physical environment.
One critical aspect of this would be that these benefits, however small, would
be passed on to the offspring. This transmission from parent to offspring will
provide a greater chance for reproductive success and, therefore, the preservation
of the species. Although the process of natural selection would seem straightfor-
ward, Darwin also recognised that this was dependent on the key observation
that only a small number of individuals that are born can actually survive. This
simply means that every living thing is always striving to increase its numbers.
But why? The answer to this is not apparently obvious. Huxley (2010) in his clas-
sic work notes that there is a tendency for all organisms to increase in geometri-
cal ratio. That is, in the early stages of existence the offspring are always more
numerous than their parents, even though the numbers of a given species tend
to remain approximately constant. Thus, if more young are produced than can
survive, the only conclusion that can be drawn is that there must be competition
for survival (Huxley 2010). It is this competition or struggle for existence that will
assist in the accumulation of variations as being either favourable and therefore
passed on or unfavourable and not passed on because of the failure to reproduce.
Natural selection is concerned only with improving the chances of reproducing.
The term adaptation or adaptedness implies that there is a shaping of a particular
feature or features of an organism in order that there is a better fit with its physi-
cal environment. However, for adaptation to take place the process relies on the
multitude of individual differences which appear in a population. In essence, all
species, including humans, are variable. That is to say that individual members of
a particular group will vary in a number of their characteristics. Some members
of a group will be taller than others, more or less agile, more or less muscular
and more or less resistant to disease. In fact, this kind of variation is seen at all
levels of the organism – from molecular to gross anatomical features. Let us now
look at two typical examples which help illustrate the importance of adapta-
tion. The most widely cited example of rapid adaptation is that of the peppered
moth during the Industrial Revolution in England (Cook & Turner 2008). There
are two types of peppered moths: the light-bodied and the dark-bodied. Before
the Industrial Revolution the dark variety was thought to be rare. However, the
light-bodied variety was much more numerous as it was able to blend in with the
light-coloured lichens on trees, whereas the black-bodied variety would be easily
picked off by birds due to their higher visibility. Within decades of the Industrial
Revolution the trees between London and Manchester became darkened as a
consequence of soot deposits from coal burning in addition to the lichens dying
on the trees as a consequence of the increased sulphur dioxide emissions. The
darkened trees now effectively provided less camouflage for the light-coloured
moths, whereas the number of dark-coloured moths being picked off by birds
was dramatically reduced. The outcome was a rapid increase in the number of
dark-coloured moths. To confirm that the population of dark-coloured moths was
indeed due to natural selection and rapid adaptation to the environment, it is
4 Human performance, health and disease

believed that a series of experiments (Kettlewell 1955, 1959) in which the film-
ing of the predation of birds on moths in both polluted and unpolluted woodlands
is an instance where Darwinian evolution was captured in action (Majerus 2008).
The observations on the peppered moth provide some compelling evidence
at the macro level for evolution by natural selection. Even more compelling are
the experiments conducted on the bacterium E. coli (Lenski & Travisano 1994).
These researchers took the opportunity to put to the test evolution by natural
selection in fast-forward motion since these bacteria reproduce asexually, so that
cloning can create a huge population of identical individuals in a very short time.
After taking 12 separate populations of identical bacteria and propagating them
in replicate environments for 10,000 generations, they were able to report on two
properties of the evolving bacterial population: cell size and mean fitness. These
two properties were studied because size is a trait which influences the functional
properties of an organism, whereas fitness is the trait which is utilised by the
organism to compete for resources. The interesting aspect of this experiment was
that the researchers employed natural selection by imposing an environment
on the bacterial populations rather than artificial selection. In this way they
were able to ascertain whether there were any heritable properties that would
enhance reproductive success in that particular environment. A key aspect of
this experiment was the chosen environment in which the bacteria were placed.
The environment was essentially a glucose broth which was calculated to sup-
port a given number of cells. Each day the bacteria were observed to grow until
the glucose was depleted, at which time some of the bacteria were transferred
to new replicate environments. This continued for 1,500 days until such time
that the original bacteria reached 10,000 generations in 12 different populations.
The first interesting result is that cell size in the bacterial population increased
rapidly for approximately the first 2,000 generations when introduced to the new
environment. However, when the environment remained unchanged for several
thousand generations, increases in cell size were less than negligible. As suggested
by the authors, the trajectories appear to be very similar but reached different
plateaus for cell size, leading them to conclude that the populations diverged
from the common ancestor and from one another in at least the size of the cells.
To measure the fitness of the bacteria the researchers then resurrected the
original (ancestral) frozen bacteria and placed them in direct competition with
the more recent generation. The questions they were asking were whether the
evolutionary trajectories of fitness were similar to that observed for the cell size
or fitness improved at a constant rate throughout the experiment. Beyond the
striking similarity between cell size and relative fitness is that adaptation to the
environment in all 12 populations was rapid when introduced to the new envi-
ronment compared to when the environment was constant over several thousand
generations. Taken together, the increase in cell size and the change in rela-
tive fitness show that significant variation arose in the early stages of the experi-
ment and then persisted until the end of the experiment at 10,000 generations.
The fact the mean relative fitness was initially equal to zero in all populations is
 Human performance, health and disease 5

indicative that mutations arose independently in each population, even though

the environments in which the bacteria were placed were identical.
These two examples of the adaptedness of the peppered moth and E. coli high-
light the three conditions required for evolution by natural selection to occur:
(1) there is variation among individuals within a population, (2) the variation is
heritable, and (3) the variation is related to the success of individuals in compet-
ing for resources.
The preceding discussion considered only the overarching understanding of
evolution by natural selection. It did not, for example, consider the workings of
genetics in the grand scheme of evolution. The purpose of the preceding discus-
sion was merely to outline the key determinants of evolution and provide the
reader with the conceptual framework which will be used throughout the book.

Evolution, disease and human fatigue

In the preceding section, we considered two examples of evolution by natural
selection: the peppered moths and the bacterium E. coli. One might well ask,
what have the peppered moths and E. coli to do with evolution by natural selec-
tion with respect to human performance, health and disease? The simple answer
is that whatever mechanisms were at play in the adaptedness of the peppered
moths and the bacteria to their environment would surely also have been at play
when we consider our evolutionary path, our resistance to disease and our ability
for physical and mental performance in a wide range of human endeavours. It is
a safe assumption within the scientific community that there is no dispute that
natural selection occurs. However, its significance in explaining human perfor-
mance in a wide range of activities and situations must be demonstrated by way
of evidence. This section will explore factors thought to have led to the unique
human traits that distinguish us from our ancestors, both living and past.
When we consider impressive human feats such as the breaking of the four-
minute mile, the 100m sprint in under ten seconds, edging ever closer to the
two-hour marathon and even the impressive swimming records, one can’t help
but be amazed at the resilience and beauty of the human in action. We would be
forgiven if we thought, just for a moment, that our biology was indeed perfect.
In reality, when we consider the uniqueness of humans, we cannot help but also
notice that many of our ailments can arguably be related to our imperfect biol-
ogy. Thus, there is an imperative to understand how and why our biology is the
way it is and what limitations it imposes when we interact with our environ-
ment. As we have already seen, an organism’s survival is dependent to a large
degree on its adaptability and whether those advantageous traits are passed on to
the next generation. This is the case for humans as well. Therefore, it would be
more than helpful to understand how humans evolved and which adaptations are
useful and which are not. If we understand this aspect of human evolution, we
might then be in a position to not only understand but also predict why we get
sick and why our performance is perhaps limited in certain circumstances as well
6 Human performance, health and disease

as truly appreciating the wondrous feats we are so accustomed to seeing. By way

of illustration, there are some modern-day chronic diseases which we can use to
illustrate this point.
There will be little argument that obesity is a prevalent disease for which we
seemingly have had no answer, at least within the last 20 years. The latest obe-
sity update from the Organisation for Economic Co-operation and Development
(OECD; www.oecd.org/health/obesity-update.htm) indicates that at least 18%
of the adult population in OECD countries is obese, constituting about 1%–3%
of healthcare expenditure in most countries but up to 5%–10% in the United
States. The knock-on effect of the disease is likely to result in the appearance
of other chronic diseases, such as Type 2 diabetes mellitus. Although the OECD
update and others (Gard 2011) also report the rate of rise in obesity in the last five
years has slowed, there is little to indicate that we have dealt with the problem
effectively. There is little doubt that significant gains can be made by understand-
ing the physiology on a systemic and molecular level of such a disease, yet little
or no attention has been paid to truly understanding why we have been powerless
to curb the incidence of the disease. Is there an alternative approach that can be
used to solve this problem? How can evolutionary theory by natural selection
help us to understand (1) why obesity has increased so rapidly in a relatively
short period of human history, and (2) how we can use our knowledge of natural
selection to guide us in finding the solution for such a modern-day disease? This,
of course, is not to assert that obesity never existed in the past, when it clearly
did. Rather, the issue is why this disease has appeared so suddenly and taken hold
so rapidly when in 1980 fewer than one in ten people were obese, whereas this
is now up to six in ten people in some countries. At the very least this gives us a
clue that the disease is almost entirely preventable.
So, the big question it seems is, why does it occur? Why are humans susceptible
to this disease and why are some of us more likely than others to fall into its grasp?
These questions alone are compelling enough to make us think deeply about our
roots and understand the factors of our past that have made us so susceptible
to the disease. Perhaps a better question to ponder is, what parts of our biology
actually haven’t changed since humans appeared, and are these the responsible
villains?

Adaptations and health

Returning to the phenomenon of adaptedness, it is perhaps within this construct
that the answer to our crisis of chronic ill health lies. In considering this, the
most obvious question to ask is, what adaptations took place over millions of
years that were useful over a long period of our existence in extremely differ-
ent environments and provided for reproductive success, but perhaps are now
conspiring to cause us grief? There is good reason to believe that the changes
in our immediate environment have shifted so much that our physiology has
not been able to adapt quickly enough in order to deal with the more accessible