What Teeth Reveal about Human Evolution

Over millions of years in the fossil record, hominin teeth preserve

a high-fidelity record of their own growth, development, wear,
chemistry, and pathology. They yield insights into human evolution
that are difficult, if not impossible, to achieve through other sources of
fossil or archaeological data.
Integrating dental findings with current debates and issues in
paleoanthropology, this book shows how fossil hominin teeth shed
light on the origins and evolution of our dietary diversity, extended
childhoods, long lifespans, and other fundamental features of human
biology. It assesses methods to interpret different lines of dental
evidence, providing a critical, practical approach that will appeal to
students and researchers in biological anthropology and related fields
such as dental science, oral biology, evolutionary biology, and
paleontology.

debbie guatelli-steinberg is Professor of Anthropology, and

Courtesy Professor of Evolution, Ecology, and Organismal Biology at
The Ohio State University. She has conducted extensive research on
fossil hominin teeth in Africa, Europe, and Asia, and has published
widely in the fields of dental paleoanthropology and dental
primatology.
What Teeth Reveal about
Human Evolution

debbie guatelli-steinberg
The Ohio State University, USA
University Printing House, Cambridge CB2 8BS, United Kingdom

Cambridge University Press is part of the University of Cambridge.

It furthers the University’s mission by disseminating knowledge in the pursuit of
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Information on this title: www.cambridge.org/9781107082106
© Guatelli-Steinberg 2016
This publication is in copyright. Subject to statutory exception
and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without the written
permission of Cambridge University Press.
First published 2016
Printed in the United Kingdom by TJ International Ltd. Padstow Cornwall
A catalogue record for this publication is available from the British Library
Library of Congress Cataloging-in-Publication data
Guatelli-Steinberg, Debbie, 1961– author.
What teeth reveal about human evolution / Debbie Guatelli-Steinberg.
Cambridge ; New York : Cambridge University Press, 2016.
LCCN 2016015474| ISBN 9781107082106 (hardback) | ISBN 9781107442603
(paperback)
| MESH: Paleodontology – methods | Tooth – anatomy & histology | Anthropology,
Physical | Odontometry | Biological Evolution
LCC GN209 | NLM GN 209 | DDC 599.9/43–dc23
LC record available at https://lccn.loc.gov/2016015474
ISBN 978-1-107-08210-6 Hardback
ISBN 978-1-107-44260-3 Paperback
Cambridge University Press has no responsibility for the persistence or accuracy of
URLs for external or third-party internet Web sites referred to in this publication,
and does not guarantee that any content on such Web sites is, or will remain,
accurate or appropriate.
To my husband Daniel J. Steinberg and to Rose M. Guatelli,
John L. Guatelli, Maria Catena (Zumbo) Sottile, and A. John
Sottile
 Contents

Acknowledgments page ix

Introduction: The Convenient Tooth 1

PART I: TEETH AND AUSTRALOPITHS 9

1 March of the Bipeds: The Early Years 11

2 Dentally-Derived Dietary Inferences:

The Australopiths 30

3 Curious Canines 59

4 Incisive Insights into Childhood 84

PART II: TEETH AND THE GENUS HOMO 111

5 March of the Bipeds: The Later Years 113

6 Dentally-Derived Dietary Inferences: The Genus

Homo and Its Diminishing Dentition 137

7 Long in the Tooth: Life History Changes in Homo 157

8 Knowing Neanderthals through Their Teeth 177

vii
viii contents

9 Insights into the Origins of Modern Humans and

Their Dental Diseases 211

10 Every Tooth a Diamond 232

References 246
Index 282
 Acknowledgments

There are many people whose influence and direct assistance I would
like to thank. I am indebted to my dissertation advisor, John Lukacs,
for introducing me to the world of dental anthropology. I am also
indebted to my most frequent collaborators: Donald Reid, Bruce
Floyd, Joel D. Irish, Rebecca Ferrell, John P. Hunter, Paul Sciulli, Song
Xing, and Patrick Mahoney. I thank Scott McGraw and Jeff McKee for
reading and commenting on portions of the manuscript. I am grateful
and fortunate to have worked with Alyssa Starrett, who drew many of
the figures, and Tom Broa, who helped with research and referencing.
I also thank Rob Scott for sharing his microwear texture images and
Song Xing for the images of incisor shoveling in Homo erectus.
The assistants and editors at Cambridge University Press provided
much appreciated support, most especially Sarah Payne. Sources of
ongoing inspiration are my current and former graduate students.
Above all, I am thankful to my husband Dan Steinberg for his
unflagging support of this project.

ix
 Introduction: The Convenient
Tooth

A book about fossil teeth would have been unthinkable before 1669.
Three years earlier, a group of Tuscan fishermen caught a colossal
white shark. As Brian Switek tells the story in his engaging book,
Written in Stone: The Hidden Secrets of Fossils and the Story of Life
on Earth, that shark excited the imagination of Medici Grand Duke
Ferdinando II, a great patron of the sciences (1).
The shark’s body was too large to transport and had begun to
decompose anyway, so its head was cut off and sent to the Grand
Duke, who chose his most talented resident anatomist for the privi-
leged job of dissecting it (Figure i). Danish-born Nicolaus Steno (aka
Niels Steensen) turned out to be the man for the job (1). As he poured
over his dissection, Steno was struck by the uncanny similarity of the
shark’s teeth to what were then popular triangle-shaped stones called
glossopetrae or “tongue stones” (2, 3) (Figure 1).
At the time, glossopetrae were used for all sorts of purposes: as
antidotes to snake venom, treatments for epilepsy, amulets, and when
ground into a fine powder, as toothpastes (2, 3). Roman philosopher
Pliny the Elder thought glossopetrae dropped from the sky on moon-
less nights (4). Inspired by his shark dissection, Steno published his
own explanation in 1669. He suggested that the corpuscular theory,
which held that matter was made of tiny corpuscles, could explain
how shark teeth turned to stone (5). When the teeth were buried in
sediments, the corpuscles of minerals gradually replaced the corpus-
cles that made up teeth, transforming them into stone. This explana-
tion is not so far from our modern understanding of how fossils form.
In the case of fossil teeth though, most of the original mineral remains
while mineral from surrounding sediments fills in tiny pore spaces
within them in the process of permineralization.

1
2 introduction: the convenient tooth

figure i: Shark head dissected by Niels Steensen (Steno). Image from

Elementorum myologiae specimen, 1669.
 introduction: the convenient tooth 3

That fossil teeth played such a starring role at the dawn of

paleontology is no coincidence. To be sure, sharks lose a lot of teeth.
But it is the fact that teeth are hard, compact, and composed of
mineralized tissue that makes them prime candidates for preservation
and fossilization. Indeed, most of the fossil record consists of teeth and
that is also true of the human fossil record. This book is about what
fossil teeth tell us about human evolution. Though they probably
can’t cure snake bites (I am not sure anyone has tried), the fossil
teeth of our ancestors are surprisingly versatile in their uses for telling
us about our past.
Teeth are the only parts of our skeleton that interact directly
with our environments. Their direct interactions with food place
them squarely in the path of evolutionary change. Thus, in large
part, teeth tell us so much because they have evolved directly in
response to our diets and changing ways of life. Our ancient ancestors
had big teeth for processing hard and in some cases tough foods. Yet,
over our evolutionary history, as we became increasingly dependent
on cultural solutions such as tools and fire to break down food,
our teeth dramatically reduced in size. The types of foods our ancient
ancestors ate and how they ate them also left behind traces in their
teeth during their lifetimes. These traces include distinctive micro-
scopic marks on teeth produced by chewing different kinds of foods
and tiny plant parts preserved in calcified plaque (dental calculus).
A less well-appreciated fact is that, as parts of our anatomy,
teeth are affected indirectly by changes occurring elsewhere in our
bodies, whether these changes occurred over evolutionary time scales
or during the lifetime of an individual. Thus, evolutionary changes in
a species’ teeth tell us about evolutionary changes in the species as
a whole. For example, like the rings of trees, growth lines in enamel
(the outer covering of teeth) form at known intervals. But, instead of
representing years of growth like tree rings, enamel growth lines
represent days of growth and are preserved in enamel that is
millions of years old. Because the growth of different parts of our
body is generally integrated, the pace at which teeth grow, to a large
4 introduction: the convenient tooth

extent, reflects the pace at which our bodies grow. We can track the
evolution of extended juvenile growth periods, a hallmark of human-
ity, by tracing changes in tooth growth in our ancestors through time.
Over individual lifetimes, tooth growth during childhood can be dis-
rupted by malnutrition and disease, telling us about episodes of phy-
siological stress our ancestors experienced as they grew.
Evolutionary changes in teeth took place in the broader context
of human environments that included social relationships and cul-
ture. The direct and indirect responses of teeth to our physical, social,
and cultural environments make teeth a model system for tracing the
origins and evolution of our dietary diversity, extended childhoods,
long lifespans, and other key features of our unique biology. These
insights are made possible because over the millions of years of the
fossil record, teeth preserve a high-fidelity record of their own growth,
wear, chemistry, and pathology.
On top of this, the morphology of teeth – their shapes, cusps,
and grooves – is highly heritable. This means that a great deal of
variation in dental morphology is caused by variation in genes,
rather than by the environment (6). For this reason, dental mor-
phology can be used as a marker of species identities and relation-
ships. It’s no wonder that the eighteenth-to-nineteenth century
French naturalist Baron George Cuvier is reported to have said
“Show me your teeth and I will tell you who you are.” Cuvier
was referring to the distinctive features of vertebrate species’ fossil
teeth. He could just as well have made the same claim on a smaller
scale for hominins, the taxonomic group of related species that
branched off from our common ancestor with chimpanzees.
(Figures ii and iii illustrate the morphology and names of the
principal cusps of modern human molars. These principal cusp
names will be used throughout the book.)
I have studied many of the teeth of fossil hominins, from
Australopithecus to Neanderthals, and have conducted research on
or related to several of the topics covered in this book. In doing so,
I have grown to appreciate the importance of teeth in our evolutionary
 introduction: the convenient tooth 5

B
D M
L
metacone

paracone

hypocone
protocone

figure ii: Occlusal (chewing surface) view of upper right first molar
with names of principal cusps. In the upper right of image is a direction
key. “B” stands for “buccal,” the side of the tooth facing the cheek; “L” for
“lingual,” the side of the tooth facing the tongue; M for “mesial,” the side
of the tooth facing the midline (and in the case of molars toward the front
of the mouth); and D for “distal,” the side of the tooth facing toward the
back of the mouth. Drawn by Alyssa Starrett.

entoconid metaconid

L
D M
B

hypoconulid

protoconid
hypoconid

figure iii: Occlusal (chewing surface) view of lower right first molar
with names of principal cusps. At the right of image is a direction key. “B”
stands for “buccal,” the side of the tooth facing the cheek; “L” for
“lingual,” the side of the tooth facing the tongue; M for “mesial,” the side
of the tooth facing the midline (and in the case of molars toward the front
of the mouth); and D for “distal,” the side of the tooth facing toward the
back of the mouth.

history and the many clues about our past that fossil teeth hold. What
prompted me to write this book was a desire to synthesize dental
insights into human evolution. Here, I emphasize how evolutionary
changes in human teeth are linked to key evolutionary trends in
human evolution: the broadening of our diets, our increasing reliance
6 introduction: the convenient tooth

on culture, our expanding brains, and the lengthening of our child-

hoods and lifespans. Because of these links, and because of the detailed
information fossil teeth preserve, insights into human evolution are
possible that are difficult, if not impossible, to achieve through other
sources of fossil or archaeological data. Here, I further highlight how
the evolution of teeth reflects human evolutionary dynamics, in
which cultural adaptations shape and are also shaped by biological
adaptations.
This book is meant to be an accessible account of many of the
major insights into human evolution that can be gleaned from the
study of teeth. In some instances these insights are about our teeth
themselves, but more often these insights relate to larger evolutionary
trends. The book is not about the detailed morphology of teeth but
about the hard-earned insights into human evolution that dedicated
researchers have extracted (excuse the pun) from fossil teeth. I intend
the book for those who have a passion for human evolution in general
and/or a particular curiosity about how human teeth inform us about
our evolutionary history.
Intended readership also includes undergraduates in human
evolution or dental anthropology courses. But the book is not meant
to be a textbook for these courses. The book integrates dental findings
with debates and issues in paleoanthropology, and in this respect,
I hope that the book will be used to generate discussion in under-
graduate classes. Most of the chapters (i.e., the nonintroductory ones,
Chapters 1 and 5) would also work as starting points for discussion in
graduate-level classes.
The book is divided into two parts: the first concentrates on the
earlier time period of human evolution (primarily on Australopiths)
and the second on the later time period (focusing on the genus Homo).
(See Figure iv for a timeline of human evolution.) Most chapters
emphasize particular species or lineages that are subjects of debate
and/or extensive research activity. Part I covers the broad outline of
early human evolution with special attention to teeth (Chapter 1),
explores what various lines of dental evidence tell us about diet in our
7 Mya 6 Mya 5 Mya 4 Mya 3 Mya 2 Mya 1 Mya Present

Sahelanthropus tchadensis
Orrorin tugenensis
Ardipithecus kadabba
Ardipithecus ramidus
Australopithecus anamensis
Australopithecus afarensis
Australopithecus bahrelgazali
Kenyanthropus platyops
Australopithecus deyiremeda
Australopithecus africanus
Homo habilis
Paranthropus aethiopicus
Australopithecus garhi
KEY Paranthropus boisei
Earliest possible hominins (limited evi- Paranthropus robustus
dence for bipedalism) Homo erectus
Small-brained hominins Homo antecessor
Small-brained hominins with large back Homo heidelbergensis
teeth and robust crania and jaws Homo neanderthalensis
Hominins of the genus Homo, characterized by Homo sapiens
trends of brain size increase, dental reduction,
Homo floresiensis
and longer growth periods

figure iv: Time-line for human evolution. Species are ordered chronologically by their approximate first appearance dates.
Drawn by author.
8 introduction: the convenient tooth

early (pre-Homo) ancestors (Chapter 2), considers whether sexual

dimorphism in hominin canine teeth is related to levels of competi-
tion among males (Chapter 3), and synthesizes our understanding of
what incremental growth lines in fossil teeth reveal about the length
of juvenile growth periods in our earliest ancestors (Chapter 4).
Part II focuses on the genus Homo. Chapter 5 sketches the broad
outline of evolution within the genus Homo, again with special atten-
tion to teeth. Chapter 6 explores interrelationships among changes in
tooth size, culture, and diet in the genus Homo prior to Neanderthals
and modern humans. Chapter 7 evaluates dental evidence for the
evolution of childhood and longevity in the genus Homo before
Neanderthals and modern humans. Chapter 8 highlights dental
insights into Neanderthal phylogeny, behavior, diet, and life history.
Chapter 9 emphasizes the contribution of teeth to understanding the
origin of anatomically modern Homo sapiens and our dental diseases.
Concluding, Chapter 10 recapitulates the book’s main points and
explores how an appreciation of our dental past can help us understand
how we view and treat teeth today.
To pursue the insights that fossil teeth offer, we first need to
discuss how evolutionary relationships among fossil species are
assessed and to sketch the broad outlines of early human evolution.
part i Teeth and Australopiths
1 March of the Bipeds: The Early
Years

It is, however, very difficult to establish the precise lines of descent,

termed phylogenies, for most organisms.

– Ayala FJ and Valentine JW

Evolving: The Theory and Process of Organic Evolution (7)

As understood today, human evolutionary history involves some

twenty species of fossil hominins, give or take a few depending on
the taxonomic scheme to which one subscribes. In the field of
paleoanthropology, taxonomic questions – how to classify fossil
species – are famously contentious. As Richard Dawkins com-
ments in the Ancestor’s Tale (8), there is more than one paleon-
tology book in print entitled “Bones of Contention.” Names given
to species carry implications for how species are related to one
another. A species placed in the genus Homo for example, is
recognized as sharing a more recent common ancestor with mod-
ern humans than a species placed in the genus Australopithecus.
Resolving species relationships is no straightforward task. That
is one reason (among others) why there are so many different points of
view about evolutionary relationships among hominin species. Such
relationships are summarized in diagrams called phylogenies or phy-
logenetic trees. All methods of constructing phylogenies rely on com-
paring the characteristics of species, from their DNA sequences to
their dental features to any aspect of their anatomy and even behavior.
The most direct means of genetic comparison is through DNA, but,
only in more recent hominins has it thus far been possible to extract
adequately preserved DNA (see Chapter 5). For earlier species, the
characteristics of teeth and bones must suffice for assessing evolu-
tionary relationships. As noted, teeth figure prominently in such
assessments: they are extremely well-preserved in the fossil record

11
12 march of the bipeds: the early years

and much of the variation in their morphology is due to genes (rather

than environment).
There are different ways to assess evolutionary relationships
among species. According to the method of phenetics,1 all available
traits should be used to construct phylogenies. Species with greater
similarity are considered more closely related. This method does not
take into account two big problems. The first is the problem of homo-
plasy, when two species have similar traits but not because they
inherited them from a common ancestor. One way that homoplasy
can occur is when species independently evolve similar solutions to
similar problems. The wings of dragonflies and seagulls were not
inherited from their common ancestor but evolved independently as
adaptations for flight in their separately evolving lineages. Another
way homoplasy can occur is through reversal. In this instance, a trait
that was present in an ancestor may be lost in some descendant
species, but then evolve anew in one or more of them.
The second problem with phenetics is that even for traits that
are inherited from a common ancestor, so-called homologous traits,
not all are equal. If you were an alien landing on earth and happened
across a dog, a baboon and a human, you might conclude that dogs
and baboons share a more recent common ancestor than do baboons
and humans. Dogs and baboons walk on all four legs and have very
hairy bodies, while humans lack these features. But, these features
that baboons and dogs share are primitive traits – walking on all four
legs evolved in the first vertebrates to walk on land and the presence
of hair evolved in the last common ancestor of all mammals.
As soon as you looked around a bit more, you’d notice that these
characteristics are present in nearly all living mammals. Dogs and
baboons share these features not because they are particularly clo-
sely related to one another but because their distant mammalian
ancestor had these features.

1
The word “phenetics” comes from the Greek root phainein, “to show.” It is the same
root used in the word “phenotype,” the observable features of an organism. (9. Tobin A,
Dusheck J. Asking about Life: Cengage Learning; 2004.)
 march of the bipeds: the early years 13

As you looked a bit further, you’d notice that baboons and

humans share multiple traits to the exclusion of dogs and many
other non-primate mammals. These traits include stereoscopic
vision, nails instead of claws, bony eye sockets, fewer teeth, and larger
brains. These characteristics shared by baboons and humans are
derived traits that were present in their most recent primate common
ancestor. Such shared derived traits would tell you that there is
a branch of the mammalian evolutionary tree that includes baboons
and humans but not dogs. Shared derived traits are the basis of
a second method of reconstructing phylogenies known as cladistics.2
Most paleoanthropologists prefer the cladistic method because it sepa-
rates primitive from derived traits (among other advantages).3
The product of a cladistic analysis is a cladogram – a diagram that
shows the branching sequence of a set of species from a hypothetical
common ancestor. Strictly speaking, cladistic analyses do not tell you
how species are linked to one another in ancestor-descendent lineages
and do not have a time dimension. In this way a cladogram differs from
other depictions of phylogenetic relationships. Among several and some-
times many possible cladograms that can be created from a set of trait
data, those that would necessitate the greatest number of homoplasies
are considered to be most improbable. The assumption is that
a cladogram requiring a large number of independent evolutionary
events to explain similarities among species is less likely than one
requiring fewer of them. The most parsimonious cladogram, requiring
the fewest homoplasies, is therefore preferred. The principle being
applied here is Occam’s Razor, that explanations requiring fewer
assumptions are more likely to be correct than those requiring more.
But, there are problems with cladistics and the parsimony
principle.4 Sometimes there are several equally parsimonious

2
The word “cladistics” comes from the Greek root clados, meaning “branch.” (9. Ibid.).
3
A third school, “evolutionary systematics,” constructs phylogenies on the basis of
branching sequences among species as well as on how much species have changed
since they shared a common ancestor.
4
A “maximum likelihood” approach can also be used in cladistic analysis. In this
statistical technique, a mathematical model of trait evolution is applied to a set of
14 march of the bipeds: the early years

cladograms. Furthermore, parsimonious solutions may not always be

correct ones. It is also sometimes difficult to determine the primitive
state for a characteristic. We know that walking on all fours is
a primitive state for mammals – this is obvious because the fossil
record reveals that four-legged vertebrates predate two-legged ones.
If we didn’t have the fossil record to help us here, we could look around
at a distantly related group – such as reptiles – to figure this out.
Walking on four legs is clearly a very old trait if it is shared with
reptiles. Distantly related groups, what are called outgroups, are
used in cladistics to determine the direction of evolutionary
change in a trait. But, using outgroups is tricky: whatever species
you choose has its own unique evolutionary history and therefore
may not always express the primitive condition. So, sometimes you
arrive at different answers depending on which species you choose as
an outgroup. With these problems, fragmentary remains for some
species, and an incomplete fossil record, it is no wonder hominin
species relationships are so vigorously debated.

the earliest hominins

Not surprisingly there is debate right from the start in determining
exactly which fossil species is the first hominin. From DNA evidence,
we know that our closest living relatives among modern primates are
chimpanzees and bonobos. The last common ancestor we shared with
them existed some 7–12 million years ago, according to a recent
estimate5 (10).
The anatomical similarities of humans to the African apes led
Charles Darwin to predict that the fossil hominins would be found on
the African continent. In 1924, a young woman named Josephine
Salmons, a student at the University of Witwatersrand in South
Africa, presented her anatomy professor Raymond Dart with the

species and their traits, and the phylogeny that best fits the data (the most likely one) is
produced. This is a newer method that is increasingly being incorporated into hominin
studies.
5
Previous estimates had suggested a more recent divergence, around 5–7 million
years ago.
 the earliest hominins 15

figure 1.1: Artist’s rendition of the Taung child. Drawn by Alyssa

Starrett.

fossilized skull of a monkey that miners had blasted out of limestone

(11). His interest piqued, Dart arranged to have additional fossils
brought to him. When he opened one box of fossils, Dart found the
remains of an endocast (cast of the interior of the cranium) together
with the skeleton of a face cemented to the rock. Dart reportedly used
his wife’s knitting needles to painstakingly remove the rock (breccia)
from the face of what is now known as the Taung Child (12)
(Figure 1.1).
From the base of the endocast, Dart could tell that during life the
child’s head was held on an erect spine. Clearly the creature was
bipedal, like humans today. Furthermore, the canine teeth were not
the large and pointed variety that the African apes sport; they were far
less impressive and similar in shape to those of modern humans. Yet,
partly because the Taung Child’s brain was small for a similarly-aged
modern human and partly because up until this point fossil hominins
had been found only in Europe and Asia, few of Dart’s contemporaries
believed he had found a human ancestor. Subsequent finds from South
Africa, as well as the famous Lucy skeleton from Ethiopia dated to
3.2 million years ago, made clear that of our derived human traits,
bipedalism arose first. Smaller, less pointed canine teeth than African
apes were also present in our early ancestors, but large brains were not.
16 march of the bipeds: the early years

Today there are three contenders for the title of the earliest
hominin, stretching back to 6–7 million years ago (Ma) in Africa.
They are Sahelanthropus tchadensis (from Chad, dated to 6–7 Ma),
Orrorin tugenensis (from Kenya, dated to 6 Ma) and Ardipithecus
kadabba (from Ethiopia, dated to 5.2–5.8 Ma (13). The first species of
hominin, evolving independently from the lineage that led to chim-
panzees, may not have been bipedal. Yet, it is bipedalism that
offers the clearest diagnostic clue as to the hominin status of a fossil
species. Most of the debate regarding the hominin status of these three
species therefore has to do with insufficient or ambiguous evidence of
bipedalism (14). The first of these species, Sahalanthropus tchadensis,
is a case in point: its skull was reconstructed from hundreds of pieces
(15), so that details of the cranial base diagnostic of bipedalism have
been disputed (16).
Still, the upper canine teeth of Sahelanthropus tchadensis are
relatively small compared to a chimpanzee’s and are worn at the tip as
are those of humans today (17). Ape upper canines by contrast wear on
the side facing the lower first premolar. Their projecting upper canines
sharpen against their conical single-cusped first premolar in a honing
complex (Figure 1.2). Honing creates wear on the back of the upper
canine and front of the lower premolar. Ape lower canines also project
beyond the tops of other teeth and are accommodated in the upper jaw
by a diastema (gap) between the upper canine and incisors. But smaller
canines with worn tips don’t save the day for Sahelanthropus because
some quadrupedal fossil ape canine teeth (probably those of females)
that came before it in the fossil record appear to have had similarly
sized canine teeth with similarly worn tips (16).
There is wider agreement that Ardipithecus ramidus (though
see [18]), dated to 4.4 million years ago and from the Middle Awash
area of Ethiopia (19), is a bona fide hominin. There are 109 specimens
of this species, representing at least 36 individuals, including
the individual represented by the famous Ardi skeleton. Standing 4
feet tall, Ardi had a pelvis with several key anatomical adaptations for
bipedalism, a small brain, and smaller canines than a chimpanzee’s.
 the earliest hominins 17

UC

LPI

figure 1.2: Chimpanzee skull highlighting UC (upper canine) and LP1

(lower first premolar). The distal edge of the UC hones, through jaw
movements, against the mesial side of the LP1. Drawn by Alyssa Starrett.
18 march of the bipeds: the early years

But, Ardipithecus’s mode of bipedalism was different from ours. Like

an ape’s foot, that of Ardi had a divergent big toe (Figure 1.3). Unlike
modern humans, then, Ardipithecus could not push off the ground
with its big toe while walking. Instead, Ardi seems to have propelled
itself forward by pushing with the middle portion of its foot. Ardi also
had longer arms (in relation to its legs) than modern humans do and
may have combined bipedalism with above-branch climbing and
clambering (19).
Whether Ardipithecus ramidus was a direct ancestor to modern
humans or a member of an extinct side branch is a difficult if not
impossible question to answer. After Ardipithecus ramidus appeared
on earth, many other hominin species evolved, all clearly bipedal. They
can be grouped into the genera Australopithecus, Paranthropus, and
Homo. What follows is by no means a full accounting, but an introduc-
tion to: the species relevant to Part I of this book, some of their more
salient dental attributes, and their possible phylogenetic relationships.

australopithecus
With the announcement of the Taung Child in 1925 in the journal
Nature, Raymond Dart christened a new species: Australopithecus
africanus. The literal translation of Australopithecus is “Southern
Ape,” reflecting Dart’s view that he had found “. . . an extinct race of
apes intermediate between living anthropoids and man.” (1925: 195).
The earliest representatives of this genus now known are from
East Africa. The first to appear on earth was Australopithecus ana-
mensis ranging in time from 4.2 to 3.8 million years ago, and repre-
sented by more than fifty dental, cranial, and postcranial specimens
(13). Like great apes, Australopithecus anamensis had a rectangular
dental arcade (Figure 1.4), canine teeth with large roots, lower first
premolars with only one cusp (or sometimes with an incipient second
cusp [20]), but a lower deciduous molar morphology (21) said to be
“intermediate” between that of Ar. ramidus and Australopithecus
afarensis.
figure 1.3: Ardipithecus ramidus foot. Redrawn by Alyssa Starrett
from Figure 1a in Lovejoy CO, Latimer B, Suwa G, Berhane A, White TD,
Combining prehension and propulsion: the foot of Ardipithecus ramidus.
Science. 2009;326:72e2. Reprinted with permission from AAAS.
20 march of the bipeds: the early years

figure 1.4: Artist’s rendition of the dental arcades of a chimpanzee (left),

Australopithecus afarensis (center) and a modern human (right). Drawn
by Alyssa Starrett.

Au. afarensis, first appearing in the fossil record around

3.7 million years ago (22) was the next Ethiopian hominin in time,
and likely evolved from Au. anamensis (23, 24). In 1974, Donald
Johanson and his team discovered the famous Lucy, the nearly com-
plete skeleton of an Australopithecus afarensis individual, whom
President Barack Obama had the pleasure of “meeting” during his
2015 visit to Ethiopia. Small-brained and bipedal, but with long
arms, Lucy stood about 3.5 feet tall, yet she was clearly an adult
when she died as her wisdom teeth had already erupted and begun to
wear. Since 1974, Australopithecus afarensis has become one of the
most well-known early hominin species, with hundreds of remains
from multiple sites along the East African Rift Valley (15). Like Ardi,
Lucy also had long arms, and may have spent time in the trees (15). But
with the big toe now in line with the other toes, Lucy’s kind could
“toe-off” while walking (15).
In Au. afarensis, as in Au. anamensis, the shape of the dental
arcade (Figure 1.4) is somewhat rectangular, more like that found in
Miocene and modern apes (although this is more true of Au. anamen-
sis than of Au. afarensis). Both species had projecting jaws with large
front teeth and nearly parallel-sided molar rows that created this
rectangular form. Both also had more thickly enameled teeth than
 australopithecus 21

Ardipithecus or its predecessors (15). Thick enamel is a derived feature

of later hominins (25) presumed to be an adaptation to eating harder or
more abrasive foods (see Chapter 2). In Au. anamensis, the upper
canine and lower first premolar are more apelike, but along the evol-
ving Au. anamensis-Au. afarensis lineage, these teeth became more
derived in the direction of later hominins (20). Also along this lineage,
molar teeth became larger (15).
Coexisting in East Africa with Australopithecus afarensis was
a species that seemed so unusual that its discoverers coined both
a new genus and species name for it: Kenyanthropus platyops (26).
Fossil spanning 3.5 to 3.0 million years ago include a single cranium.
The cranium has a much less projecting face than Au. afarensis: hence
the name “platyops” meaning “flat-face” (26). The single well pre-
served tooth of the upper jaw is a second molar that falls below the
known size range of Australopithecus afarensis second molars (26).
These features appear to make it more humanoid. Yet, the fossilized
face does not retain its original shape, as the over 1,000 tiny pieces of
the face are separated by matrix-filled cracks of varying sizes (27).
Given this distortion, paleoanthropologist Tim White (27) suggested
that K. platyops may simply be a variant of Au afarensis – though one
with smaller molars.
Two other middle Pliocene hominins should be noted. The first
is Australopithecus bahrelghazali (28), from Chad, dated to between 3
to 3.5 Ma, and represented by a single mandible fragment with some
teeth. The teeth have several similarities to those of Australopithecus
afarensis, but with a few differences (e.g., both premolars with three
separate roots). The second is the species Australopithecus deyire-
meda, from Ethiopia, dated to between 3.3 and 3.5 Ma, and repre-
sented by a partial maxilla (upper jaw), two mandibles (lower jaws)
and associated teeth (29). This species, announced in 2015 in the
journal Nature, has molars that are generally smaller than those of
Au. afarensis, but with different root structures. In a commentary
accompanying the Nature article (30), paleoanthropologist Fred
Spoor questions whether Au. deyiremeda and K. platyops are distinct
22 march of the bipeds: the early years

species, given their gnathic (jaw-related) and dental similarities

(including small first molar crowns).
It now also appears that stone tools may have made their first
appearance in the east African middle Pliocene (31), though the spe-
cies identity of their maker(s) is/are unknown. The evidence comes
from a 3.3 Ma-site in Lomekwi, West Turkana, Kenya and consists of
149 stone artifacts, including stone cores and flakes that appear to
have been struck from them.
Finally, late in the East African Pliocene is Australopithecus
garhi, a hominin dated to 2.5 Ma, from the Middle Awash of
Ethiopia (32). “Garhi” means “surprise” in the local Afar language,
and the fossil remains of this species were a surprise for two main
reasons. First, there are few Australopithecus remains from this time
period in East Africa (13). Second, the skeletal remains of this species
have a surprising combination of features, including premolar and
molar teeth as large as those of Paranthropus boisei, the most
“robust” of the robust australopiths (described below) and a humerus
to femur ratio that is derived in a modern human direction (32).
Shifting the scene to South Africa, Raymond Dart’s
Australopithecus africanus species made its appearance in the fossil
record a bit later in time, between 3 and 2 million years ago (13). Much
is known about Au. africanus today, as hundreds of fossils have been
recovered from South African limestone caves.
Relative to Australopithecus afarensis, Australopithecus afri-
canus had a slightly larger brain. In some ways, its teeth were more
derived in a human direction. In contrast to the more rectangular
shape of many Au. afarensis dental arcades, those of Au. africanus
more closely approach the parabolic dental arch seen in humans (13).
Diastemata (pl. diastema) or gaps in the upper and lower jaws for
accommodating canine teeth when the jaws are closed are present in
great apes. Diastemata were also often present in Au. afarensis, while
they were rarely present in Au. africanus (33). In Au. afarensis, upper
canines generally have wear at the tip but there is often also wear on
the side facing the lower first premolars, which are in some specimens
 paranthropus and early hominin phylogeny 23

(but not all) ape-like in bearing only a single cusp (34). Despite these
more ape-like features, the first lower premolar of Australopithecus
afarensis does not appear to have actually functioned as a whetstone
for the upper canine (35). In Au. africanus, however, canines wear
mainly at the tip and the lower first premolars are bicuspid (33), as
are the lower first premolars of humans today. Yet Au. africanus has
larger molars than both Au. afarensis (15) and early Homo (33) and in
this respect, Au. africanus appears to be derived in the direction of
species of Paranthropus, which had enormous molars.
Following closely on the (bipedal) heels of Australopithecus afri-
canus in South Africa is the recently discovered Australopithecus
sediba dated to 1.97 million years ago (36). Two partial skeletons and
other fossil fragments currently represent this species (36). Like other
Australopithecus species, it retained long arms with strong hands and
had wrists that would have enabled it to climb (37). Also like other
Australopithecus species, it had a small cranium. But, in some features
it seems more derived in the direction of humans than
Australopithecus africanus. These features include a more human-
like pelvis and smaller molars (36, 38).
Overall, then, species of the genus Australopithecus were small-
brained bipeds that retained climbing abilities and had canines and
lower first premolars that became more humanoid over time. That is
not the case for molars, which do not exhibit such a temporal trend,
with some later species having small, more human-like, molars (e.g.,
Au. sediba, and others having extremely large ones (e.g., Au. garhi).
That much seems clear. The more detailed picture of the phylogenetic
relationships among Australopithecus species, to our own genus
Homo, and to the genus Paranthropus is, however, not at all clear, as
the next section explores.

paranthropus and early hominin phylogeny

The genus Paranthropus includes three “robust” hominin species,
so-called because they have faces and crania with large bony attach-
ments for chewing muscles, bony buttresses for resisting large bite
24 march of the bipeds: the early years

forces, huge molars, and square premolars that are often called
“molarized.” South African paleontologist Robert Broom gave the
genus its name (39), announcing discovery of a Paranthropus robus-
tus skull in 1938 in Nature. “Paranthropus” literally means “beside
man.” Broom remarked on the human-like qualities of the skull’s
relatively flat face, broad and short palate, and diminutive canine
teeth. He also noted that its large premolars, which he estimated to
be twice the size of those of humans, were completely different from
those of other South African Australopithecus hominins found to
date. To Broom, the distinctiveness of these premolars justified
naming both a new genus and species. Paranthropus robustus is
estimated to date from 2.0–1.5 Ma (15).
Similar robust forms were later found in East Africa, the most
famous of which is “Nutcracker man,” discovered by Mary and Louis
Leakey at Olduvai Gorge in Tanzania in 1959 after they had spent
nearly thirty years searching for hominin remains (40). The sobriquet
seemed apt at the time given that this skull is robust in the extreme
and has huge back teeth (Figures 1.5 and 1.6). Nutcracker Man is
joined by many other similar finds from the East African Rift valley
dating from about 2.5 to 1.4 million years ago into the genus
Paranthropus boisei (15). Figure 1.6 illustrates a Paranthropus boisei
mandible (Peninj) beside that of the African Homo erectus specimen
WT 15000. The huge molars and premolars of Paranthropus boisei are
larger than those of any other hominin. These teeth have extremely
thick enamel on both their chewing surfaces and sides (41, 42).
Immediately preceding Paranthropus boisei in the East African fossil
record is the earliest of the robust species – Paranthropus aethiopicus –
dating from 2.7–2.5 million years ago (15). It differed from
Paranthropus boisei mainly in having more primitive characteristics,
such as a more projecting face and a smaller brain (15).
What do paleoanthropologists make of this plethora of early
hominin species, each with a unique combination of primitive and
derived traits? Most introductory paleoanthropology texts include
multiple possible phylogenies, outlining the arguments for and
 paranthropus and early hominin phylogeny 25

figure 1.5: Artist’s rendition of Nutcracker Man. The first skull of

Paranthropus boisei ever found. Drawn by Alyssa Starrett.

against them. Unfortunately, even cladistic analyses, which are cur-

rently the most objective and replicable methods for reconstructing
phylogenies, are not in strong agreement.
Consider four cladistic analyses that use different data sets,
though with some overlap among them. The first is an extensive
analysis published in 2004 by Strait and Grine (43) using 198 cranial
and dental characters. As in most cladistic analyses, in this study
traits were treated as having discrete states: traits are either absent
or present with different levels of expression. Figure 1.7a (redrawn
26 march of the bipeds: the early years

figure 1.6: On the left is the Peninj mandible, belonging to the species
Paranthropus boisei. On the right is the mandible of the Nariokotome Boy
(WT15000) of the species Homo erectus (or Homo ergaster).
The proportions of the two mandibles are to scale. Drawn by Alyssa
Starrett.

from their Figure 10) shows a consensus of their most parsimonious

cladograms. Note that many species branch off separately but that the
top half of the cladogram consists of two multispecies branches: one
that includes Paranthropus and Kenyanthropus and the other consist-
ing of Homo species.
Compare and contrast this figure with Figure 1.7b, a simplified
version (omitting the relationships among later Homo species) of the
2008 analysis of González-José and colleagues (44). These researchers
used a novel approach, measuring and treating cranial size and shape
variation as continuous. In so doing, they captured biological variation
more realistically than previous analyses that divided it into discrete
states of expression. Furthermore, these researchers performed their
cladistic analysis with respect to functional or developmental mod-
ules, instead of treating every trait as an independently evolving unit.
This is important because traits used in cladistics analyses are
assumed to be independent, each providing a unique piece of data
included in the analysis. In the resulting cladograms from this
(a) (b) sis us 5 us
en ic s 06 H an
is s sis s s ar op tu i-4 i O ric
ns du en si nu s s af thi bus ise ise af
de ami am aren rhi rica yop tus i icu s e o o us
s e iop es u a ro b b
a
h r n f a f t la ty ec s s s s ec is
tc s a s a s a s g s a pla obu ois eth
s u u u u u s sis r o nl lod pith opu opu opu opu pith bit
pu c c c c c u s s s
r b a
en te s g g r
lo h h h hr r r lo ha
ro ithe ithe ithe ithe ithe rop opu opu opu itis olf as en lla tro tra nt nt nt nt tra o
h b d g pi on n s ra ra ra ra s m
nt p p p p p th r r r ha ru er sa G Pa Au Pa Pa Pa Pa Au Ho
e la tralotralo tralo tralo tralo yan nth nth nth o o o o
Other Homo
h s s s s s n ra ra ra m m m m
Sa Au Au Au Au Au Ke Pa Pa Pa Ho Ho Ho Ho

(c) s (d)
us an is
sis ens sis da s
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lo ib ica an ns ad dus nam fare arh eyir fric ei iop stu tyo
tra o s ed a fr ar r ica
h
tc mi s a s a s g s d s a ois eth obu p la is
s
Ho
m s s h Af us ra cu cu cu cu cu s b a r s ns s
Au cu cu Sa op s e e e e e u us us pu lfe is tus en
lla n p us an t he t he u b- o r th hr ecu pith pith pith pith pith rop rop rop thro do abit rec pi
on r ica o i
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c
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an pith ralo ralo ralo alo ralo nth nth nth n
u
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a o
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o
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Pa Sa Ar Au Au Au Au Au P Pa Pa Ke Ho Ho Ho Ho
G Ea Pa Ea Au Au M M

figure 1.7: Phylogenetic relationships as redrawn by author from the following studies: (a) Strait and Grine (2004), (b) González-
José (2008), (c) Irish et al. (2014), and (d) Haile-Selassie et al. (2015). Figure 1.7b is adapted by permission from Macmillan
Publishers Ltd: Nature: González-José R, Escapa I, Neves WA, Cúneo R, Pucciarelli HM. Cladistic analysis of continuous
modularized traits provides phylogenetic signals in Homo evolution. Nature. 2008;453:775–778. Figure 1.7d is adapted by
permission from Macmillan Publishers Ltd: Nature: Haile-Selassie Y, Gibert L, Melillo SM, Ryan TM, Alene M, Deino A, et al.
New species from Ethiopia further expands Middle Pliocene hominin diversity. Nature. 2015;521:483–488.
28 march of the bipeds: the early years

approach (one derived from the method of maximum parsimony, the

other from the other of maximum likelihood), the closest species to
Homo is Australopithecus africanus. Figure 1.7b shows the cladogram
resulting from their maximum parsimony analysis.
Next, consider the maximum parsimony cladogram shown in
Figure 1.7c from 2013 and 2014 studies by Joel Irish, myself, and our
colleagues (45, 46), which included the recently discovered
Australopithecus sediba and used only dental traits, such as root
number and the number and degree of expression of cusps on premo-
lars and molars. We analyzed a particular set of dental traits whose
outward expression is known in living humans to be highly heritable
(i.e., variation in these traits is largely due to variation in genes rather
than environment [6]). We also tested for correlations among these
dental traits, using only those that were not strongly (statistically)
correlated with one another. In our strictly dental analysis,
Australopithecus africanus and Australopithecus sediba are the clo-
sest species to Homo, sharing several derived dental features. This was
true whether we used gorillas or chimpanzees as outgroups.
Lastly, with their 2015 announcement of Australopithecus
deyiremeda, Haile-Selassie and colleagues presented a consensus cla-
dogram (of seventeen equally parsimonious trees) shown in
Figure 1.7d. Their analysis included nineteen traits of teeth and jaws
of these species. The newly named Australopithecus deyiremeda
branches off just before Australopithecus africanus, which is then
followed by a multispecies Paranthropus clade, a clade including
Kenyanthropus platyops and Homo rudolfensis, and a clade contain-
ing the remaining Homo species.
These four studies, including one focusing specifically on crania
and one focusing exclusively on teeth, differ in many ways, but have
a few things in common. They all indicate that East African
Australopithecus species (not including Kenyanthropus) are more
distantly related to Homo than are South African Australopithecus
species. Those that include multiple species of Paranthropus also find
that these species are closely related to one another. The different
 paranthropus and early hominin phylogeny 29

approaches at least converge on these points. But, exactly which

species are most closely related to Homo varies in these studies, as
well as in many other studies not reviewed here. Beyond this incon-
sistency, it turns out that the dental and cranial traits commonly used
in paleoanthropological cladistics studies do not always give the same
answers about phylogenetic relationships among living species that
their DNA does (47)! Given these problems, we have some clues about
the origin of our genus, but do not yet (and may never) know exactly
where it came from. In the understated words of Ayala and Valentine
in the quote that heads this chapter, establishing “precise” lines of
descent for most organisms is “very difficult.”
This brief overview sets the stage for exploring the insights teeth
provide into early hominin evolution. These insights begin with what
teeth reveal about the evolution of hominin diets, a fundamental
adaptation affecting multiple facets of species biology and therefore
intertwined with all of the topics in Part I.
 2 Dentally-Derived Dietary
Inferences: The Australopiths

The diet of Paranthropus appears to have been primarily vegetarian, while

that of Australopithecus seems to have been omnivorous and to have
included a fair proportion of flesh.

– Robinson JT
Prehominid Dentition and Hominid Evolution

Australopiths were not likely to have gone on diets but they certainly
had them. Diets provide the energy and nutrients that enable survival
and reproduction. Natural selection favors those individuals who are
best at transforming their diets into surviving offspring, who will, in
turn pass on the genes that made them and their parents successful.
For this reason, diets fundamentally shape species’ biology, from how
they distribute themselves in relation to resources to the contours of
their molar cusps.
Because what a species eats is a keystone adaptation, scenarios of
human evolution often begin with changes in diet. In the 1950s, the
South African paleoanthropologist John T. Robinson (1923–2001), pre-
sented an argument about early human evolution (48, 49), now referred
to as the “Dietary Hypothesis.” According to Robinson, the cranial and
dental differences between South African hominins Paranthropus
robustus and Australopithecus africanus pointed to a major dietary
difference between them. Robinson reasoned that the large muscles of
mastication (as inferred from bony anatomy) and expanded molars of
Paranthropus robustus were adaptations to a tough vegetarian diet,
including roots and bulbs, that required a great deal of chewing. His
analysis of craniodental morphology in Australopithecus africanus,
however, led him to conclude that this species was the founder of
a new line of more omnivorous, tool-using hominins that could respond

30
 dentally-derived dietary inferences 31

more flexibly to changing environmental conditions. This is the line, he

argued, that eventually gave rise to us.
Raymond Dart’s ideas (50) about early human evolution were
likely to have influenced Robinson. Dart’s study of South African
cave sites led him to believe (incorrectly, it turned out [51]) that
hominin hunting was responsible for the animal bones accumu-
lated there. In his view, hunting transformed our peaceful ape-like
ancestors into intelligent, weapon-wielding, blood-thirsty preda-
tors. More recent ideas about the importance of meat in human
evolution de-emphasize the act of hunting as a prime mover of
human evolution, focusing instead on the nutritive benefits of
meat in facilitating human evolution. Humans and chimpanzees
do differ in their meat-eating habits. Per year, chimpanzees are
estimated to consume only 10% of the amount of meat that
African hunter-gatherers do (52), so, anthropologists’ seeming
obsession with meat as having to do with human origins makes
some sense.
Aiello and Wheeler’s (53) “Expensive Tissue Hypothesis” con-
tends that the incorporation of increasing quantities of meat and
decreasing quantities of plant foods over human evolutionary history
made the evolution of large brains possible. Because leafy plants,
which are rich in fiber, are difficult to digest, animals who specialize
in eating them have evolved complex stomachs and long intestines.
These digestive tissues are energetically expensive to maintain, and
any reduction in their size frees up energy for other purposes.
According this hypothesis, the increasing proportion of meat and
decreasing proportion of plants in the line that led to modern humans
relaxed the selective pressure to maintain large guts. Energy was now
available to sustain another energetically expensive organ: the brain.
This hypothesis has been questioned though, on the basis of a test
across 100 mammals (54) showing that brain size is not negatively
related to the size of the digestive tract – in other words there doesn’t
seem to be an energetic trade-off between the two, at least on this
large scale.
32 dentally-derived dietary inferences

Still other dietary hypotheses have de-emphasized the impor-

tance of meat in human evolution, focusing instead on gathered plant
foods (55, 56). The argument here is that plant foods comprise the bulk
of modern-hunter-gatherer diets. In addition, even though meat may
be an important dietary component (providing protein), it is not as
reliably acquired as are plant foods, which are more abundant and
evenly distributed in space and time. For these reasons, the impor-
tance of meat in human evolution has been doubted. World-renowned
primatologist and chimpanzee authority Richard Wrangham (and col-
leagues) (52, 57) propounded the view that it was cooking plant foods
that was the critical adaptation. Cooking released nutrients locked in
otherwise indigestible plant parts and improved the digestibility of
other parts, fueling the evolution of large brains in the genus Homo.
The kinds of plant parts Wrangham and colleagues had in mind were
underground storage organs (USOs): tubers and other root vegetables
that are staples of some modern African hunter-gatherer groups.
These ideas, however, get a little ahead of the present chapter.
This chapter focuses on the diets of the australopith species that
preceded and coexisted with the genus Homo, and from whose ranks
the genus evolved. Based on the study of teeth, what do we think we
know about the diets of the earliest australopiths? Do their diets
suggest a fundamental adaptive shift that differs from the diets of
modern chimpanzees and bonobos, our closest living relatives? How
different were the diets of Australopithecus africanus and
Paranthropus robustus and how much meat were these species likely
to have consumed? How variable (i.e., flexible) were australopith
diets? And, with such huge and thickly-enameled back teeth, did
Nutcracker Man really eat nuts or at least foods that were very hard?
These questions are explored in this chapter, the answers to which
differ depending upon which paleoanthropologists you talk to.
A case in point is the Viewpoints section of the July 2013 issue of
the American Journal of Physical Anthropology. In it is a debate from
two groups of paleoanthropologists, one led by David Strait from the
University at Albany SUNY (58) and the other by David Daegling from
 dentally-derived dietary inferences 33

figure 2.1: Skull of an Aye-Aye, a lemur of Madagascar that, like

rodents, has ever-growing incisors. Aye-Ayes consume a variety of food
types yet have a reduced number of teeth. Drawn by Alyssa Starrett.

the University of Florida (59). Both Davids were PhD students of

paleoanthropologist Fred Grine at Stony Brook University. Both of
them agree that australopiths were dietary generalists, in not being
limited to eating items within one or two specific food categories.
Primates, as a whole are dietary generalists. So, although robust aus-
tralopiths appear morphologically specialized in having large faces and
back teeth, it would seem unlikely that they were highly restricted in
their dietary proclivities. The most specialized primate, the aye-aye of
Madagascar, has rodent-like ever-growing incisors (unlike any other
primate), that it uses to gouge tree bark and expose grubs that it stabs
with its elongated bony middle finger. Despite these specializations and
the loss of permanent second incisors, canines, and most of its premo-
lars (Figure 2.1), the aye-aye nevertheless consumes several different
kinds of foods including seeds, nectar, fruits, and fungi (60).
On the other hand, the two Davids most definitely do not agree
about the role of hard foods in selecting for australopith craniodental
34 dentally-derived dietary inferences

morphology. Hard foods are those that are “stress-limited” in that

high forces are required to initiate cracks in them. Strait and his
colleagues contend that the consumption of hard foods (e.g., hard
nuts and seeds) can explain the masticatory adaptations of australo-
piths: enlarged chewing muscles provided the force necessary to frac-
ture hard foods while reinforced facial bone and thick enamel were
selectively advantageous in preventing fracture of bone and enamel,
respectively, under high force.
Daegling et al. point out that these features of australopiths do
not necessarily signal that australopiths were eating hard foods but
could result from other causes. For example, enlarged chewing mus-
cles and buttressing of the facial skeleton in australopiths could also
have resulted from selection for the repeated chewing necessary to
break down tough, fibrous plant foods. These are foods that fracture
when they are subject to high displacements (i.e., movements in
the direction of force). It doesn’t necessarily take a lot of force to
induce a crack in tough foods, but it does take a sustained force in
one direction – by tearing or slicing– to propagate the initial crack.
The disagreement over hard vs. tough foods stems from the kinds of
evidence the two different groups of paleoanthropologists believe
provide the most reliable evidence for reconstructing hominin diets.
There are two broad categories of fossil evidence. The first cate-
gory consists of morphological or structural features of fossil crania,
faces, and dentitions that are inferred adaptations to eating different
kinds of foods. Such inferences are usually based on associations
between these features and diet in living primates. For example, mod-
ern primates that frequently eat hard foods or eat them as “fallbacks”
when their preferred foods are unavailable (62), typically have low,
blunt cusps and thick enamel (63). Those that eat tough foods, such as
leaves, either frequently or as “fallbacks” (42), tend to have thinner
enamel (at least on their chewing surfaces) with taller cusps and
shearing crests (61). As the thin enamel of the cusp wears, it exposes
patches of softer dentine underneath. Because dentine wears away
more quickly than enamel, a sharp edge of enamel is maintained
 difficulties of dietary inference 35

along these dentine patches that can slice through tough foods (61).
The inferential reasoning is that if specific morphological features are
adaptations to specific dietary items, then fossils with these features
probably attest to the presence of these items in fossil species’ diets, at
least during their evolutionary histories if not in their actual lifetimes.
The limitations of such inferences are explored below.
The second category of evidence consists of physical and che-
mical traces of ingested food. This category includes such evidence as
chipped enamel, food particles trapped in dental calculus, microscopic
wear on chewing surfaces, and the chemical composition of enamel.
I will first review the strengths and weakness of these different kinds
of evidence. Then, I will explore the questions raised at the beginning
of this chapter emphasizing what arguably provides the most reliable
source of evidence coupled with the greatest number of insights – the
chemical signatures of food in tooth enamel.

difficulties of dietary inference from

anatomical features
While aspects of craniodental anatomy and morphology exhibit strong
correlations with dietary variation in primates, inferring the diets of
fossil species based on these correlations is complicated by several
factors. First, similar selection pressures may result in multiple solu-
tions. Although hard object feeding is associated with thick enamel in
primates (61), Lawrence Martin and colleagues (64) note that there is
a group of new world monkeys, the Pitheciini (Pitheciins), that feed on
fruit protected by hard husks but have thin molar enamel. These
monkeys use their robust and splayed canine teeth to puncture
through the hard husks of these fruit but use their molar teeth to
process the soft seeds inside. As these authors point out, their obser-
vations reveal that thick molar enamel is not always associated with
hard-object feeding. They suggest that the morphology of both ante-
rior and posterior dentition should therefore be considered when
inferring the diets of fossil species.
36 dentally-derived dietary inferences

Perhaps more problematic than the existence of multiple solu-

tions to similar adaptive problems is the situation in which different
selection pressures result in similar adaptations. A good example of
this problem is once again enamel thickness. Joanna Lambert and
colleagues (62) (2004) drew the attention of physical anthropologists
to the fact that grey-cheeked mangabeys from the Kibale Forest
Uganda, which have very thick enamel, do not subsist on hard
foods year-round. When soft fruits are available, they prefer to eat
those. It is only when their high-quality preferred soft fruit are
not available that they rely on hard seeds and bark. These authors
suggest that although seeds and bark are consumed infrequently, these
are critical “fallback” resources for grey-cheeked mangabeys. In these
authors’ view, natural selection favored thick enamel in grey-cheeked
mangabeys because it allowed them to make use of these resources
during “crunch” times, when high-calorie and easier-to-process fruits
were not available. Thus, there is a “mismatch” between grey-
cheeked mangabey enamel thickness and the soft fruits they prefer
and eat most frequently. This mismatch is often referred to as Liem’s
paradox, after Karel F. Liem who demonstrated (65) that cichlid fish of
the East African Rift valley lakes often have specialized jaws for
accessing specific food types but nevertheless are dietary generalists
in eating a wide variety of food items.
Fallback foods are generally considered to be low quality,
mechanically challenging foods (i.e., foods that are difficult to break
down physically) that animals resort to only when their preferred high
calorie and softer foods are unavailable. The association between fall-
back foods and specialized morphology has suggested to some that
fallback foods have had a primary role in selecting for specialized
dental adaptations. However, that this is not necessarily the case is
indicated by another mangabey, the sooty mangabey of the Tai Forest
in the Ivory Coast. Sooty mangabeys have very thick enamel, among
the thickest in the primate order. Analyzing two years of feeding data,
Ohio State University primatologist Scott McGraw and colleagues
 difficulties of dietary inference 37

(66) found that the hardest item in the sooty mangabey diet is
eaten year round.
The tale of the two mangabeys – grey-cheeked and sooty – tells us
that thick enamel can be an adaptation to hard foods that are eaten
either as fallbacks or as regularly consumed items. It also tells us that
“preferred” food items are not always soft. Furthermore, thick enamel
is not associated with only hard foods. Evolutionary anthropologist J.D.
Pampush and colleagues (67) analyzed the relationship between enamel
thickness and diet across seventeen primate species. They pointed out,
as have others before them, that thick enamel could be an adaptation to
abrasive particles in primate diets that come either from grit adhering to
their foods or from phytoliths. The latter, literally “plant stones,” are
formed when plants take up silica from the soil and deposit it in within
their cells. In the first portion of their analysis, Pampush and colleagues
found an association between hard food items in the diet and enamel
thickness, just as others had before them (61, 63). But, in the second
portion of their analysis they omitted the hard-object feeding species
and analyzed only the ten remaining species. In the remaining portion,
they found a relationship between enamel thickness and the interaction
between dietary abrasives (measured in terms of the phytolith content
of plants) and lifespan. It seems that species with longer lifespans,
whose teeth must function for longer time periods, and who have
abrasive diets tend to have thicker enamel on their chewing surfaces.1
Pampush and colleagues note that most mammals whose teeth
are subject to high wear from abrasion – for example, horses – have
evolved other solutions, such as hypsodonty, which appears in many
1
In their In vitro experiment at the nano level, Peter Lucas and colleagues suggest that
phytoliths do not actually remove enamel but instead simply scratch it. (68. Lucas PW,
Omar R, Al-Fadhalah K, Almusallam AS, Henry AG, Michael S, et al. Mechanisms and
causes of wear in tooth enamel: implications for hominin diets. Journal of the Royal
Society Interface. 2013;10(80):20120923.) If this is also the case in vivo, then an
adaptive association between enamel thickness and phytolith load in terms of wear
resistance becomes implausible. Yet, a more recent papers suggests otherwise – that
phyoliths can indeed remove enamel and cause tooth wear (69. Xia J, Zheng J, Huang D,
Tian ZR, Chen L, Zhou Z, et al. New model to explain tooth wear with implications for
microwear formation and diet reconstruction. Proceedings of the National Academy of
Sciences. 2015;112(34):10669–72.)
38 dentally-derived dietary inferences

occlusal
surface
mandible
reserve
crown

root

figure 2.2: Hypsodont dentition of a horse with mandible cut away to

show reserve crown and root. Drawn by Alyssa Starrett.

grazing mammals (70). Hypsodont teeth are tall with reserve crown
embedded within the jaw (see Figure 2.2). The reserve crown gradually
erupts at a rate that is about equal to the rate of wear. For unknown
reasons, hypsodonty did not evolve in primates, but thick enamel may
be an analogous adaptation to abrasive foods in some primates. So,
thick enamel in australopiths may be an adaptive response to hard
foods or to dietary abrasives and it would be difficult to tell simply on
the basis of the thickness of the enamel (although microstructural
details of enamel prism orientation might provide a way to discrimi-
nate between these two possible causes (71).
Finally, adaptations such as thick enamel tell you most clearly
about what animals ate in their evolutionary past that selected for
these adaptations. They do not provide evidence of what animals eat
currently. Translated into the fossil record, features of morphology
such as low relief on the chewing surfaces of teeth and thick enamel
tell you something about the kinds of foods the ancestors of these
fossil species ate. Morphological change may lag considerably behind
changes in diet. An example of such a time lag is found in fossil bovids
and suids from East Africa (72). Analysis of tooth enamel (see below for
 interpreting physical and chemical traces of diet 39

discussion of these methods) suggests that these lineages experienced

a rapid change in their diets around 2.8 million years ago, when they
began consuming large quantities of tropical grasses. Their rapid diet-
ary shift, however, is not matched by a rapid change in dental mor-
phology. Instead, the teeth of these lineages change very gradually
over the Plio-Pleistocene, becoming more hypsodont over time, pre-
sumably in response to their more abrasive diets.
Because of the issues associated with dietary inference from
anatomy, data derived from the physical and chemical traces left by
foods eaten during the lifetimes of the fossil individuals themselves
provide more direct evidence of diet, as explained next.

interpreting physical and chemical

traces of diet
For dietary inference in fossil hominins, three physical sources of
evidence have proven most informative. These are plant-specific and
plant-part-specific phytoliths trapped in dental calculus, distinctive
microscopic wear on chewing surfaces, and the size of chipped areas of
enamel on chewing surfaces. Each of these methods provides different
kinds of information and each has its limitations.
Dental calculus is calcified plaque, a slime (or biofilm) con-
taining thousands of bacteria that bathes your teeth. If you don’t
brush your teeth for a few days, a yellowish plaque can build up, and
if you don’t brush them for a couple of weeks of so, the plaque will
calcify, becoming dental calculus (which dental hygienists spend
a lot of time scraping off of teeth). Luckily for us, australopiths had
no dental hygienists, and it has so far been possible to analyze
phytoliths in dental calculus from one Australopithecus sediba
individual. Different plants and different plant-parts have differ-
ently shaped phytoliths, so it is possible to gain very specific infor-
mation about diet from identifying phytoliths. Unfortunately, the
presence of distinctive phytoliths in dental calculus cannot tell you
how frequently the items containing them were consumed.
40 dentally-derived dietary inferences

The analysis of dental microwear has a long history and has been
studied in multiple early hominin individuals of diverse species.
During the 1970s, several studies established associations in living
primates between microwear pitting and hard object eaters and
between microwear striations and leaf-eaters (70). Primates that
primarily eat soft fruit were found to have intermediate microwear
patterns (70). These studies involved scanning electron microscopy
at magnifications of 500x and painstaking identification of pits vs.
striations in micrographs. In addition to being time-consuming, this
method involved subjectively assessing whether microwear features
were pits or scratches, which in some cases was not so clear and can
vary with slight differences in the angle at which the electron beam
hits the tooth surface. Although microwear on enamel surfaces could
have been produced while fossils were lying in the ground for thou-
sands or millions of years, methods were developed in the 1980s to
distinguish such “artifacts” from true dental microwear associated
with chewing during life (73). The specific regions of enamel surfaces
studied microscopically are those involved in the crushing and grind-
ing of food trapped between molar cusps (74).
In more recent times, automated techniques have trans-
formed microwear studies, making it possible to quantify micro-
wear objectively (75). In “microwear texture analysis” the surface of
molar facets are scanned with a confocal imaging system to obtain
three dimensional images of the enamel surface. These images are
then analyzed using “scale-sensitive fractal analysis” to quantify
different characteristics, such as surface complexity and anisotropy
(76). The consumption of hard plant foods is associated with micro-
wear textures with high complexity values (owing to pitting) while
the consumption of tough plant foods is associated with high aniso-
tropy, meaning that there is strong directionality to the scratches.
Species such as brown capuchins who eat hard seeds have micro-
wear textures with high complexity and low anisotropy (77).
By contrast, species like howler monkeys who eat large quantities
 interpreting physical and chemical traces of diet 41

Alouatta palliata
Weer Facet 9

1.27 µm

139 µm 10 µm
102 µm

Cebus apella
Wear Facet 9

7.79 µm

139 µm 10 µm
102 µm

figure 2.3: Microwear textures of a howler monkey (Alouatta palliata)

and a capuchin monkey (Cebus apella). Notice the high directionality of
scratches on the howler monkey wear facet (high anisotropy) and the
uneven and pitted surface of the capuchin monkey wear facet (high
complexity). These images were kindly provided by Professor Robert
Scott, Rutgers University.

of leaves, have microwear textures with high anisotropy and low

complexity values (77) (Figure 2.3).
These important technical advances in microwear analysis, how-
ever, do not address other limitations of this approach. Experimental
studies have shown that microwear features have high rates of turnover
(78). Some features can be formed and then erased within twenty-four-
hour periods. Striations of average size observed in microwear studies
can be worn away less than one week after they have formed. So,
microwear observed on fossil teeth represents what was eaten in the
few days before death, in what is often called the “Last Supper” effect
(79). Given the likelihood of dietary variability owing to seasonal or
interannual food availability, microwear therefore gives us a limited
view into what individuals ate during their lifetimes.
42 dentally-derived dietary inferences

Another problem may have to do with what exactly produces

microwear. In 2013, physical anthropologist Peter Lucas and collea-
gues published in vitro experimental evidence that rocked the micro-
wear world (literally actually, because quartz was involved). These
researchers slid individual particles of quartz dust, phytoliths, and
enamel chips across flat enamel surfaces, but it was only the quartz
dust that was hard enough to actually remove enamel (68). Much
softer phytoliths and enamel chips formed nanowear in the form of
grooves or troughs in the enamel but did not cause enamel loss.
A question that remains unclear, however, is how well this experi-
ment corresponds to what actually happens during chewing in the
mouth and to microwear patterns above the nano level.
These researchers further suggest that pitted enamel surfaces
found in microwear studies are not likely to be caused by hard foods
which are softer than quartz dust or phytoliths. Instead, they argued,
quartz dust may cause this pitting, and although phytoliths may
create microgrooves in enamel, phytoliths themselves reveal nothing
about whether hard or tough foods were eaten. They point out that
there are several examples of living primates with very different diets
but similar microwear and that it is likely that such inconsistencies
reflect the fact that quartz dust and phytoliths have more to do with
microwear than do food particles themselves.
Microwear researchers countered that they had been misunder-
stood (59, 77), that they never contended that food particles them-
selves create microwear. Instead, they explained, it is the phytoliths or
other silica-based structures in plants that leave distinctive micro-
scopic marks on enamel chewing surfaces depending on the material
properties of foods (77). Hard plant parts require that upper and lower
molars are brought together in direct opposition in order to crush
them. As the molars press against one another, silica-containing par-
ticles are driven into the enamel creating pits in the enamel surface.
Tough plant parts require molars cusps to slide past each other in order
to tear them, creating directional striations on the enamel surface
where silica-containing particles are dragged across it.
 interpreting physical and chemical traces of diet 43

This explanation is reasonable and very likely explains why there

are associations between microwear textures and the toughness vs.
hardness of plant foods, as Rob Scott and colleagues showed in their
analysis of twenty-one anthropoid species (77). Yet, it does not rule out
the complicating factors of quartz dust or exogenous grit adhering to
foods as causes of microwear. David Daegling and Fred Grine (80) found
that grit adhering to plant underground storage organs (USOs), such as
tubers and corms, resulted in microwear pitting in chacma baboon
enamel similar to that of primates who eat hard foods. What all this
means is that microwear can be influenced by more than food proper-
ties and therefore can be a somewhat noisy dietary signal.
Recently, molar enamel chipping has emerged as a potential
source of information about hominin diets. John Robinson of the
“Dietary Hypothesis” noted chips in the molar enamel of
Paranthropus robustus and Australopithecus africanus (48). Because
the boundaries of these chipped areas were not sharp but were dulled
by subsequent wear, Robinson inferred that the chips had been created
during life. But, it is only in the last few years that meaningful infor-
mation has been extracted from enamel chips.
Paleoanthropologist Paul Constantino and colleagues (81)
showed by experiment that the sizes of chips along the edges of
molar crowns (more precisely, the scar left behind after a chip was
removed) are mathematically related to the force used to create them.
Essentially, large molar edge chips imply strong bite forces.
The presence of large chips with worn boundaries on the edges of
fossil molars may indicate that some kind of hard food, requiring
a strong bite force was chewed. Yet, a hard piece of gravel ingested
along with tough food that required a strong bite force could theoreti-
cally produce a similar enamel chip. What can be concluded for this
type of analysis, then, is that large molar enamel edge chips may signal
the consumption of hard foods that required high bite forces.
In support of the association between enamel chips and hard
foods, Constantino and colleagues (82) showed that within the great
apes, the highest frequencies of chipping are found in orangutans who
44 dentally-derived dietary inferences

are frequent consumers of hard seeds and nuts. But, frequencies of

enamel chipping are difficult to interpret because, as Daegling and
colleagues point out (59), they may be affected by the size of the molar
crown and the period of time a molar has been in use, both of which are
likely to affect the chances of chip formation.
In sum, the least controversial physical evidence of hominin
diets derives from the analysis of particles trapped in dental calculus.
Microwear and enamel chip analysis also provide useful information
but have some limitations that must be considered when interpreting
what these sources of evidence signal about hominin diets. Chemical
evidence of hominin diets, specifically the analysis of stable carbon
isotopes2 and trace elements locked within dental enamel, provide
a rich source of information that has yielded important insights into
hominin diets.
Chemical evidence rests on the principal that you are what you
eat (83). The analysis of stable carbon isotopes in tooth enamel reveals
whether certain types of plants were eaten during the period of tooth
formation. Plants using different enzymatic pathways during photo-
synthesis incorporate into their tissues different proportions of the
stable carbon isotope C-13 in relation to C-12, the most common form
of carbon. These differing proportions are incorporated into the tis-
sues, including the enamel, of animals that eat these plants (and the
animals that eat the animals that eat these plants). Enamel forms only
during a limited time frame: when teeth are developing during
infancy and childhood. Enamel is also the most mineralized tissue of
the body consisting of 96% mineral with the remaining 4% consisting
of water and some protein. With these attributes, enamel essentially
locks the ratio of ingested C-13 to C-12 into its dense mineral struc-
ture which can be preserved with minimal chemical alteration for
millions of years (83).
The different photosynthetic pathways are C3, C4, and CAM
(crassulacean acid metabolism) (84). Plants that use the C3 pathway

2
Stable isotopes are nonradioactive versions of atoms.
 interpreting physical and chemical traces of diet 45

initially incorporate carbon dioxide into a three-carbon molecule,

while those that use the C4 pathway initially incorporate carbon
dioxide into a four-carbon molecule (84). Both pathways discriminate
against C-13 in favor of C-12, but to a different extent, resulting in
their having different C-13 to C-12 ratios in their tissues.3 C3 plants
have less C-13 relative to C12 than do C4 plants. The majority of
plants use the C3 pathway. Trees, shrubs and bushes all use the C3
pathway but tropical grasses and sedges (e.g., papyrus) use the C4
pathway. Without going into great detail, the C4 pathway makes it
possible for plants to fix carbon dioxide quickly, and so minimizes the
time that stomata (pores in plants that allow gas exchange) are open.
With stomata open for shorter periods, the evaporation of water is
minimized. For this reasons, C4 plants, such as tropical grasses and
sedges, are believed to be well-adapted to the warm environments in
which they are found.
CAM plants are similar in their enzymatic pathway to C4 plants
(84), but they open stomata only at night, and are also adapted to dry
conditions. Such plants include succulents such as cacti and are found
primarily in desert or semidesert environments. Since living primates
rarely make use of CAM plants which are, in addition often toxic (84),
stable carbon isotope ratios in hominin tooth enamel are likely to
reflect only the proportions of C4 vs. C3 plants (or the animals that
eat them) in their diets.
The stable carbon isotope signal in enamel reflects the percen-
tage of C3 vs. C4 food sources eaten during the juvenile phase of
growth, when tooth formation is occurring. The dietary signal there-
fore reflects a longer span of time than does the signal from microwear.
It is even possible to gain insight into variability in the proportion of
C3 vs. C4 foods in the diet over the time span of enamel formation (see
below). Clearly, however, the information obtained is quite general –
C3 vs. C4 plants are broad categories. Furthermore, eating the animals

3
By convention, C13 composition is reported as percent per thousand as δ13C = [(13
C/12Csample)/(13C/12Cstandard) – 1] × 1000, where the international standard is the
Vienna Peedee Belemnite (VPDB).
46 dentally-derived dietary inferences

that eat plants from those categories (or some animal/plant combina-
tion) can produce similar signals.
Trace elements can, however, provide insight into animal vs.
plant matter in the diet. Mammalian digestive systems discriminate
against Barium (Ba) and Strontium (Sr) (trace elements) relative to
Calcium (Ca) (84). Thus, herbivores have higher levels of Ba and Sr
relative to Ca in their tissues than do the animals that eat them and so
on, up the food chain. It is possible to compare, for example, the Sr/Ca
composition of dental enamel in fossil teeth to that of modern herbi-
vores, and if it is similar, to deduce that the fossil tooth came from an
individual who ate a large quantity of plant matter during the period of
enamel formation.

what early hominins ate

The carbon isotope signal of our closest living relatives, the African
apes, reflects the predominantly forested environments they inhabit.
Chimpanzee and gorillas are said to have nearly “pure” C3 signatures
(85). Even where chimpanzees inhabit savanna woodlands, their
strong C3 signals are nearly unvarying, suggesting that chimpanzees
do not make use of C4 resources even when they are available. Yet,
modern humans do, and hominins such as Australopithecus africanus
and Paranthropus robustus did, incorporate substantial quantities of
C4 foods in their diets. Physical anthropologist Matt Sponheimer and
colleagues (86) suggested that the ability to make use of C4 foods
provided australopiths with critical dietary flexibility, allowing
them to survive in the more arid and open habitats that increasingly
characterized the African Plio-Pleistocene. If flexible diets that incor-
porated C4 plants represent a fundamental hominin shift, then how
early does this adaptation appear in the hominin fossil record?
Stable carbon isotope analysis on the tooth enamel of
Ardipithecus ramidus (19) from Aramis Ethiopia dated to 4.4 million
years ago suggests a diet focused on C3 plants. Most of the
Ardipithecus ramidus individuals from which enamel was sampled
had δ13C values that were slightly elevated relative to savanna-
 what early hominins ate 47

woodland chimpanzees, but were much less than the values of later
hominins (19). Such a diet is consistent with the reconstructed envir-
onment of Ardipithecus ramidus. The many kudu, colobine monkeys,
and other faunal as well as floral remains suggest a forest-woodland
environment, dominated by C3 plants. Savanna resources may have
been nearby, which may explain the slightly elevated δ13C levels
relative to savanna-woodland chimpanzees (87).
Two hundred thousand years later, between 4.2 and 4.0 million
years ago, Australopithecus anamensis from the Kenyan Turkana
Basin has δ13C values quite similar to that of Ardipithecus ramidus
(88), indicating that it too had a diet dominated by C3 resources (either
C3 plants or animals that ate them or some combination). That these
were likely to be C3 plants rather than animals that ate C3 plants is
likely because most of the contemporary herbivores in this region
were C4 plant consumers.
Like modern chimpanzees, both Ar. ramidus and Au anamensis
avoided C4 resources even though these resources were becoming
increasingly available in the Pliocene. The microwear of neither of
these hominins is characterized by the high complexity or pitting
associated with the consumption of hard foods or foods with exogen-
ous grit (89, 90). Despite these similarities, Au. anamensis had con-
siderably thicker molar enamel that did Ardipithecus ramidus (84).
Furthermore, Au. anamensis had enamel that was “decussating” in
having enamel prisms that cross one another. Decussating enamel is
thought to be an adaptation that stops cracks from propagating (91).
Opposite to the suid case discussed earlier, here there is no direct
chemical evidence of dietary change from one species to another
over time. Anatomical changes in tooth enamel have nevertheless
occurred.
A marked dietary shift toward the incorporation of significant
quantities of C4 based foods occurred by 3.5 million years ago in
Australopithecus bahrelghazali, Australopithecus afarensis, and
Kenyanthropus platyops. In the first of these, Au. bahrelghazali
from Chad, the teeth of three individuals were sampled, and these
48 dentally-derived dietary inferences

figure 2.4: Plant corm: an underground storage organ. Drawn by Alyssa

Starrett.

indicate diets composed of 55–80% C4 food sources (92).

Environmental indicators, such as the fossils of open-country grazing
bovids, attest to the likelihood that C4 plants were dominant in the
environment of Au. bahrelghazali. But whether they were eating C4
plants or animals that ate these plants or some combination is not
clear. Because the low-cusped and thickly enameled teeth of Au.
bahrelghazali do not seem well-adapted to slicing through grass
blades (nor do they appear well adapted to slicing through tough
meat), Julia Lee Thorp and colleagues (92) suggest that some of the
C4 plant resources that Au. bahrelghazali ate might include fleshy
tubers or corms (Figure 2.4). Or perhaps they ate rhizomes of the most
abundant C4 sedge plants surrounding Lake Chad today – papyrus.
The latter suggestion prompted Nathaniel J. Dominy to title his com-
mentary on this paper “Hominins living on the sedge” (93).
 dietary patterns in southern africa 49

In Australopithecus afarensis, there was wide variability in

δ13C levels in a sample of twenty Ethiopian specimens spanning the
time frame of 3.4 to 2.9 million years ago (94). Four of them had
low δ13C levels, comparable to those of chimpanzees, but the rest
had much higher levels, some indicating consumption of up to 50%
C4 plants. This variability likely reflects the diverse habitats that Au.
afarensis occupied, from more open grasslands to closed woodlands
(84) (Grine, 2012). Surprisingly, no temporal trends in C4 plant con-
sumption were detected over this time period. Dental microwear of
Au afarensis also indicates no change over time. Both Au afarensis
and its hypothesized predecessor, Au. anamensis, had microwear
with low complexity as well as low anisotropy, which microwear
expert Peter Ungar and colleagues (90) believe is consistent with
“milling” tough foods on relatively flat molars. Meanwhile, twenty-
one Kenyanthropus platyops specimens, from 3.4 to 3.0 million years
ago, show a level of variability along the C3-C4 spectrum equivalent
to that of Au. afarensis (95). Thus, by 3.5 million years ago, hominins
in different regions of east Africa had begun to incorporate levels of C4
based resources in their diets that are not seen in today’s African apes.
The question now becomes whether similar dietary shifts were afoot
in Pliocene southern Africa.

dietary patterns in southern africa:

australopithecus africanus, paranthropus
robustus, and australopithecus sediba
Environmental conditions appear to have changed considerably over
the periods in which Australopithecus africanus and Paranthropus
robustus roamed southern Africa. In the limestone caves of
Makapansgat South Africa, where the oldest (96) Australopithecus
africanus remains have been found, the mammalian fossil fauna
assemblage consists predominantly of browsing species (97).
Browsers tend to eat leaves and fruit from trees and shrubs, while
grazers mostly feed on grasses. The dominance of browsers as opposed
to grazers at Makapansgat suggests dense vegetation, although study
50 dentally-derived dietary inferences

of the full mammalian fossil community suggests a mosaic habitat

with bushland, riparian woodland, and grasslands (97, 98).
The presence of C4 grasses is also indicated by isotopic studies of
mammalian tooth enamel (99). The Sterkfontein cave site where
hundreds of Australopithecus africanus fossils have been recovered
appears to have also been a mosaic habitat, consisting of woodland,
bushland, riverine forest (100), and open savanna (101).
Like Australopithecus africanus, Paranthropus robustus seems
to have lived in a mosaic environment, but analysis of the mammalian
faunal community from the cave sites Swartkrans and Kromdrai (from
which a majority of the Paranthropus robustus specimens derive)
indicates a significant expansion of the grassland component (97).
Further analysis of stable carbon isotopes in the enamel of fossil
mammals from South African cave sites corroborates this finding
and suggests a major expansion of open, grassy environments around
1.7 million years ago, parallel to that occurring in East Africa at this
time (99). A shift in environments from Australopithecus africanus to
Paranthropus robustus is consistent with Robinson’s dietary hypoth-
esis if the latter, living in drier more open conditions, had to increas-
ingly rely on hard foods or tough roots and tubers (aka underground
storage organs) to find sufficient food.
Direct evidence from teeth, however, suggests differences as
well as similarities in the diets of Australopithecus africanus and
Paranthropus robustus. In 1986, using a scanning electron micro-
scope, microwear pioneer Fred Grine found a marked difference in
microwear between Au. africanus and Pa. robustus (79). The latter
exhibited a much higher frequency of pit features than the former.
Subsequent microwear texture analysis supported his analysis. Of all
the australopiths, Paranthropus robustus has the most complex
microwear textures. Daegling and colleagues (59) calculated means
and confidence intervals around complexity values of australopith
species reported in various studies. Only Paranthropus robustus had
confidence intervals around its mean that overlapped with those of the
habitually hard-object feeding sooty mangabeys of the Tai forest
 dietary patterns in southern africa 51

(Cercocebus atys). Although microwear may not distinguish species

of differing diets (see above), in this case a clear microwear complexity
difference between Paranthropus robustus and other australopiths
species is evident. Whether this difference indicates that
Paranthropus robustus consumed harder foods (at least for its
last suppers) and/or underground storage organs along with a lot of
grit, however, remains unclear. But relative to other hominins,
Paranthropus robustus has higher variation in complexity values,
suggesting dietary variability (90).
Despite these microwear differences, Australopithecus afri-
canus and Paranthropus robustus are alike in the stable carbon
isotope composition of their enamel. In both species, mean carbon
13 values are similar (84), suggesting diets composed of some
35–40% C4 resources (plants or the animals that ate those plants).
Teeth of Australopithecus africanus from Sterkfontein (102) of
Paranthropus robustus from Swartkrans (103) show high variabil-
ity in the δ13C composition of their enamel over the period of
tooth formation. They were clearly neither specialized grazers nor
browsers, but instead were flexible foragers, at times relying
almost exclusively on C4 resources, while at other times consum-
ing nearly entirely C3 resources. For Paranthropus robustus, in
a study to which I contributed data on enamel formation, such
wide dietary swings occurred over the course of less than two
years’ time (103). These data weaken the notion that the extinc-
tion of Paranthropus robustus can be attributed to dietary
rigidity.
Adding a wrinkle to this dietary picture of South African homi-
nins is Australopithecus sediba, at 1.9 million years ago. In 2012,
Amanda Henry and colleagues published data on the first-ever phyto-
liths extracted from the dental calculus of an early hominin. These
included phytoliths of shade and water-loving C3 grasses and sedges
and well as fruit, leaf, or wood/bark phytoliths. The carbon isotope
composition of the teeth of both Au. sediba individuals (MH1 and
MH2) is unusual for hominins in this time period – it is similar to that
52 dentally-derived dietary inferences

of giraffes, who are C3 specialists, and to that of savanna chimpanzees.

Like the much older East African Ardipithecus ramidus and
Australopithecus anamensis, Australopithecus sediba seems to
have consumed C3 foods even though C4 foods were available.
It will be interesting to see if these findings are replicated in additional
Australopithecus sediba finds.
Returning to Australopithecus africanus and Paranthropus
robustus, in Robinson’s view, the absence of meat in the diet of
Paranthropus robustus was the critical component. His point was
that Australopithecus africanus and Homo became omnivorous
while Paranthropus robustus remained stubbornly vegetarian, lead-
ing to its demise. Data on Sr/Ca and Ba/Ca ratios help to address this
question. Unexpectedly, initial studies on bone yielded low Sr/Ca
ratios in Paranthropus robustus (104) similar to those of carnivores.
Yet, as mentioned, fossilized bone is highly susceptible to chemical
alteration, while the enamel of fossilized teeth is much more stable.
Accordingly, Matt Sponheimer and colleagues (105) analyzed Sr/Ca
ratios in the enamel of Australopithecus africanus, Paranthropus
robustus, as well as of modern and fossilized mammalian teeth.
They found that both hominin species had higher Sr/Ca ratios than
contemporaneous baboons or browsing mammals. Given these
results, there is no support for either of these species having consumed
more meat than do today’s baboons.
More recently, Balter and colleagues (106) measured both Sr/Ca
and Ba/Ca ratios in the teeth of Australopithecus africanus,
Paranthropus robustus and early South African Homo. For early
Homo, both ratios were indistinguishable from those of carnivores
while for Paranthropus robustus, both ratios were similar to those of
browsing mammals. Australopithecus africanus had values that
spanned a wide range, indicating a more complex diet. Variation in
the Sr/Ca and Ba/Ca ratios over the course of enamel formation was
also much higher in Australopithecus africanus than it was in
Paranthropus robustus or in early Homo. These findings are quite
consistent with Robinson’s contention that Australopithecus
 did nutcracker man chew nuts or eschew them? 53

africanus included more meat in its diet than did Paranthropus robus-
tus, the latter of which it seems was more focused on plant foods.
From the broader omnivorous diets of Australopithecus africanus,
then, came the more narrow diets of the later species Paranthropus
robustus and early Homo, who appeared to have gone in different
directions with respect to meat vs. plant eating. This is similar to
what was happening in East Africa with Paranthropus boisei and
Homo habilis, except that the diet of Paranthropus boisei, aka
“Nutcracker man,” was quite different from that of its robust South
African cousin.

did nutcracker man chew nuts or eschew them?

“Nutcracker man” has a slightly better ring to it than “C4-resources-
man,” but C4 resources are what Paranthropus boisei predominantly
ate. Somewhere between 75–80% of the Paranthropus boisei diet
consisted of these resources (95). Based on a sample of twenty-two
Paranthropus boisei individuals (a large sample for these kinds of
studies), Thure Cerling and colleagues (95) argued that Paranthropus
boisei was eating a large amount of the C4 grasses and sedges them-
selves, rather than the animals that ate those plants, because to accu-
mulate such high δ13C in enamel by only eating animals,
Paranthropus boisei would have had to have consumed an unrealisti-
cally large amount of animal food. Grasses and sedges don’t produce
nuts. (There are such plants called nutsedges, but the “nuts” are
actually underground tubers, not true nuts.)
It seems that the percentage of C4 grasses and sedges in the
Paranthropus boisei diet was comparable to that of a zebra or warthog
(59). As Julia Lee-Thorp noted (107), such high dependence on C4
resources in monkeys and apes is not seen today. The percentage of
C4 foods in the Paranthropus boisei diet even exceeds that of
the extinct gelada baboon Theropithecus oswaldi, a presumed grass
and/or grass-seed eater. Furthermore the δ13C values indicate little
variability in C4 consumption among the twenty-two individuals
54 dentally-derived dietary inferences

sampled. With such apparent dietary mono-focus, Paranthropus boi-

sei has been labelled a “C4 specialist” (83).
These isotopic findings square nicely with the microwear data
on Paranthropus boisei. Alan Walker first noticed an absence of pits in
the microwear of Paranthropus boisei, yet for many years it was
simply assumed that Paranthropus boisei must have eaten hard
foods (84). Fred Grine points out (84) that the reason for this assump-
tion is that his 1986 study of Paranthropus robustus revealed heavily
pitted microwear, indicating the consumption of hard foods.
By anatomical analogy to Paranthropus robustus, it made sense to
consider Paranthropus boisei a hard-object feeder, though no Pa. boi-
sei teeth had yet been sampled.
Then, in 2008 Peter Ungar and colleagues (108) conducted
a microwear texture analysis on a sample of Paranthropus boisei
teeth. Surprisingly, the teeth had very low complexity and anisotropy:
in other words the surfaces were nearly featureless. There is no evi-
dence for hard food eating here, yet there is also no evidence for leaf
eating. Aside from Jell-o™ (not a likely dietary candidate), featureless
microwear could have been produced by milling grasses and/or sedges
between opposing teeth. Dental anthropologist Gabrielle Macho
notes that the flatly worn and polished surfaces of Paranthropus boisei
premolars and molars attest to repetitive chewing of tough, abrasive
foods which, by analogy with baboons, she thinks may have been
corms. Reliance on C4 plants is consistent with the paleoenviron-
ments in which Paranthropus boisei remains have been recovered.
These range from riverine forests and woodlands to grasslands, but
include an increasing number of drier grassland habitats
over time (84).
The repetitive chewing of such C4 plant parts may explain Pa.
boisei’s perplexing combination of a C4 diet consisting of tough foods,
and teeth with low, blunt cusps that are conspicuously unadapted to
shearing such foods. With low and blunt molar cusps, Paranthropus
boisei would have had to engage in repeated chewing to break down
these tough foods. In line with the “tough foods” idea, analysis of Pa.
 did nutcracker man chew nuts or eschew them? 55

boisei’s temporomandibular joint indicates that its mandible moved

transversely (109), as it would have if its teeth were used in repetitive
chewing of tough foods. Yet, there is a problem with the idea that
these tough foods were primarily corms. The outer surfaces of corms
are usually gritty with particles of quartz – these would tend to pro-
duce pitted microwear that Paranthropus boisei simply doesn’t show.
Nathanial Dominy (93) suggests that Pa. boisei could have peeled the
corms before eating them, removing most of the grit. Or, as
Sponheimer and colleagues suggest (83), perhaps Paranthropus boisei
concentrated on the kinds of C4 plants that the gelada baboons
include in their diets – grass blades and grass seeds, which do not
leave much microwear pitting on gelada baboon teeth (77).
If Paranthropus boisei was a C4 specialist, then this raises the
question of whether its diet was too narrow to allow it to flexibly
respond to the vacillating environmental conditions of the Plio-
Pleistocene. In living primate species, specialized diets appear to
increase the risk of extinction (110). It might seem tempting then, to
blame Paranthropus boisei’s extinction on dietary inflexibility. But if
Paranthropus boisei was so limited in adaptability, it seems difficult
to understand how it persisted in East Africa during a period of widely
fluctuating environmental conditions for over 1 million years. That is
800,000 years longer than anatomically modern humans have mana-
ged to exist so far. By analogy with baboon dietary ecology, Gabrielle
Macho estimates that Paranthropus boisei could have met 80% of its
caloric requirements and all of its protein requirements just by spend-
ing about 40% of its feeding time on C4 resources (111). Life on the
“sedge” does not appear to have been life on the edge.
At several locations, Paranthropus boisei appears to have lived
near seasonally wet areas where C4 sedges and grasses flourished
(112). These areas provide a home to huge numbers of microorganisms
and tiny crustaceans, that Kathlyn Stewart believes Paranthropus
boisei would likely have eaten as well. Furthermore, Paranthropus
boisei teeth, like those of several other australopiths, exhibit large
edge chips suggesting at least the occasional presence of hard foods in
56 dentally-derived dietary inferences

the diet (81), so there was probably more to Paranthropus boisei diets
than sedges and grasses. Given that even the most dentally specialized
primate today – the aye-aye – eats a variety of foods with very few
teeth, it seems plausible that Paranthropus boisei, with its complete
set of very large teeth, did the same.

conclusions
Here, I have emphasized the difficulties involved of drawing conclu-
sions about the diets of fossil species based on known links between
dental morphology and diet in extant primates. The causes of these
difficulties are several. Morphological change may be gradual and lag
considerably behind dietary change, as is the case of the bovids and
suids of East Africa who began eating more C4 foods 2.8 million years
ago, but whose teeth became more hypsodont only gradually over the
Plio-Pleistocene.
In addition, there may be different adaptive solutions to similar
problems. Indeed, Matt Sponheimer and colleagues found that the
increasing consumption of C4 resources from Australopithecus ana-
mensis to Australopithecus afarensis to Paranthropus boisei is asso-
ciated with a trend to larger and larger premolars and molars over
time, most likely for processing these tough foods (83). It is not clear
why the consumption of these foods did not select for the thin enamel
and sharp cusps with shearing crests present in today’s primates who
eat tough foods. Thick enamel may have provided a selective benefit
in maintaining tooth longevity, as Pampush and colleagues (67) sug-
gest is the case for the longer-lived extant primates that subsist on
tough, phytolith-containing abrasive plant foods. Consistent with this
idea, it has been noted that in some nonprimate herbivores, the chew-
ing surfaces of teeth are flat despite their tough food diets – a different
solution from that of modern primates (67). In addition, of course, it is
entirely possible that thick enamel and large posterior teeth evolved in
response to eating hard foods as fallback resources. Unfortunately,
this possibility is not easily tested.
 conclusions 57

Matt Sponheimer and colleagues (85) consider the incorpora-

tion of C4 resources into australopith diets to reflect a “fundamental
hominin trait” that enabled hominins to adapt to the increasingly
open and grassier environments in which they lived. Chimpanzees
living in savanna environments today spend the majority of their
feeding time on fruits, giving them their strong C3 dietary signal (85).
Judging from their predominantly C3 signals, the early east African
hominins Ardipithecus ramidus and Australopithecus anamensis
were probably like chimpanzees in this regard. Beginning with
Australopithecus afarensis in east Africa, hominins began adapting
to changing resource availability, making use of C4 resources in
a way that modern savanna chimpanzees do not. In the case of
Paranthropus boisei, with its highly elevated C4 signal, it is likely
that sedges and grasses themselves were predominantly eaten, rather
than the animals that ate those plants. But as Kathlyn Stewart sug-
gests (112), tiny freshwater shrimp and copepods living in seasonal
C4 wetland environments could easily have been consumed along
with these plants.
Meanwhile, in southern Africa, Australopithecus africanus and
Paranthropus robustus incorporated sizeable percentages of C4
resources in their diets, though not nearly at Paranthropus boisei
levels. One source of South African australopith C4 resources could
certainly have been tropical grasses and sedges themselves, although
it is possible that animals that ate these resources also contributed to
their C4 signals. Termites have been suggested as one potential ani-
mal food Paranthropus robustus may have consumed. Microscopic
wear on experimental bone tools used to poke into termite mounds
matches the wear on bone tools recovered from Swartkrans cave
where Paranthropus robustus remains have been found (113).
Chimpanzees are well known to use tools in “termite fishing.”
Some termite species consume C3 plants, while others consume C4
plants, so it is possible that termites could have contributed to C3 or
C4 signatures, or both (114). Oddly, Australopithecus sediba main-
tained a C3-rich diet despite wide availability of C4 resources.
58 dentally-derived dietary inferences

The analysis of this species dental calculus nevertheless attests to

diverse foods in its diet, including fruits, leaves, grasses, and even
bark.
Australopiths were therefore flexible foragers. In terms of meat
consumption, Australopithecus africanus appears to have had the
most variable diet of the South African australopiths. Appearing
later in time, Paranthropus robustus and early South African Homo,
seem to have survived drier conditions by taking divergent adaptive
paths, Paranthropus becoming more herbivorous and Homo including
more meat in its diet. This situation points to evolutionary niche
divergence, which results when members of coexisting species are
able to access more food if they avoid competing with one another
over the same resources. As explored further in Chapter 6, Homo in
East Africa also seems to have included more meat in its diet than did
its contemporary robust cousin, Paranthropus boisei. Proffered in
1954, John Robinson’s Dietary Hypothesis continues to gain empirical
support today. But, before turning to what teeth tell us about the diets
of early and later Homo, the next chapter considers whether the
uniquely reduced canines of hominins are related to their diets, mat-
ing habits, or both.
3 Curious Canines

He who rejects with scorn the belief that the shape of his own canines, and
their occasional great development in other men, are due to our early
progenitors having been provided with these formidable weapons, will
probably reveal by sneering the line of his descent. For though he no longer
intends, nor has the power, to use these teeth as weapons, he will uncon-
sciously retract his “snarling muscles”. . . so as to expose them ready for
action, like a dog prepared to fight.

– Darwin CR
The Descent of Man and Selection in Relation to Sex, Vol. 1

Charles Darwin’s analysis of the size and shape of human canine

teeth convinced him that at some point, human male ancestors
possessed large and projecting canines, similar to those of male
gorillas or orangutans. In Darwin’s view, male canine teeth, like
other male armaments such as horns in mammals or spurs in birds,
were the result of sexual selection: the advantage that members of
the same sex have over one another in “exclusive relation to
reproduction.”
Darwin conceived of sexual selection happening in two ways:
first, through competition among males for mating opportunities with
females, and second through differences among males in their ability
to attract females. These two sides of the sexual selection coin are
called intrasexual and intersexual selection, respectively. In the first
case competition occurs among males and in the second, females
select males who they find most attractive (or on the basis of other
traits that would presumably enhance the survival of their offspring).
Thus ensues the evolution of armaments, like the large curved horns
of male bighorn sheep, and ornaments, like the peacock’s tail. Slashing
canine teeth, in Darwin’s view, were a male armament which evolved
through time because males with larger and sharper teeth were able to

59
60 curious canines

win more contests for females and thus pass these traits to their
offspring.
Darwin unfortunately did not have a satisfactory answer for
why there is a general pattern in nature of male-male competition
for mates and female choice of them, but later work (116, 117) offered
an explanation in terms of sex differences in investment in offspring.
In mammals, it is usually females that make an enormous investment
in offspring through gestation and lactation. Males, who by compar-
ison invest much less, compete with one another for access to females.
The pattern of male-male competition and female choice has been
attributed more fundamentally to anisogamy—the difference in size
of eggs and sperm. Males whose individual sperm cells are “cheap” in
comparison to the much larger egg cells of females, can maximize
offspring number by increasing the number of females with which
they mate, while females maximize their reproductive success by
“ensuring” the quality of their offspring through being choosy about
their mating partners.1
While Darwin believed that our remote ancestors must have had
intimidating canine teeth, he also believed that once our ancestors
began to walk bipedally, males could have used their free hands to
throw stones or to wield “clubs or other weapons.” Assuming that
males won more fights in this way rather than by using their slashing
canines, selection for maintaining large canines would be relaxed.

1
As evolutionary anthropologist Michael Plavcan and colleagues point out, sexual
dimorphism should not be assumed to result from selection acting only on male traits.
(118. Plavcan JM, van Schaik CP, Kappeler PM. Competition, coalitions and canine size
in primates. Journal of Human Evolution. 1995;28(3):245–276.) A tendency to make
that assumption arises from Darwin’s conception of competition among males as the
cause of intrasexual selection and female choice of mates as the mechanism of inter-
sexual selection. In both cases, male traits – armaments and ornaments – are being
selected. To be sure this is the general pattern in nature that Darwin observed, later
understood to result from the generally greater investment in offspring made by
females. In primates it is now clear that there are situations in which females compete
with other females, potentially resulting in intrasexual selection among them, as well
as situations in which males may be choosy about mating partners, potentially result-
ing in intersexual selection for female traits (119. Dixson AF. Primate Sexuality:
Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings, 2nd ed.
Oxford: Oxford University Press, 2012.)
 curious canines 61

Darwin explained that like other anatomical structures which are no

longer of use to animal, canines would, over generations, diminish in
size (owing, most likely, to selection for energy economy).
In ruminants, Darwin reasoned, canine teeth are either absent or are
vestigial because horns took over their function as weapons; so too did
human canine teeth reduce in size as males could now use their hands
to deploy weapons. Darwin did not explain why canine teeth did not
become vestigial or disappear altogether. Yet, he saw human canines
as “perfectly efficient instruments for mastication” (1871:126). He
might therefore have envisioned that no longer under selection as
weapons, canines could have been maintained by selection for their
contribution to food processing, as some anthropologists would later
propose.
Darwin’s view of canine evolution in humans ties together
defining human features – bipedalism, tool-making, and small
canine teeth – in a tidy evolutionary scenario. Indeed, to Darwin,
one of the key selective benefits of bipedalism was that it freed the
hands for other uses, including making tools and weapons.
As many have noted, evidence of stone tools in the fossil record
postdates the evolution of bipedalism, casting some doubt on this
explanation. But of course, it remains possible that early hominins
could have begun to use unmodified stones or wooden clubs to
a greater extent than chimpanzees do today. Such objects would
be difficult to recognize in the archaeological record as tools in the
first instance, and in the second instance, would be unlikely to be
preserved over millions of years.
Nevertheless, if Ardipithecus ramidus is ancestral to later
hominins (19), then the link between small canines and bipedalism
breaks down. Analysis of this species’ skeleton suggests facultative
bipedalism – Ardi had the ability to walk on two legs when necessary
but still spent a significant portion of time spent in the trees as an
arboreal quadruped. Yet, the canines of Ardipithecus ramidus are
considerably smaller than those of modern chimpanzee, gorilla, or
orangutan males (Figure 3.1).
figure 3.1: Comparison of upper canine teeth of Ardipithecus ramidus
and Pan troglodytes (chimpanzee) males. Redrawn by Alyssa Starrett from
the Author Summary figure in Lovejoy CO., Reexamining human origins
in light of Ardipithecus ramidus. Science. 2009;326:74. Reprinted with
permission from AAAS.
 curious canines 63

Paleoanthropologist and Ardipithecus-discoverer Tim White

(19) described canines from twenty-one Ardipithecus ramidus indivi-
duals. These canines are all similar in size and shape to those of female
apes and derived in the direction of those of later hominins. The upper
canines and lower first premolars do not show signs of functioning as
a “honing complex”: sharpened edges on the upper canine are not
present and there are no wear facets on the lower first premolar.
There is minimal variation in the size and shape of these canines,
and, assuming that some of the twenty-one individuals were males,
this limited variation suggests little difference in the canines of males
and females. Finally, Ardipithecus ramidus maxillary canines were
shorter than their mandibular canines, while in chimpanzee, gorilla
and orangutan males, maxillary canines are longer, reflecting their use
as weapons. This canine sample provides evidence that in
Ardipithecus ramidus, substantial changes in canine teeth toward
the modern human condition preceded the evolution of either the
more habitual bipedalism of later australopiths or the obligate (com-
mitted) bipedalism of Homo erectus and later Homo.
In 1925, when South African anatomist Raymond Dart intro-
duced the name Australopithecus to the world, he considered one of
its defining human-like features to be its small canine teeth. If the
connection between bipedalism and canine reduction envisioned by
Darwin breaks down with Ardipithecus ramidus, then what explains
the curiously small canine teeth of hominins, including modern
humans? Although many different ideas have been proposed, they
primarily fall into two classes of explanation. The first suggests that
the selection pressure maintaining large canines would diminish if
males were no longer competing for mates as much as their ancestors
did. The second suggests that changes in diet may have brought about
hominin canine size reduction.
These classes of explanation are not mutually exclusive, but
there is substantial debate as to which of them had more influence
and at what point during human evolution they may have come into
play. For example, if one can rule out changes in diet as a factor leading
64 curious canines

to the initial reduction of canines, then does this suggest that there
was comparatively little physical competition among early hominin
males, or even a monogamous mating system (120)? On the other
hand, if dietary changes are primarily responsible for the initial reduc-
tion in canine size, then the presence of small canines in hominins
implies little if anything about their mating habits.
Hominin canines are distinctive not only in their small size
relative to those of most other primates but also with respect to
their minimal sexual dimorphism – differences between the sexes
other than those related to the sex organs themselves. In the case of
canines, sexual dimorphism refers to the differences between the
sexes in the size and shape of these teeth. It is possible to have large
and projecting canine teeth with minimal sexual dimorphism, as
occurs in gibbons. In gibbon species, monogamously paired males
and females defend their territories. With both males and females
engaged in territorial defense, selection has presumably favored
enlarged canines in both sexes. So, for humans and earlier hominins,
the question is: why are canine teeth small and nonprojecting as well
as minimally sexually dimorphic?
Here I will first explain that given available evidence,
a reasonable case can be made for relating diminution in canine size
and sexual dimorphism to reduced competition among males for
mates in Ardipithecus ramidus, as White and colleagues (19) and
Lovejoy and coworkers (121) contend. Reduced male-male competi-
tion, however, does not necessarily imply monogamous social organi-
zation or mating. I will then argue that in some later hominins species,
even though evidence of skeletal sexual dimorphism may suggest
more intense mate competition (or female choice for large males),
the incorporation of canines into food processing functions and/or
changes in jaw architecture would have acted to constrain the evolu-
tion of canine size and sexual dimorphism. This argument relies
entirely on Leonard Greenfield’s analysis of canine function in early
hominins and Peter Lucas’ (122, 123) and William Hylander’s (124)
 ultimate and proximate causes of canine 65

biomechanical analysis of canine size and jaw gape in nonhuman

primates.
But first, to explore the contribution of sexual selection and diet
to canine size and sexual dimorphism in hominins, it is necessary to
examine what we know about the causes of canine variation in living
primates and about how canine size and shape changed over primate
evolutionary history.

ultimate and proximate causes of canine

variation in modern primates
Causes of canine variation in modern primates can be sought at “prox-
imate” and “ultimate” levels. Evolutionary causes and influences
constitute an ultimate level of explanation in biology, while genetic,
developmental, and physiological causes constitute proximate expla-
nations (125). The primary focus here is on ultimate causes of canine
variation in modern primates. Yet, elucidating proximate causes are of
interest as well because they may illuminate evolutionary events. For
example, if different developmental mechanisms are associated with
a shared feature among species, then it is likely that this feature
evolved in these species independently and therefore constitutes
homoplasy. Shared developmental mechanisms may suggest common
evolutionary origins or the lack of alternative developmental path-
ways for the evolution of an anatomical feature.
Insight into both categories of causes can be gleaned by examin-
ing patterns and correlates of canine size and sexual dimorphism in
living primates. First, taxonomic patterns are clearly evident.
In prosimians, upper (maxillary) canines are generally similar in size
for males and females (118). Where there are differences, male canines
are larger than those of females, with some exceptions (e.g., the dia-
demed sifaka whose canines are larger in females than they are in
males). In some prosimians upper canines may be somewhat large
and projecting (e.g., in ring-tailed lemurs), yet they do not reach the
size – either absolutely or in relation to their body sizes – of those of
some anthropoids (118). Similarly, sexual dimorphism in body size in
66 curious canines

prosimians is limited (119). In anthropoids, and especially in some Old

World monkeys, males have maxillary canines that are up to four
times larger than those of females (126–128) and are very tall in rela-
tion to their other dimensions. Body size dimorphism reaches an
extreme in Old World monkeys as well.
In great apes, neither canine nor body size sexual dimorphism
reaches such extremes, with male maxillary canines approaching
twice the size of that of females (gorillas and orangutans), and with
similar differences in body size (128). The proportions of great ape
canine teeth are different from those of Old World monkeys in being
wider and thus appearing stouter than those of older world mon-
keys (128).
From the standpoint of human and hominin canine size and
sexual dimorphism, it is interesting that in great apes, our closest
primate relatives, canine dimorphism size and shape does not
approach the extremes seen in some old world monkeys. And, as
anthropologist Michael Plavcan points out (128), in bonobos and
common chimpanzees, to whom we are most closely related, canine
size in both sexes as well as canine sexual dimorphism are rather
modest by anthropoid standards. Relative to body size, bonobo male
canines even appear to be “reduced” to a degree comparable to
Australopithecus afarensis male canines (129). Bonobos are no more
closely related to hominins than are chimpanzees, so either reduction
occurred in parallel in hominins and bonobos or the ancestors of the
hominin-chimpanzee-bonobo clade had modest canines to begin with,
and these evolved to larger size in chimpanzees.
A second pattern in primates is that sexual dimorphism in both
canine and body size is related to body size (130–133). The relationship
between sexual dimorphism and body size extends beyond primates to
a wide array of animals, and is known as Rensch’s rule (134). Exactly
why sexual dimorphism should be more pronounced in larger-bodied
species is debated (128), but Rensch’s rule suggests that it may be
useful to compare the degree of sexual dimorphism among species in
a way that takes into account their differences in body size.
 ultimate and proximate causes of canine 67

In anthropoids, not only is sexual dimorphism in canine size

correlated with body size, but so is absolute canine size itself (131,
135). Canine size dimorphism is also correlated with body size
dimorphism (132, 136–138). Yet, it is important not to overstate
these relationships because canine size and body size as well as
dimorphism in the two can clearly be dissociated. For example, in
living humans, there is greater body size dimorphism than canine size
dimorphism (139). The opposite is true of most colobine monkeys, in
which high sexual dimorphism in canines is coupled with minimal
sexual dimorphism in body mass (128). Selection pressures can there-
fore act independently on canine size and body size and on sexual
dimorphism in both.
Just as Darwin anticipated, a sizeable portion of the variation in
primate canine sexual dimorphism and male canine size relates to
male-male competition for mates. Observation of primates makes it
clear that males in some species inflict slashing wounds with their
canines on their competitors and may use them in threat displays
(119). (Not all canine exposure appears to relate to threat displays,
however [140].) Females too can inflict harmful wounds with their
canines in some species (141).
Early studies found ambiguous associations between canine
sexual dimorphism and intrasexual selection because they relied on
social organization as a proxy for male competition. For example,
Harvey and colleagues (131) proposed that in monogamous primate
species, where each male has a mate, there should be minimal com-
petition among males and canines should be least dimorphic. They
argued that species that form “harem” or single-male polygynous
groups (one adult male, several adult females and their offspring)
would have the greatest degree of sexual dimorphism because in
these species, bachelor males would frequently challenge “harem”
leaders for access to their females, and “harem” leaders would in
turn be required to defend them. Finally, multimale groups (several
adult males and females and their offspring) were expected to exhibit
68 curious canines

intermediate levels of canine dimorphism, because, in such groups

males cannot maintain exclusive access to females.
These early investigations did find that monogamous species
had the least sexually dimorphic canines, but there was no statisti-
cally significant difference in canine dimorphism between single-
male and multimale groups, lending only partial support to the
hypothesis that the degree of male-male competition in primate
groups is related to canine sexual dimorphism. Harvey and colleagues
(131) also found that terrestrial species had greater canine sexual
dimorphism than arboreal species, supporting the notion that selec-
tion has also acted on males as protectors of their groups against
predators in open environments. (Tree-living species can more easily
hide.)
What was needed to adequately test the intrasexual selection
hypothesis was a more accurate measure of male-male competition.
To see why social organization is not a reliable proxy for male-male
competition, consider baboons and woolly spider monkeys, both of
which form multimale groups. Baboons form multimale groups in
which males vigorously compete for dominance rank year-round and
are highly sexually dimorphic in both canine and body size. Woolly
spider monkeys have a much more relaxed mating system, in which
many males mate with many females (142) and canine sexual
dimorphism is minimal. In the latter case, competition has gone
“underground” in the form of sperm competition—male woolly spider
monkeys have very large testes in relation to their body sizes (143) as
do other species in which females mate with multiple males during
their peri-ovulatory periods (119).
Owing to such problems with using social organization as
a proxy for male-male competition, Richard Kay and colleagues (144)
devised a four-point rating scale to investigate the relationship
between degree of male-male competition and canine sexual dimorph-
ism, and in so doing found an unambiguous positive association
between the two. Building and expanding on this analysis, Plavcan
and van Schaik (138) created a rating scheme reflecting both the
 ultimate and proximate causes of canine 69

frequency and intensity of male-male competition and applied it to

a wide range of primates. These authors too found a clear relationship
between male-male competition and canine sexual dimorphism (and
later with body mass sexual dimorphism [139]). The relationship held
within substrate type (arboreal vs. terrestrial), taxonomic groups and
dietary categories (e.g., folivore vs. frugivore vs. insectivore and their
combinations), meaning that when “controlling for” these other fac-
tors, male-male competition is independently associated with canine
sexual dimorphism.
A recent study further demonstrated that male canine size is not
simply a reflection of male body size (145): males of sexually
dimorphic species with large body sizes had larger canine sizes than
expected on the basis of scaling their canines to their body sizes.
Selection therefore appears to be acting specifically on male canine
size. Consistent with this conclusion is an innovative study by Steve
Leigh and colleagues showing that male mandrills sired most of their
offspring during the period of maximum canine height – after the
canine was fully erupted and before the canine began to wear. Adult
male mandrills join groups of adult females and their offspring only
during the mating season, when they must establish dominance and
relationships to females in a limited period of time. Thus, sexual
selection is thought to be intense in this species, which exhibits
extreme sexual dimorphism in body and canine size as well as colora-
tion (119) (Figure 3.2).
An important point to keep in mind, though, is that variation in
female canine size is associated with the degree of competition among
females (usually for food and other resources) (118). This means that
canine sexual dimorphism should be viewed as a result of selection
acting not only on males but also on females, as Michael Plavcan often
emphasizes. The fact that gibbons have large canines but minimal
sexual dimorphism reflects selection on both sexes for large canines in
intra sexual competition. Plavcan and colleagues (118) found reduced
female canine size in species in which females compete in coalitions,
as in macaques, baboons, and mandrills. This finding suggests that
figure 3.2: The dentitions of a mandrill male (top) vs. that of a female
(bottom) showing strong sexual dimorphism in upper canines. Drawn by
Alyssa Starrett.
 ultimate and proximate causes of canine 71

part of the reason why canine sexual dimorphism is so great in these

species may be not only because selection is acting to increase male
canine size but also because there is minimal selection for large
canines in females.
Although much of the variation in canine size and canine sexual
dimorphism in anthropoids (monkeys and apes) relates to sexual
selection (146), there is evidence for relationships to diet as well. For
example, in marmosets, lower canines are small and are used, in
conjunction with lower incisors, to gouge tree bark in obtaining
gums. In the pithecine New World monkeys (a subfamily including
saki monkeys and uakaris), both upper and lower canines are used to
crack open hard fruit. Both males and females have tall canines with
a “chisel-like” morphology that appears to be adapted for this specific
use (147, 148).
Leonard Greenfield (149, 150) suggested that in primates, pri-
mary (deciduous) canines and the canines of females are often incor-
porated into incisal functions. He further argued (150), in his “dual
selection hypothesis,” that primate canines are under competing
selection pressures for use as incisors in acquiring food and for use as
sexually-selected weapons. Much of the evidence for these ideas came
from Greenfield’s observation that female canines often had blunted
tips as compared to male canines. Greenfield argued that blunted wear
in the lower canine is produced by contact with the upper lateral
incisor. Blunted wear in the upper canine, he explained, is produced
by tip-to-tip occlusion (contact) with the lower canine as well as by the
functional use of the upper canine in puncture-crushing.
Plavcan and Kelley (151) questioned whether tip-to-tip occlusion
could actually occur, given the ways in which jaws typically move
during chewing. They also countered that “incidental contact” with
food during food gathering may be an alternative explanation of such
blunted wear and that it is not necessarily indicative of “tip-to-tip”
occlusion between upper and lower canines, functional use of upper
canines in “puncture-crushing,” or functional contact between the
lower canine and upper lateral incisor. These points are important to
72 curious canines

bear in mind, yet they do not negate the possibility that the higher
frequency of blunted canine tip wear in primate females that Greenfield
found (150) reflects the functional use of canines in food acquisition.
Diet may also have an indirect role in constraining the evolution
of canines as weapons. This idea has its roots in the work of Peter
Lucas and colleagues (122, 123), who showed that the size of primate
males’ canines appears to be related to their gape. The use of tall
canines to inflict a wound requires that the jaw be opened widely.
These authors found that the length of the mandible and the height of
the jaw joint relative to jaw length – variables that affect gape – were
strongly related to canine size in male primates. This finding sug-
gested that the size of male canines may be limited by their gapes.
William Hylander and coworkers (124) actually measured gape
in living subjects and showed, across twenty-seven species of Old
World monkeys and apes, that jaw gape is closely linked to canine
crown height. Going a step further, these authors made the point that
evolutionary adaptation to diet can affect gape. A forward shift in the
position of jaw muscles makes it possible to increase bite force with-
out adding muscle mass because this is a position of greater mechan-
ical advantage for the jaw muscle lever system. Thus, an energetically
efficient solution to chewing hard and/or tough foods that require high
bite force is to shift the chewing muscles forward, but this has the
effect of decreasing gape. Thus, in species that solve the problem of
chewing hard or tough foods by shifting the chewing muscles forward,
the evolution of the canine is constrained by the reduction in gape.
Research into proximate causes of canine size and sexual
dimorphism has thus far focused primarily on the Y-chromosome,
testosterone and the developmental processes that lead to sex differ-
ences in male versus female canine crown height. The work of
Alvesalo and Verrela suggests that forty-six X,Y females with andro-
gen insensitivity syndrome have teeth as large as those of males (152).
This syndrome is characterized by lack of receptors for androgens
(including testosterone) indicating that independent of testosterone,
there are genes on the Y chromosome affecting tooth size. On the
 ultimate and proximate causes of canine 73

other hand, of all tooth types, canines were least affected in size in
forty-seven, XYY males (153), suggesting that the additional
Y chromosome had a disproportionately smaller effect on the canine
than on other tooth types.
Other evidence suggests a direct influence of testosterone on
canine size. Prenatal administration of testosterone propionate (an
injectable form of testosterone) to female rhesus macaque fetuses
resulted in taller canines than were present in control females
(154). More recently, Ribeiro and colleagues (155) measured
dimensions of deciduous and permanent canine teeth of human
opposite-sex dizygotic (fraternal) twins and same-sex dizygotic
twins. They hypothesized that females in opposite-twin pairs
would have larger canine teeth if testosterone from the male
twin had an influence on the female twin’s canine development
in utero. Their results supported their hypothesis, suggesting that
testosterone in utero affects the size of both deciduous and per-
manent canines. In opposite-sex twins, the female twin’s canine
eruption timing is also “masculinized” in the sense that canine
eruption occurs later in childhood than is normal for females,
approaching the time when male canines normally erupt (156).
In humans, boys erupt their canines approximately one year later
than females do, in part because their canine teeth take longer to
form.
The longer development of canine teeth in males relative to
females is even more pronounced in primates with strong sexual
dimorphism than it is in humans. For example, on average male
orangutan lower canine crowns take approximately three years longer
to form than do those of females (157). My colleagues and I showed
that in both Old and New World monkeys, the primary mechanism by
which males achieve their greater canine crown heights is through
prolonging their periods of crown formation, rather than by increasing
their speeds of crown formation (158). The common ontogenetic path-
way of anthropoid primates suggests that the alternative pathway of
speeding up crown formation in males was, for some other reason, not
74 curious canines

favored within this group of primates. It appears, however that the 50-
million-year-old Eocene primate Cantius (not an anthropoid), did
achieve canine sexual dimorphism by speeding up crown formation
in males, rather than by extending the period of male canine crown
formation (159).
The ultimate and proximate influences on variation in canine
size and sexual dimorphism in living primates reviewed in this section
provide important context for evaluating hypotheses about the evolu-
tion of hominin canines. Yet, these hypotheses must also be evaluated
with respect to the fossil evidence, which we turn to next.

the evolutionary transition to hominin canines:

fossil evidence
Sexual dimorphism of the Eocene primate Cantius dates to more than
50 million years ago, yet because the developmental pathway by
which Cantius grew large male canines was by speeding up growth,
its canine sexual dimorphism probably evolved independently from
that of anthropoids. Canine sexual dimorphism is also present in early
anthropoids (Catopithecus and Proteopithecus) in the fossil record of
Egypt, dating to 36 million years ago. These early anthropoids had
small bodies (less than the size of a guinea pig), yet they had pro-
nounced canine sexual dimorphism in apparent defiance of Rensch’s
rule.
But it is the fossil apes of the Miocene that are the immediate
predecessors of hominins and living apes, and are therefore more likely
to provide insight into hominin canine evolution. Many of the fossil
apes of the Miocene (of which there were a great many species) exhib-
ited canine sexual dimorphism in both size and shape (160). One of
them, Lufengpithecus from China may, have even been more sexually
dimorphic than any of the living apes (161). From which of these
Miocene apes the African ape and human clade descended is not clear.
Cladistic analysis suggests it may be the “Greek Ape,Ouranopithecus
macedoniensis,” dating to 9.6 to 8.7 million years ago. Synapomorphies
linking Ouranopithecus to this clade include in part its facial
 the evolutionary transition to hominin canines 75

morphology (162) and several dental traits: minimally sexually

dimorphic canines (though this has been questioned, as explained
below), the lack of a honing facet on the lower premolar (163), and
molarized deciduous premolars (164).
Miocene ape expert David Begun and coauthors (164) contend
that reduction in canine size, change in the upper canine-lower pre-
molar honing complex, and postcanine megadontia characterize
Ouranopithecus and some other Miocene apes including
Sivapithecus and Gigantopithecus (though these two Asian genera
exhibit affinities to Asian great apes). The authors suggest that these
are interrelated characteristics consistent with selection for powerful
chewing and so could represent homoplasy in these Miocene genera as
well as in the hominin Paranthropus. The co-occurrence of these
characteristics would be consistent with Hylander and colleagues
(124) explanation of the trade off between canine size and gape that
would accompany a forward shift in jaw musculature. The presence of
these features in Ouranopithecus raises the possibility that the com-
mon ancestor of the African-ape human clade had relatively small
canines that were inherited by early hominins, with larger canines
subsequently evolving in the chimpanzee and gorilla lineages. This
idea is challenged by other analyses suggesting that the canines of
Ouranopithecus were not so small relative to their estimated body
sizes and may have been rather sexually dimorphic after all (129).
If Ouranopithecus had sexually dimorphic canines comparable
to those of great apes of similar body size (129), then in addition to
weakening the possibility that early hominins inherited their small
canines from Ouranopithecus, the association between large back
teeth and relatively small, minimally dimorphic canines breaks
down. Incidentally, sooty mangabeys habitually eat very hard nuts
and have enlarged premolars and molars, but they also maintain
a wide gape (165) and quite sexually dimorphic canines. Clearly eating
mechanically challenging foods doesn’t necessitate small canines,
a point which Hylander and colleagues (124) make when they note
that the forward movement of jaw muscles is only one solution to
76 curious canines

apex
apex

figure 3.3: Lingual (tongue-side) view of Australopithecus anamensis

canine on left, and Australopithecus afarensis canine on right. Note that
in Australopithecus afarensis, the shoulders of the canine (marked by
asterisks) are closer to the apex of the crown. The Australopithecus
afarensis canine is therefore said to be more “diamond-shaped.” After
Ward CV, Plavcan JM, Manthi FK. Anterior dental evolution in the
Australopithecus anamensis–afarensis lineage. Philosophical
Transactions of the Royal Society B: Biological Sciences. 2010;365:
3333–3344 by permission of the Royal Society. Drawn by Alyssa Starrett.

a mechanically challenging diet. Another solution would be enlarging

the muscles themselves with no change in position.
The very strong evidence of reduced canines and minimal
canine sexual dimorphism in Ardipithecus ramidus was reviewed
earlier. Ardipithecus, however, retained a canine with large roots
(similar to those of chimpanzees) and had a crown shape that was
similar to that of its presumed descendent Australopithecus anamen-
sis. In the Australopithecus anamensis-Australopithecus afarensis
lineage, there were further changes in canine size and shape. In their
analyses, Carol Ward and colleagues (166) and Fredrick Manthi (167)
and coworkers showed that although there was no reduction in crown
height along this lineage, there were shape changes in upper canines,
lower canines and lower first premolars. The upper canine crown
became more diamond-shaped as the “shoulders” of the crown shifted
toward the crown apex (Figure 3.3), the lower canine crown became
less “blade-like,” and the lower premolars “less unicuspid.” Modern
 hypotheses for hominin canine reduction 77

humans have canine teeth with a similar diamond shape, although

they are of smaller size (166, 167). In addition, there was a strong
reduction in the size of the canine root with the transition to
Au. afarensis, a change that is also in a modern-human direction.
The canine crown shape changes, according to Ward and collea-
gues (166) would increase the area of contact between upper and lower
teeth and are therefore the likely result of selection for the increased
use of the canine in acquiring food (i.e., functioning like an incisor)
and also perhaps for an expanded role of the lower first premolar in
mastication. The authors further suggest that changes in jaw structure
as well as in molar crowns (which become taller) denote dietary
changes that would have affected premolar use.

hypotheses for hominin canine reduction

It is not yet possible (and may never be) to conduct definitive tests of
the various hypotheses for hominin canine reduction. It is possible to
evaluate some of the strengths and weaknesses of these hypotheses in
light of what we know about canine variation in living primates and
fossil hominins. Darwin’s ideas about the link between canine reduc-
tion and bipedalism are questionable based on what we know from the
fossil record today. But, the idea that hominin canine reduction is
related to changes in sexual selection pressures remains
a plausible one.
In an influential 1981 Science article entitled “The Origin of
Man,” Owen Lovejoy (120) proposed a complex scenario for the evolu-
tion of distinctively hominin traits. Ecological changes during the
Miocene (greater seasonality and variability) combined with long per-
iods of infant dependency were suggested to have intensified selection
for adaptations that increased both offspring survival and adult repro-
ductive rate. These adaptations included bipedalism and monogamy.
Bipedal males who could use their free hands to “provision” their
families would, in so doing, enhance the survival of their offspring as
well as hasten the return of their lactating mates to reproductive
condition. This situation could only evolve under the condition of
78 curious canines

monogamously mated females – males who provisioned the offspring

of other males would simply not pass on the genes that predisposed
them to provisioning behavior. Males would also be selected to mate
monogamously because by doing so they would devote their energies
to the survival of their own offspring rather than to competition with
other males. Monogamous mating would then result in relaxed selec-
tion pressure on maintaining large male canines, as intermale compe-
tition diminished.
In a footnote (120), Lovejoy pointed out that he did not mean to
imply that monogamy was the “cause” of canine reduction, but that it
simply relaxed selection pressure on canines, which then evolved to
smaller size by positive selection “. . . most likely to be found in the
concurrent dentognathic changes of greater molar dominance and
general anterior tooth reduction” in hominins (1981:350).
Lovejoy’s scenario raises the possibility that the reduced canines
and minimal canine sexual dimorphism of the earliest hominins is
a signal of monogamous mating. The reason that this is not necessa-
rily so, is that there is no clear link between mating system and canine
size or sexual dimorphism in living primates (see above). Michael
Plavcan explains that even his competition level categories that
have been linked to canine sexual dimorphism in living primates
account for only 48% of the variation in canine sexual dimorphism
in 128 species. Some of that variation also has to do with selection on
female canine size as well as on selection for dietary uses of canines in
some species. Thus, small male canines and reduced canine sexual
dimorphism are in and of themselves ambiguous evidence of a low
level of male-male competition in fossil forms.
In the case of Ardipithecus ramidus, however, there is evidence
of minimal canine sexual dimorphism and reduced canine size rela-
tive to great apes coupled with minimal skeletal sexual dimorphism
(19, 121). The combination of both skeletal and canine sexual
dimorphism strengthens the possibility that there was relaxed sexual
selection for large male canines in Ardipithecus. It does not appear
that Ardipithecus ramidus was eating mechanically challenging foods
 hypotheses for hominin canine reduction 79

to the same extent as Australopithecus afarensis and later hominins

were – it was not incorporating C4 plants to the extent that these later
hominins did, and it had not yet evolved the enlarged molars of these
species, nor had it evolved enamel as thick as that of later australo-
piths (see Chapter 2). For these reasons, it would be difficult to support
the view that canine reduction in Ardipithecus and reduced canine
sexual dimorphism was in some way a consequence of adaptation to
mechanically challenging diets (either through reduced gape or by
some other connection).
But what about other possible explanations for canine reduction
in Ardipithecus ramidus as well as in later hominins? Several other
ideas have been proposed, although many early ideas appear less plau-
sible today. One older idea was that large interlocking canine teeth
might interfere with “rotary” chewing of mechanically challenging
foods (169). But as Jungers (170) pointed out years ago, male baboons,
which have very large canine teeth, are quite capable of rotary and
lateral chewing movements. Experimental studies on male anthro-
poids with extracted canines showed that there was no change in
molar occlusal relationships following extraction of the large canine
(171, 172). Canine reduction in Ardipithecus ramidus, in any case,
occurred prior to the incorporation of significant quantities of C4
foods that may have been milled between upper and lower molars.
Another influential idea was that of developmental dental
crowding (170). This idea held that molarized premolars in early
hominins limited the space available to later-erupting canine teeth,
thus limiting their size. This idea has difficulty accounting for the
reduced canines of Ardipithecus ramidus, which did not have molar-
ized premolars. Yet one more idea was that canine reduction might
have simply been a by-product of incisor tooth reduction in hominins
(i.e., genes affecting incisor reduction simultaneously affected canine
reduction). While this is possible for Ardipithecus, which had smaller
incisors than modern chimpanzees, it is difficult to see why this
would necessarily be so because there are living primates with rela-
tively small incisor teeth (leaf-eating colobines) that nevertheless
80 curious canines

have very large canines. Lucas Delezene (173) recently showed that
across anthropoid primates, there is no evidence that canine tooth size
covaries with incisor tooth size (or with postcanine tooth size either).
Against the backdrop of these earlier ideas, Leonard Greenfield
(150) applied his “dual selection” hypothesis to hominin canine reduc-
tion. At the time of Greenfield’s writing, the earliest hominin canines
known were those of Australopithecus afarensis. Greenfield argued
that Australopithecus afarensis canines exhibited “incisor-like
traits” and were therefore probably under selection to function as
incisors. For example, the lower canines had enlarged “mesial cris-
tids” or ridges which would have contacted the lateral incisors when
the incisors were used to bite, and on some of Au. afarensis specimens,
the mesial cristids and points of contact with the lateral incisors were
worn. Not all showed such wear, indicating to Greenfield that the
mandibular canines were not yet functioning as fully as incisors as
they would be in later hominins and modern humans.
Plavcan and Kelley (151), in questioning various aspects of the
dual selection hypothesis, did not argue against the possibility that
these changes reflected a change in canine function, but rather dis-
puted that this change was the cause of canine reduction. The recent
analysis of changes in canine size and shape from Ardipithecus rami-
dus to Au. anamensis to Au. afarensis reveal an initial reduction in
upper canine size that remained constant from Ardipithecus ramidus
to Au. anamensis to Au. afarensis. Both upper and lower canines
only changed shape, toward the derived human condition with more
incisor-like traits, after this initial reduction (167).
Thus, a good case can be made that with Ardipithecus ramidus,
canine reduction and minimal canine sexual dimorphism may have
had less to do with changes in diet and more to do with diminished
male/male competition and/or with female choice of males with
smaller canines. Yet, because of the tenuous links between canine
sexual dimorphism and mating systems, it would a leap to conclude
on this basis that the mating system of Ardipithecus ramidus was
monogamy. Diminished competition among males would also be
 hypotheses for hominin canine reduction 81

consistent with a relaxed multimale-mutifemale mating system like

that of woolly spider monkeys.
It would be an even greater leap to suggest that modern humans
inherited monogamous tendencies (which are debatable anyway) from
Ardipithecus ramidus. That is both because direct descent of modern
humans from a line extending back to Ardipithecus ramidus is
unclear and because in several later hominin species (with some
question about Australopithecus afarensis (174, 175), there appears
to have been substantial body size dimorphism (128), potentially
indicating elevated male-male competition and/or female selection
for large males. Among characteristics deemed consistent with mono-
gamous ancestry for humans are their relatively small testes, low
sperm motility, and lack of penile spines (176). But, these traits do
not specifically point to monogamy. In living primates, these traits are
associated with minimal sperm competition, which occurs when
females mate with only one (or few) males during their peri-
ovulatory periods (119). Minimal sperm competition occurs not only
in today’s monogamous primates but also in those that live and mate
in polygynous groups (one male, several females). In both groups,
females mate with only one (or a very limited number) of males, so
that a female rarely has the sperm of multiple competing males in her
reproductive tract at one time.
What is interesting, and the crux of the problem, is that despite
body size sexual dimorphism in some later hominins, including early
Homo (177), canine sexual dimorphism continued to decrease.
It seems possible that, as per Greenfield’s “dual-selection” hypothesis
(150), the increasing incorporation of the canine into incisal functions
in Au. afarensis onwards might partly explain this continued reduc-
tion. In addition, in the evolution of Paranthropus species, the zygo-
matic root shifted forward and prognathism decreased – the result
would have been improved mechanical efficiency of the jaw muscles
but with a reduction in gape. Prognathism decreases in the Homo
lineage as well. Hylander and colleagues’ (124) biomechanical analysis
suggests that even if male-male competition had been high in these
82 curious canines

species, such changes in the face and jaw would have constrained the
canine from evolving to greater size. And finally, returning to Darwin,
since Paranthropus and Homo were more consistent bipeds than
Ardipithecus ramidus, the ability to use hand-held weapons may
have precluded selection for large canines anyway.

canine conclusions
Overall then, what can we conclude about the curiously small size of
human canines? First of all, it is clear that small, sexually mono-
morphic canines have been part of our evolutionary history since the
time of Ardipithecus ramidus 4.4 million years ago. Secondly, it is
difficult to see how the evolution of these diminutive canines in
Ardipithecus ramidus could be related to changes in jaw architecture
associated with chewing mechanically challenging foods, given what
we think we know about the predominantly C3 diet of this species and
its relatively thin enamel. On the other hand, changes in the morphol-
ogy of Australopithecus afarensis canines hint at the incorporation of
these teeth into incisal functions. Furthermore, the greater incorpora-
tion of C4 foods in the diet of Australopithecus afarensis and most
later australopiths (especially Paranthropus) suggest that adaptive
changes in jaw architecture associated with chewing mechanically
challenging foods would have limited gape. Gape limitation in
Paranthropus and minimally prognathic early Homo species in turn
would now have acted as constraints on canine size, even if males
began to compete more vigorously with one another.
None of this means, of course, that sexual selection was not
operating during our evolutionary history, but simply that it did not
result in much of sex difference in canine size. It has been suggested
(178) that across primates there appears to be a “trade off” in sexual
selection for large male canines vs. wide male faces. The evidence
comes from a study of fourteen species of anthropoid primates, in
which there is a negative correlation between sexual dimorphism in
canine height and sexual dimorphism in the width of the face across
the cheekbones. The authors of this study point out that male
 canine conclusions 83

cheekbones become larger under the influence of testosterone during

puberty and that several studies have demonstrated that human
females have a preference for wide male faces. While the number of
species in this study is small, it is nevertheless an interesting possibi-
lity that wide faces in both human and nonhuman primates may serve
as a signals to females of male quality when canines lose their signal-
ing function.
Leaving behind the question of our small canines, the next
chapter considers dental evidence for another unique aspect of
human biology – our prolonged periods of growth that are unmatched
by any other primate. The question this next chapter looks into is
whether any of the australopiths show signs of extending their growth
periods beyond those of modern great apes.
 4 Incisive Insights into Childhood

Although a prolonged period of juvenile helplessness and dependency

would, by itself, be disadvantageous to a species because it endangers
the young and handicaps their parents, it is a help to man because the
slow development provides time for learning and training, which are far
more extensive and important in man than in any other animal.

– Dobzhansky T
Mankind Evolving: The Evolution of the Human Species (179)

Humans, along with their teeth, take a very long time to grow. A puppy
does not stay little for long, and her first adult teeth come in around
five to six months of age. Contrast this puppy with a human baby, who
will not get her first adult teeth until she is around six years of age.
A protracted growth period is considered one of humanity’s
uniquely derived features relative to other primates. One view is
that over the course of our evolutionary history, human juvenile
growth was extended by the insertion of a novel developmental
phase – childhood – which has been defined as a period after weaning
during which a juvenile continues to depend on others for survival
(180). Whether or not human childhood is unique, it is clear that
subadult growth spurts begin at much later ages in humans than
they do in African apes (181). Humans reach sexual maturity at com-
paratively later ages as well (181).
Viewed through the lens of “life history” theory, the scheduling
of key life benchmarks such as age at weaning, age at sexual maturity,
age at first reproduction, intervals between births, and natural life
span, is shaped by natural selection. For different species experiencing
different environments and ecologies, natural selection will result in
different life history solutions – or adaptations – to the problems of
survival and reproduction. Natural selection is thought to have

84
 incisive insights into childhood 85

optimized the amount of energy organisms devote to growth versus

reproduction at different points in their lives. There is a trade off
between the two because energy is limited and so can be devoted to
either growth or reproduction, but usually not simultaneously to
both (182).
According to life history theorists and biologists Eric Charnov
and David Berrigan (182), the optimal age at which a primate species
reaches sexual maturity is largely determined by adult mortality – the
risk of death due to “extrinsic factors” such as predation, disease, or
accidents. If that risk is high, the earlier a primate species can start
reproducing, the better for leaving lots of offspring. If that risk is low,
then the selective pressure to mature early is relaxed. But, that leaves
open the question of whether there are actually selective
advantages to prolonging juvenile growth periods and delaying repro-
duction, as primates tend to do in comparison to many other mam-
mals, and humans do in the extreme.
One school of thought is that slower rates of growth are favored
when juveniles face the risk of starvation. According to Janson and
Van Schaik’s “ecological risk aversion hypothesis” (183), extended
juvenile periods with slow rates of growth in primates evolved as an
adaptation to avoid feeding competition with adults, with whom
juveniles must maintain close proximity for protection. In species
that face uneven resource availability where the risk of starvation is
greater, even slower growth rates are favored. For example, frugivor-
ous primate species that rely on seasonally available fruits tend to
have slower rates of growth that folivorous ones, who face less fluc-
tuation in their food supplies (184).
Anthropologist Steve Leigh (181) points out that “ecological risk
aversion” might help to explain the evolution of the extremely slow
growth of humans. Leigh notes that human brains are energetically
expensive. Slower rates of body growth would prevent starvation
when so much energy is being devoted to brain growth and develop-
ment. It is surprising how much energy the brain guzzles during child-
hood. Using PET scan and MRI data, human biologist Chris Kuzawa
86 incisive insights into childhood

(185) and colleagues recently found that the brain’s use of glucose rises
to a lifelong high during childhood, corresponding to 66% of the
body’s resting metabolic rate and 43% of the body’s daily energy use.
These researchers further found that rates of body growth during
the period from infancy to puberty are slower when the brain is con-
suming glucose at its highest levels, potentially explaining why large-
brained humans take so long to grow up. The selective benefits of large
brains, such as greater success in obtaining food, avoiding predators,
and acquiring mates, are the key to this scenario. Slow growth rates
permit the diversion of energy to brain growth and development when
larger brains make a substantial contribution to reproductive success.
A related idea is that slow human growth rates are related to
maternal energetics. Primate females, and especially humans, make
use of fat stores as body “capital” to supply the energy needed to
gestate and nurse offspring. By growing for longer periods, human
females may have been able attain the large body sizes required to
support their offspring’s energetically expensive brains (186).
According to this idea, human mothers with delayed maturation
would have had a selective advantage in being able to support offspring
with large and complex brains.
Evolutionary theorist Theodosius Dobzhanksy, in the 1962 quo-
tation that heads this chapter, encapsulates a long-held explanation
for the evolution of childhood, namely that it provides necessary
learning time (187). In this view, extended association with mothers
affords children time to master complex cultural adaptations that will
greatly enhance their survival and reproduction. The large evolution-
ary payoff of learned skills and knowledge offsets the cost of the
reproductive delay that prolonged growth periods entail.
To what extent these different possible influences on our pro-
tracted growth periods came into play over the course of human
evolution is not clear. That brains are in some way related to the
pace of life history seems quite likely. There is a strong correlation
between brain weight and gestation time across placental mammals
(188). Similarly, there are strong correlations between brain weight
 incisive insights into childhood 87

and various aspects of life history across the primate order (187,
189–191). We may never know whether selection initially favored
prolonged growth because of the increased learning time it pro-
vided, or whether increased learning time was a by-product of the
slow growth that our energy-consuming large brains required.
Nevertheless, through the study of fossil dental growth and devel-
opment, great insight has been achieved into the question of
whether early hominins shared this defining feature of our biology.
Published in 1981, Lovejoy’s scenario of human evolution
(discussed in Chapter 3) tied together monogamy and male provi-
sioning of females and their young with a decrease in interbirth
intervals that would have allowed early human ancestors to speed
up their reproductive rates. Lovejoy’s perspective was that these
greater reproductive rates made possible “. . . protraction of the
subadult (learning) period” (1981:348) with its consequent delay in
age at first reproduction. Based on Anthropologist Alan Mann’s
studies of dental development in South African autralopiths,
Lovejoy felt that there was “. . . strong evidence that a major demo-
graphic shift was fully developed 2.0 to 2.5 million years ago which
included an extended period of sub-adult dependency” (1981:350).
Dean and Lucas (192) note that the idea of prolonged juvenile
growth in australopiths goes back to Raymond Dart (193), who
believed that the Taung Child’s greatly worn deciduous teeth evinced
a delay in the eruption of the first permanent molars. Long periods of
childhood dependency in australopiths would mean that they had
taken a “giant biological and cultural leap toward ‘humanness,’” as
science writer Bruce Bower put it (194). But, the view that early
hominins had human-like childhoods was about to change dramati-
cally over the course of the 1980s, as research on dental development
increasingly focused on growth increments in teeth that represent
absolute time.
Today it seems clear that early hominins tended to develop
more quickly than do modern humans. However, today most
researchers also recognize that not all aspects of dental development
88 incisive insights into childhood

are equally informative about the length of juvenile growth periods,

that not all aspects of dental development in early hominins can be
characterized as either ape-like or human-like (195, 196), and that
growth periods in early hominin species may have been rather variable
(196). As this chapter recounts, such advances in understanding were
made possible by much work–on clarifying the strength and nature of
relationships between dental development and life history, on docu-
menting ranges of variation in great ape and human dental develop-
ment, on understanding enamel growth processes, and on applying
innovative technologies.

how strong are the links between dental

development and juvenile growth periods?
In 1935, anatomist Adolph H. Schultz published a pioneering com-
parative study (197) of dental eruption in fifteen primate genera on
2,908 skulls from various laboratories and museums. His data on
dental eruption sequences revealed a pattern today known as
“Schultz’s Rule.” The idea rested on differences in eruption between
molars, which have no deciduous predecessors, and the eruption of
incisors, canines, and premolars, which do. Schultz noticed that in
species with rapid growth periods, first and second molars are the first
teeth to erupt into the oral cavity. But in slower growing species, the
permanent successors of deciduous teeth – the permanent incisors,
canines, and premolars – erupt early relative to molars.
In lemurs, for example, first and second molars erupt in advance
of the permanent replacing teeth. This is not so in chimpanzees, for
whom first molar eruption is followed by eruption of permanent
incisors, and only after that do the second molars erupt. Humans are
even more extreme in this regard, with permanent central incisors
generally erupting before or together with first molars (198), and lat-
eral incisors, canines, and premolars erupting before the second and
third molars do. Schultz’s Rule is a generalization about the sequence
of permanent tooth eruption. According to this rule, longer-lived
species shift the eruption of their replacing teeth to earlier in the
 links between dental development & juvenile growth 89

sequence of dental eruption. The evolutionary reason for this has to do

with tooth wear. If a species prolongs growth, it will be necessary to
replace the deciduous teeth relatively earlier in the sequence of dental
development because the deciduous teeth will simply wear out before
the first molar erupts.
As Schultz put it, “. . . in man the tremendous and unique
lengthening of postnatal growth, accompanied by corresponding
increases in the ages of dental eruption, has brought about
a dangerously long period of functioning for the deciduous teeth with-
out any improvement in the durability of the substance of these teeth”
(1953:543). Why didn’t larger deciduous teeth evolve instead?
Anthropologist B. Holly Smith points out (191) that this may not
have been an option. In placental mammals, deciduous teeth begin
to form in utero and are often already present at birth, when the small
size of the face and jaw would limit the size of the deciduous teeth
they could accommodate.
Beyond noting patterns of dental development, Schultz (199)
found that the absolute ages at which teeth erupt tend to increase
across the primate order in relation to the “pace” of life history.
Schultz superimposed dental eruption ages over a diagram of life
stages across different grades of primates (Figure 4.1, based on
Schultz [199]). He used tooth eruption ages as a relatively stable
marker of development associated with life stages. He defined infancy
as the period between birth and the eruption of the first permanent
tooth and juvenility as the period of time between this and the erup-
tion of the last permanent tooth. Dental eruption could be used in this
way because, as B. Holly Smith explains, teeth are developmentally
integrated with the development of the organism as a whole. Teeth
must be present for weaning to occur, permanent teeth must replace
deciduous ones before they wear out, and the face and jaw must grow
large enough so that there is space for the molars to erupt.
Building on Adolph Schultz’s work, B. Holly Smith established
a comparative primate context of great utility (191, 200). She found
that across primate species, brain size, body size, and life history
 -65- KEY

Female post-
-60-
reproductive period

-55- Female reproductive

period

-50- Juvenile period to last

permanent teeth

-45- Infancy period to first

permament teeth

-40-
-years-

-35-

-30-

-25-

-20-

-15-

-10-

-5-

birth
Lemur Macaque Gibbon Chimp Human

figure 4.1: Approximate primate life history phases, based on Schultz

(1960). Schultz defined the period of infancy as the period of time prior to
the eruption of permanent teeth. He defined the juvenile period as the
span between the eruption of the first and last permanent teeth. Dental
eruption provided Schultz with a stable marker of development with
which to define these phases. Approximate time periods in Schultz’s
diagram were retained here, with the exception of the postreproductive
period, which is shown here to be much longer in humans than in other
primates. Drawn by author.
 links between dental development & juvenile growth 91

variables were highly correlated with the age at which first molars
erupt. For twenty-one primate species, the correlation between brain
weight and M1 eruption was highest, at 0.98 (a correlation of 1 is
a perfect correlation), supporting the view that the brain acts as
a “pacemaker” for life history. The second highest correlation was to
weaning age, at 0.93 (fifteen species), which in Smith’s view reflects
a functional tie: having first molars in occlusion at weaning facilitates
the processing of solid food. Holly Smith’s work suggested that first
molar eruption ages determined for fossil forms could be used as
a proxy for the paces of their life histories, and might be particularly
informative about weaning age.
Today, most researchers on dental development in fossil homi-
nins realize there are limitations to such inferences. Correlations
among living species do not necessarily hold for fossil species that
are millions of years old, as relationships may have changed over time.
Furthermore, a correlation across a broad taxonomic range of species
does not guarantee that at finer scales the correlation will hold true.
Indeed, much of the variation in life history present in mammals
occurs at higher taxonomic levels, i.e., it is associated with the evolu-
tion of major clades (201). More specifically, the idea that molar erup-
tion age is related to life history variables within the great ape clade
has recently been challenged (202). Even so, Kelley and Schwartz
showed that ages at first reproduction in great apes are consistent
with their ages at M1 eruption, with the earliest ages for both in
gorillas, followed by chimpanzees, orangutans and lastly,
humans (203).
Still, it isn’t clear that the presence of first molars is functionally
related to weaning. First molar eruption in wild chimpanzees does not
appear to dictate when mothers introduce solid foods to their young
(204). Modern humans are themselves a challenge to the notion that
first molar eruption predicts weaning age. Although first molar erup-
tion occurs at around five to six years of age in different human groups,
weaning age is usually much earlier than this (205). These modern
understandings of the limits of life history inference from teeth leave
92 incisive insights into childhood

us with the recognition that first molar eruption may not be a specific
indicator of weaning age. But, first molar eruption age nevertheless
appears to be associated with ages at first reproduction within the
great ape clade (203). Because this clade includes hominins, the asso-
ciation between age at first molar eruption and age at first reproduc-
tion may be usefully applied to them – assuming, of course, that the
association has not changed over time.

other aspects of dental growth and development

in relation to life history variation
Beyond first molar eruption, other aspects of dental growth and devel-
opment have been studied for their potential relationships to the pace
of life history in a comparative primate context. Gabrielle Macho (206)
found that adult brain size, body size, weaning age, age at reaching
sexual maturity and lifespan were strongly correlated across a broad
taxonomic range of primates with the length of time it takes for first
molar crowns to form. Her result makes sense if the time it takes to
form first molar crowns affects the time at which first molars erupt.
Yet, once again on a smaller scale, it has been noted (207) that the first
molar crown formation times of humans, gorillas, and orangutans are
essentially the same (202, 207), even though ages at first molar erup-
tion differ among them. This finding suggests that first molar crown
formation time is not a useful indicator of variation in growth periods
within the great ape clade.
Another dental growth variable that may have some relation-
ship to the pace of life history at a broad taxonomic level is the rate of
enamel formation in the tips of tooth cusps. This variable shifts from
faster to slower from monkeys to apes to humans (208).
The possibility of relationships between other microstructural dental
growth variables and life history variation has also been explored, but
they are only weakly-to-moderately correlated with the scheduling of
life history (209). Such relationships may be tenuous because process
is not the same as outcome. For instance, while there is a strong link
between first molar eruption age and life history variation across
 dental growth and development in relation 93

a broad taxonomic range, different processes or factors may contribute

to different ages at eruption in different species. If natural selection
acts on first molar eruption (an outcome) and there are many different
processes or developmental stages that species alter to achieve that
outcome (e.g., changing rates of crown or root formation, or changing
their overall formation periods without altering their formation rates),
then there is no reason to think that relationships between these
processes and stages to life history variation will be strong.
Nevertheless, in recent years, one dental growth variable has
been shown to be rather strongly associated with life history variation
across the primate order. This variable is the length of time between
“long-period” growth lines in enamel. To describe what we currently
know about this relationship requires a digression into how enamel
forms.
Enamel begins to form at the cusp tip of a developing crown
(Figure 4.2). Ameloblasts, which are enamel-forming cells, secrete an
organic matrix of proteins, primarily composed of amelogenins,
which serve to “accept” mineral. As ameloblasts differentiate from
their epithelial cell precursors, they move away from the boundary
between enamel and dentine (the enamel-dentine junction or EDJ) and
toward what will eventually become the enamel surface. During this
secretory stage of enamel formation, enamel becomes 30% minera-
lized. In the following maturation stage, ameloblasts alternate
between adding mineral to the matrix and removing water, amelo-
genin proteins, and other organic materials until the enamel attains
a state of 96% mineralization.
During the secretory stage, as ameloblasts migrate away from
the EDJ secreting the enamel matrix, ribbon-like mineralized struc-
tures known as “enamel prisms” or “enamel rods” form in their wake.
In thin sections of enamel viewed under a transmitted light micro-
scope, fine lines called cross-striations can be seen cutting across the
diameter of each enamel prism at regular intervals (Figures 4.2 and
4.3). Studies dating to the early 1900s (210, 211) first suggested that
cross-striations form according to a circadian rhythm. Mimura
94 incisive insights into childhood

(a) enamel (b) (c)

a1
dentine
a1 enamel- a2
crown a2 dentine
pulp junction
a3
(EDJ)

root

(d)
enamel rods (or
Striae of prims) marking
Retzius the path taken by
marking ameloblasts;
EDJ
successive stripes along the
enamel- rods represent
forming cross-striations
fronts

figure 4.2: Diagram showing the process of enamel formation in

a section through the middle of a tooth. The area in B is an enlarged
portion of the cusp of the tooth, just as the first two ameloblasts, a1 and a2,
have differentiated from the inner enamel epithelium and begun to move
outward, secreting enamel matrix. The area in C shows the process of
enamel formation at some later point in time, as a third ameloblast, a3, has
differentiated and has begun to move outward, secreting enamel matrix in
its wake. The area in D diagrams mineralized structures known as enamel
rods (or prisms) that mark the paths of ameloblasts. Along the rods are
cross-striations or short-period lines that reflect daily fluctuation in the
secretion of enamel matrix. Every few days, a slowing of enamel
formation occurs at and is marked by dark lines called striae of Retzius.
These lines represent the enamel-forming front at successive time
periods. striae of Retzius are also called long-period lines and the number
of days between straie is called the stria periodicity. All of the permanent
teeth of an individual have the same stria periodicity, although
periodicities range from six to twelve days in modern humans (see text for
further explanation). Drawn by author.

confirmed this rhythm in 1939 by injecting growing mammals with

lead acetate and sodium fluoride (212). These chemicals marked the
enamel forming in their teeth at the time of injection. The number of
 dental growth and development in relation 95

cross-striations between these marking corresponded exactly to the

number of days between injections.
Anthropologist Timothy Bromage used a similar experimental
design to confirm the daily formation of cross-striations in enamel in
a primate (simultaneously confirming the daily formation of analo-
gous structures in the underlying dentine). More recently Rodrigo
Lacruz and colleagues showed that mouse ameloblasts not only
express “circadian clock” genes, genes required for generating circa-
dian rhythms, but also produce amelogenin proteins according to a 24-
hour rhythm (214). Cross-striations are therefore now well accepted as
growth lines that form according to a daily rhythm.
Cross-striations also go by the name of “short-period incre-
ments” to differentiate their 24-hour formation period from that of
“long-period increments” in enamel. Microscopically, long-period
increments appear as dark lines traversing a series of enamel rods at
an angle (Figure 4.3). They are also called striae of Retzius, after their
discoverer Anders Retzius, a Swedish anatomist of the nineteenth
century (74). Striae of Retzius are actually a series of growth layers in
a three-dimensional tooth that form when all the ameloblasts along
the enamel-forming front (Figure 4.2) simultaneously slow their secre-
tion of the enamel matrix (215).
The simultaneous slowing of secretory ameloblasts occurs at
regular intervals throughout all of the teeth of an individual (215, 216),
which suggests a common cause. The interval, however, varies among
individuals. In humans, the average interval for permanent teeth is
eight or nine days, ranging from a minimum of six days to a maximum
of twelve (217). To determine the interval for an individual’s teeth,
one counts the number of cross-striations falling between striae of
Retzius. For the virtual (synchrotron-imaged) tooth section shown in
Figure 4.3, striae of Retzius repeat with a periodicity of eight days.
Exactly what causes the regular periodicity of Retzius striae is not
clear. There are metabolic (218) and cardiovascular rhythms with simi-
lar periodicity in humans and other animals (219), possibly suggesting
that a systemic rhythm produces the periodicity of Retzius striae.
96 incisive insights into childhood

figure 4.3: Synchrotron image of striae of Retzius (white arrows).

Eight short-period increments (white brackets) can be seen between the
 dental growth and development in relation 97

Recently, anthropologist Timothy Bromage and colleagues developed

the idea of systemic growth rhythms further (220, 221). They found that
mean periodicities in mammalian species range from one to fourteen
days, with small-bodied mammals (e.g., mice) having low periodicities
and large-bodied mammals (e.g., elephants) having high periodicities.
They also found that across primates, species’ mean periodicities cor-
relate with life history variables, mean body masses, mean basal meta-
bolic rates and the mean rates at which bone-forming cells (osteoblasts)
proliferate. These associations led them to conclude that “some aspect
of metabolism” regulates “. . . cell proliferation rates and growth, thus
controlling the pace, patterning, and co-variation of life history traits”
across primates” (2012:131). In their view the periodicity of striae is
a result of a species-specific metabolic growth rhythm, which they
named the Havers-Halberg Oscillation (in reference to scientists
Clopton Havers, hard tissue anatomist, and Franz Halberg, chronobiol-
ogist who pioneered the investigation of long-period rhythms).
Whether Bromage and colleagues are correct in the entirety of
their explanation – that the periodicities of striae represent species-
specific metabolic growth rhythms that control the pace of life his-
tory – there are moderate to strong correlations between mean peri-
odicity and such aspects of life history variation as weaning age, age at
sexual maturity, age at first breeding and lifespan. These associations,
however, are not strong within the great ape clade, as lowland gorillas
have higher periodicities than common chimpanzees, but are weaned
and begin to reproduce at earlier ages than do chimpanzees. Stria
periodicities along with other aspects of dental growth and

caption for figure 4.3: (cont.)

striae of Retzius. This tooth therefore has an eight-day periodicity. This is

a fossil hominin tooth (DNH 67). The image is modified from (196)
Figure 1 in Smith et al. (2015) PLoS ONE, reprinted here under the terms of
the Creative Commons Attribution License, https://creativecommons.o
rg/licenses/by/4.0/.
98 incisive insights into childhood

development discussed above clearly vary in their reliability as indi-

cators of juvenile growth periods. It may be informative to study as
many aspects of dental growth and development as possible in fossil
species to determine if they give the same signal. Do they all, for
example, indicate more rapid rates of development? Of course, when
they don’t give the same signal, that makes the problem of interpreta-
tion a lot more tricky.

dental growth and development in autralopiths:

human-like or ape-like?
Alan Mann’s pioneering study (222) suggested human-like patterns of
development in four specimens of Paranthropus robustus from the
site of Swartkrans. He noted, for example, that in the SK-64 mandible,
the unerupted first permanent molar is close to completion,
the second deciduous premolar root is almost complete, and there is
no development as yet of the second permanent molar. This pattern of
relative dental development is similar to a human at this stage of
development, and not to a chimpanzee, in which the second perma-
nent molar would have already begun to form. Because the teeth of
autralopiths appeared to progress through the same stages of develop-
ment relative to one another as those of humans, Alan Mann argued
that they all likely erupted according to the same schedule as well.
Of course (and Alan Mann noted this), the whole sequence of
tooth formation and eruption could have been accelerated in austra-
lopiths even if they maintained the same pattern of relative dental
development as modern humans. What was needed here was an esti-
mate of the absolute timing of development, and that is what Bromage
and Dean’s (223) innovative study, published in 1985, offered. These
researchers counted enamel surface manifestations of striae of
Retzius – perikymata (Greek: peri = around; kymata = waves) – to
obtain such estimates. The wavelike “crests” and “troughs” of peri-
kymata encircle the lateral enamel, enamel on the sides of teeth
(Figure 4.4). As long as they haven’t been worn or eroded away, peri-
kymata can be directly observed and counted on fossil teeth under low
 dental growth and development in autralopiths 99

figure 4.4: Synchrotron image of fossil hominin incisor DNH 71.

The virtual section of the tooth shows the striae of Retzius (oblique dark
lines) cropping out onto the enamel surface as perikymata (marked with
asterisks). The image is modified from (196) Figure 1 in Smith et al. (2015)
PLoS ONE, reprinted here under the terms of the Creative Commons
Attribution License. https://creativecommons.org/licenses/by/4.0/

magnification (around 20x or so). Perikymata are simply surface man-

ifestations of striae of Retzius so, the periodicity of an individual’s
striae is exactly the same as the periodicity of his or her perikymata.
By counting all the perikymata from the tip of the tooth to its cervix
(the “bottom” of the tooth) and then multiplying by the mean periodi-
city for a species, an estimate of their lateral enamel formation time
can be made. Bromage and Dean’s counts of perikymata on incisor
teeth from Australopithecus and Paranthropus suggested abbreviated
periods of lateral enamel formation in these teeth (223).
More to the point, Bromage and Dean estimated age at death in
six immature australopith individuals. These individuals died when
their incisor crowns had just completed forming. To estimate their
100 incisive insights into childhood

ages at death, Bromage and Dean assumed that the incisor teeth had
begun to form three or four months after birth. They added to this
“initiation time” an estimate of the amount of growth that had
occurred in the cusp of the tooth. In the cuspal region of the tooth,
the striae of Retzius cover one another like layers of an onion and so do
not emerge as countable perikymata on the crown surface. This period
they estimated to be about six months, bringing the total to nine
months of life so far. The crucial step was to add to this nine-month
estimate the count of perikymata in the lateral enamel multiplied by
the periodicity of seven days (then assumed to be the mean periodicity
for both humans and hominins).
For example, for Australopithecus afarensis specimen LH2, the
perikymata count of 130 was multiplied by seven days. Added to
the nine-month estimate for growth prior to this, the age at which
the incisor crown completed formation works out to about 3.25 years
of age. Yet, previous estimates for the age of death based on modern
human charts of dental development suggested the individual had
died at 4.45 years of age. Indeed all of the hominins in their sample
had a “. . . biological equivalence to modern man at roughly two-thirds
the chronological age, demonstrating that they had growth periods
similar to modern great apes” (1985:326).
Bromage and Dean’s study broke new ground and many support-
ing studies based on growth increments followed. Despite the huge
size of Paranthropus boisei molars, they appeared to form in shorter
time periods than do those of modern humans (224). P. boisei molars
appeared to accomplish this feat through increasing the rate at which
ameloblasts secreted enamel matrix as well as by increasing the rate at
which the crown grew in height. For immature individuals who died
while their first molars were erupting (or had recently erupted),
Beynon and Dean (225) estimated age at death by using growth incre-
ments on incisors, just as Bromage and Dean had done. (See Figure 4.5,
which shows the LH 2 mandible, in which the incisor has just com-
pleted crown formation as the first molar is erupting.) This gave ages
at M1 eruption for Australopithecus at 3.5 years and even slightly
 dental growth and development in autralopiths 101

erupted permanent first molar

central
incisor
crown

figure 4.5: Artist’s rendition of right side of LH 2 mandible

(Australopithecus afarensis) in which lower the central incisor crown has
just completed formation and the first molar has just erupted. Using
growth increments (perikymata) from the incisor crown, it was possible to
estimate the age at death of the LH2 juvenile and to therefore estimate the
age at which the first molar erupted into occlusion. See text for additional
explanation and discussion. Figure 4.5 is a drawing by Alyssa Starrett
adapted by permission from Macmillan Publishers Ltd: Nature:
Beynon AD, Dean MC. Distinct dental development patterns in early
fossil hominids. Nature. 1988;335:509–514.

earlier in Paranthropus, within the known range of M1 eruption ages

for apes but well outside the known range of M1 eruption in modern
humans. Ape-like eruption times for australopths made sense given
that their brain sizes were comparable to those of chimpanzees and
first molar eruption ages are highly correlated with brain size across
the primate order (190, 200).
Continuing along this line of investigation and using a large
modern human comparative sample, Dean and colleagues (226)
demonstrated that counts of perikymata on australopith anterior
teeth were lower than those of Homo sapiens. They were especially
low for the small anterior teeth of Paranthropus. Rates of cuspal
enamel formation were also faster in australopiths than they are in
modern humans. Both of these findings point to faster developmental
rates in australopiths. Dental biologist and anthropologist Rodrigo
Lacruz and colleagues (227) used a confocal microscope to obtain
periodicities from naturally fractured teeth. This method allowed
them to make serial “optical sections” from the fractured planes.
102 incisive insights into childhood

Overall, the periodicities they obtained for eight Australopithecus

africanus teeth and seven Paranthropus robustus teeth centered
around seven days. If periodicities bear some relationship to the pace
of life history, these results too suggest a faster pace in australopiths
than in modern humans, whose periodicities center around eight to
nine days (217).
In parallel with this work on incremental growth lines in teeth,
work on patterns of dental development in fossil hominins continued
to progress. As long ago as 1951, Broom and Robinson had suggested
that the eruption patterns of Paranthropus were more similar to those
of Homo than to Australopithecus (228). Using radiographs,
Christopher Dean (229) seemed to find evidence of this in the nearly
simultaneous eruption of the first molar and first incisor in both Homo
and Paranthropus. Australopithecus afarensis and Australopithecus
africanus were more like modern apes in erupting their first perma-
nent molars well before erupting their incisors. Following Schultz’s
logic, Australopithecus afarensis and africanus would be assumed to
have had abbreviated growth periods compared to both Paranthropus
robustus and to modern humans. Modern humans have to erupt their
permanent anterior teeth relatively early in order to replace their long-
functioning and worn out deciduous precursors. This explanation
however, did not seem to fit Paranthropus robustus, whose deciduous
teeth did not show excessive wear. Dean therefore suspected that the
similarity between Paranthropus robustus and modern humans was
superficial—that it represented homoplasy rather than a shared
derived feature. Further analysis based on CT scans suggested that
Paranthropus may not have been like modern humans in the simulta-
neous eruption of the M1/I1 (230) after all, but that it did have a more
human-like M1/I1 developmental pattern (231).
Follow-up studies also suggested a more ape-like overall pattern
of dental development in australopiths. In 1986, Holly Smith (195)
plotted stages of dental development of fossil hominins on develop-
mental charts for apes versus humans. P. boisei, P. robustus,
Au. africanus and Au. afarensis all were more similar in their relative
 dental growth and development in autralopiths 103

states of dental development to apes than to modern humans.

The following year, Conroy and Vannier (232) CT-imaged developing
teeth inside of the Taung Child’s jaw, whose first molar had erupted.
They compared the developmental state of the Taung Child to that of
a 3–4-year old chimpanzee and a 5–6-year old modern human, both of
whose first molars had just erupted. Like the chimpanzee, the Taung
Child’s anterior teeth had not yet developed much of their roots.
The modern human, by contrast, had more advanced anterior tooth
development, in line with Schultz’s rule.
These studies of incremental growth and patterns of dental
development did not go unchallenged. Chief among the critics
were Alan Mann and colleagues, whose analyses helped move
this entire area of research forward. With respect to studies of
incremental growth, Mann and colleagues (233) questioned
whether cross striations or striae of Retzius were truly markers
of time in enamel, whether the latter consistently emerged onto
the enamel surface as perikymata, whether comparisons had been
made to a sufficient number and range of modern humans as well
as apes, and whether anterior tooth formation times reliably indi-
cated the length of juvenile growth periods.
The first of these criticisms spurred Bromage’s (213) demon-
stration of the circadian rhythm of cross-striations. The second
criticism spurred work demonstrating a close correspondence
between striae and perikymata counts on anterior teeth (234).
The third was partly addressed by later studies that broadened
the range and number of modern humans to which hominins
were compared. But, even today, we lack complete knowledge of
the extent to which ape and human dental development can vary,
and as this knowledge trickles in, interpretations can and do
change. As for the fourth criticism, this is still valid. Ape anterior
teeth are larger than those of modern humans – their crowns take
absolutely longer to form than those of modern human teeth
(235) – yet their life histories are certainly faster paced. That fact
104 incisive insights into childhood

suggests it is unwise to rely on anterior teeth as an indicator of life

history variation within hominoids, including fossil hominins.
Up until just the last few years, the consensus has been that
hominins correspond more closely to apes than to modern humans in
the pace and pattern of their dental development, and by extension in
the length of their juvenile growth periods. Yet, it was also clear that
they were not identical to modern apes in their dental development.
For example, early fossil hominins had abbreviated anterior tooth
crown formation times relative to great apes (196) as well as to most
humans (226). Another difference is that robust australopith crowns
have perikymata that are more uniformly distributed along their
enamel surfaces than do either modern humans or chimpanzees,
which show greater compaction of perikymata toward the cervix
(236). The specific enamel formation processes underlying this differ-
ence are not clear from examining the enamel surface, but clearly the
robust australopiths were forming their enamel differently in some
way than do either apes or humans. While such observations hint at
hominin uniqueness, the most recent research gives hominins their
dental developmental due.

dental development in australopiths

re-envisioned: neither human nor ape-like?
As teeth erupt, they move from their bony crypts through the jaw bone
(specifically the alveolar bone), then break through the gingiva (gums),
and finally come to rest in their functional positions in the jaw. It has
been pointed out that the event of M1 eruption in fossil hominins is
assessed from bones and teeth, yet correlations between M1 eruption,
brain size, body size, and life history features in living primates are
based on M1 emergence through the gingiva, soft tissue which does
not preserve in the fossil record (203). It has also been pointed out that
estimates of first molar eruption in fossil hominins using growth
increments are based on a mix of actual data from the fossils (e.g.,
counts of perikymata) and estimates of unknown variables (e.g., per-
iodicity, initiation of crown formation, cuspal enamel formation)
 dental development in australopiths re-envisioned 105

(196, 203). With these points in mind, two sets of researchers have
recently conducted new assessments of australopith dental
development.
Just how similar australopiths are to apes or humans in dental
development requires knowledge of variation within and among
species of great apes as well as among different human population
groups. M1 eruption ages, it turns out, are more variable than pre-
viously realized, both within the great apes and within modern
humans. Up until recently, chimpanzee M1 eruption ages were
obtained primarily from captive individuals, and fell into the range
of 3 to 3.5 years (203). Now data are becoming available from indivi-
duals who grew up in the wild, and their average age for first molar
eruption is close to four years of age (203). Other primate studies have
also shown a tendency for dental eruption to occur earlier in captive
individuals (237). Possibly this is because in in captivity, greater
availability and stability of food resources allow growth rates to
accelerate. Meanwhile, there is much variation within great apes.
Lowland gorilla first-molar eruption appears to be slightly earlier
than that of chimpanzees while orangutans top the great ape M1
eruption chart at 4.6 years of age (203, 207).
As for modern humans, average M1 eruption ages for humans
are said to be around 5.8 years (203), yet this average masks much
interpopulation variation. In her review of dental eruption data world-
wide, dental anthropologist Helen Liversidge (in (238)) found that
Africa has great variation in M1 eruption ages. For one Kenyan popu-
lation, the average age of M1 eruption was 4.74 years in girls and 5.15
years in boys. But also in Kenya, another population exhibited M1
eruption ages of 6.08 years on average for girls and 6.47 years for boys.
So how do the recently revised age estimates for M1 eruption in
hominins compare?
Kelley and Schwartz reevaluated M1 eruption in six fossil homi-
nins by estimating when gingival emergence would have occurred in
these specimens (203). This had the result of shifting M1 eruption to
earlier ages than previous estimates, ranging from 2.9 years of age
106 incisive insights into childhood

(LH2, Australopithecus afarensis, and STS 24, Australopithecus afri-

canus) to 3.8 or 3.9 years of age (SK 62, Paranthropus robustus). When
they considered the known range of eruption in apes – 3.8 (gorillas) to
4.6 years (orangutans), it seemed to them that dental eruption in
hominins occurred even earlier than it does in today’s apes!
What might that mean? It might mean that these australopiths
also had more accelerated life histories even than apes – except for one
small problem. Using newly acquired data, Kelley and Schwartz rea-
nalyzed the relationship Holly Smith showed between M1 emergence
and brain size across anthropoid primates. They found that if you
plotted brain sizes of hominins on these graphs, you could predict
what their M1 emergences ages “should” be for their brain sizes.
It turned out that M1 emergence ages predicted in this way were all
greater than the new estimates Kelley and Schwartz obtained for M1
emergence ages in the fossil hominins. What could account for the
mismatch? Perhaps their fossil hominin M1 gingival emergence esti-
mates were all uniformly too low. Or, perhaps the relationship
between brain size and M1 gingival emergence in australopiths dif-
fered from that of living hominoids.
And, finally, it is also possible, as Kelley and Schwartz noted,
that M1 gingival emergence in australopiths could be out of sync with
their pace of life history and rates of somatic growth. There is pre-
cedent for such a situation in modern primates. A family of prosi-
mians, the Indriids of Madagascar, have fast rates of dental
development and early weaning coupled with slow rates of somatic
growth (239). Laurie Godfrey proposes that early dental eruption and
weaning together with slow infant growth rates are adaptations to the
severe drought conditions Indriids face (239). Essentially, slow infant
growth rates reduce the amount of milk mothers need to produce on
a daily basis, while the presence of deciduous teeth at birth allows
mothers to wean their offspring early. These adaptations lessen the
energetic burden of lactation during drought conditions, when
resources are scarce. Perhaps in australopiths, like these Indriids,
selection pressures associated with energetic stress on lactating
 dental development in australopiths re-envisioned 107

mothers account for M1 emergence times that are earlier than

expected on the basis of these hominin’s brain sizes.
Most recently, anthropologist Tanya Smith and her colleagues
shed some light – actually, very high-energy x-rays – on this conun-
drum (196). They used a technique called x-ray synchrotron micro-
tomography to create “virtual sections” of fossil teeth. The work was
done at the European Synchrotron Radiation Facility in Grenoble,
France, which is one of only a few such facilities in the world. This
technique allowed Tanya Smith and her colleagues to “see inside”
teeth without having to cut them up. They were able to image both
long- and short-period lines (see Figures 4.3 and 4.4). They were also
able to determine actual periodicities and actual time periods for
cuspal enamel formation. Finally, they could see the “neonatal”
line, an accentuated line in enamel that marks the event of birth.
Using that line, and matching the pattern of other accentuated lines
like a bar code across other developing teeth, they reassessed age at
death in twelve australopiths. As they explained, their method
required no estimation by substituting values from great apes or
humans for unknown variables. All of the variables estimated in
previous studies – periodicity, initiation, and cuspal enamel forma-
tion – were directly ascertained from the fossil teeth themselves.
Smith and colleagues then determined what the “dental ages” of
the hominins would be based on a chimpanzee-like developmental
schedule. In other words, how old would these hominins have been
when they died if their teeth developed on a chimpanzee time frame?
It turned out that the “chimpanzee” ages didn’t match the
synchrotron-derived ages at death. But the “dental ages” of the homi-
nins predicted on the basis of human developmental standards also
didn’t match the synchrotron-derived ages. So, it seems that the
autralopiths developed according to their own schedule.
Furthermore, some of them appear to have been on the high end of
the ape range for M1 emergence – the age at death in one specimen
(STS 24) whose first molars had just erupted into occlusion was 4.4
years. One of the robust australopiths (DNH 107) had an age at death of
108 incisive insights into childhood

4.8 years, but with only slight wear (and the right mandibular incisor
had not yet erupted), suggesting M1 emergence was not much earlier.
So, not all australopiths, it seems had early ages of M1 eruption.
Indeed, the low end of first molar eruption average values in modern
humans – 4.74 years in girls and 5.15 years in boys – is close to the M1
eruption age of one of the robust australopiths. Finally, Smith and
colleagues also found that australopiths did not have uniformly lower
periodicities than modern humans. While the averages for each spe-
cies are small, the fossil australopith periodicities ranged between 6 to
12 days, very similar to those of modern humans. (Chimpanzee peri-
odicities are found in a narrower range of 5–7 days).

conclusions
Taking Kelley and Schwartz’s and Smith’s and colleagues’ reassess-
ments together, it now seems that some fossil hominin species had
faster dental development than some modern apes, while others were
at the slow end of the modern ape developmental range. Based on their
M1 eruption ages, australopiths do not seem to have quite reached the
slow developmental pace of modern humans, though some indivi-
duals may have come close. In a way, this should not come as a huge
surprise, as these species had their own evolutionary histories and
were neither ape nor human. Their rates of dental development and
the paces of their life histories would have been varied, shaped by
selection pressures in the diverse environments and time periods in
which they lived.
There are still some unresolved questions, however. Recalling
the dissociation between dental development and somatic growth in
Indriids, it would be interesting to know whether rates of somatic
growth in these australopiths matched their rates of dental develop-
ment. Another unresolved question is how these australopiths’
human-like periodicities comport with their generally earlier ages of
first molar eruption relative to modern humans. If periodicity is
determined by a metabolic rhythm that “sets the pace” of life history
as Bromage and colleagues propose (220, 221), then why do these
 conclusions 109

australopiths have generally earlier ages at M1 eruption than do most

modern humans? Clearly, more basic research on living primates is
required to discover the many factors that may influence periodicity,
M1 eruption ages, rates of somatic growth and development and the
disjunctions that can occur among them.
This chapter concludes the first part of this book, which to this
point has considered how the study of fossil teeth informs us about the
biology of our distant australopith ancestors. Different facets of the
biology of our ancient ancestors and close relatives were considered:
their dietary proclivities and flexibility, the initial causes of and con-
straints on the evolution of their canine teeth, and their developmen-
tal rates. Teeth tell us that these early hominins were diverse – in
some ways human-like, in some ways more like great apes, and in
some ways, unique. Species of the genus Homo, however, demon-
strate a clearer trend. With some exceptions (e.g., Homo floresiensis),
they become more “human-like” over time in their dental morphol-
ogy, dietary breadth, and developmental rates. Part II traces these
changes through teeth.
part ii Teeth and the Genus
Homo
5 March of the Bipeds: The Later
Years

We have come to the conclusion that, apart from Australopithecus

(Zinjanthropus), the specimens we are dealing with from Bed I and the
lower part of Bed II at Olduvai represent a single species of the genus
Homo and not an australopithecine . . . But if we are to include the new
material in the genus Homo (rather than set up a distinct genus for it,
which we believe to be unwise), it becomes necessary to revise the diag-
nosis of this genus.

– Leakey LSB, Tobias PV, and Napier JR

A new species of the genus Homo from Olduvai Gorge. Nature.

With these words, Louis Leakey and colleagues named the species
Homo habilis. In so doing, they widened the definition of the Homo
genus to include a species with smaller average brain size than that of
Homo erectus, which was up until then the earliest known species of
our genus. To include this species in the genus Homo, Leakey and
colleagues revised the so-called “cerebral Rubicon” dividing
Australopithecus from Homo down to 600 cubic centimeters from
the 750 cubic centimeters used up until that point (240). This is what
Leakey et al. meant by revising the “diagnosis of the genus.” Indeed,
over the history of paleoanthropology, definitions of the genus Homo
have expanded further, encompassing the varied features of fossils
assigned to the genus (177, 241). Thus, how to define the genus
Homo – and indeed how to define a genus in the first place – are
matters of long-standing and vigorous debate (47, 177).
In a 2014 review paper in the journal Science, paleoanthropolo-
gist Susan Antón and colleagues’ employed a broad definition of the
genus that included specimens traditionally assigned to the species
Homo habilis (e.g., KNM-ER 1813). In their view, these specimens
shared with later genus members a suite of characteristics that
contributed to their evolutionary success. Namely, these are:

113
114 march of the bipeds: the later years

“. . . increases in average body and brain size and changing dental size
coupled with increased toolmaking and stone transport” which they
contend “suggest dietary expansion, developmental plasticity,
cognitive evolution and social investments” (2014: 1236828–8).
The present chapter gives an overview of species that have been
considered to be members the genus Homo, that to varying degrees
partake in the package of adaptations Antón and colleagues describe.
Key dental features and possible phylogenetic relationships to anato-
mically modern human are integrated into this overview.

homo habilis
Discovered at Olduvai Gorge in 1959 were some hominin teeth that
were strikingly different from those of Nutcracker man found that
same year (13). These teeth, a lower premolar and lower third molar
(wisdom tooth), were small and narrow from side to side, quite unlike
the enormous and square premolars and molars of Nutcracker man.
Yet, the teeth appeared to be of equivalent antiquity. Additional finds,
including more teeth, parts of a cranium, and hand, wrist, and foot
bones, led Louis Leakey and colleagues in 1964 to coin a new
species – Homo habilis. This earliest species of the Homo lineage
dates at least as far back as 2.3 million years ago (242, 243) and possibly
as early as 2.8 million years ago (244).
To Leakey and colleagues, this species rather than Nutcracker
man was the more likely candidate for the maker of the two-million-
year-old stone tools found at Olduvai Gorge. These Oldowan tools
(after Olduvai Gorge) were made by hitting one stone against another,
removing flakes that were then used as tools. Based on two parietal
bones (parts of the cranium), Leakey and colleagues reconstructed the
cranium of Homo habilis, coming up with a larger cranial volume
than for Nutcracker man. So, Homo habilis was judged to be the more
brainy (i.e., more likely toolmaker) of the two species. Furthermore,
their analysis of Homo habilis hand bone fossils suggested that this
species had could achieve a precision grip: the kind of grip used when
grasping an object, like a pencil, between the fingertips and thumb.
 homo habilis 115

Hence, the literal meaning of Homo habilis—handyman. Add to this

picture the smaller molar teeth and more human-like premolars
(although with relatively large incisors), and both mentally and
dentally, Homo habilis seemed to Leakey, Napier, and Tobias to
deserve a place within our own genus.
Later discoveries (of course) greatly complicated the picture.
To begin with is a specimen described in 1987 by Donald Johanson
and colleagues (245). Its palate and teeth indicated that it was
H. habilis, but it seems to have had longer arms than Lucy! This is
not exactly what was expected for a species within our genus. Finds
of H. habilis from other sites: Koobi Fora in Kenya and from Malawi
(246) suggested that H. habilis should be split into two – one species
with australopith limb proportions but more Homo like teeth and
jaws (including the original finds from Olduvai) and a second spe-
cies called Homo rudolfensis with more Homo-like limb propor-
tions but with jaws and teeth that were more robust (247). Indeed,
one of the H. rudolfensis skulls from Koobi Fora has posterior teeth
(molars and premolars) greater than the mean for Paranthropus
boisei (15).
But then, a very H. rudolfensis-looking find was recovered
from Olduvai, where Homo habilis was originally discovered
(248). Such variability from a single site suggests that Homo habilis
may simply be more variable than previously realized, and should
not be split into two species (248). In 2012, Meave Leakey and
colleagues discovered additional early Homo fossils that they
argued confirmed the coexistence of two early Homo species in
Pleistocene East Africa, aside from Homo erectus (249). Most
recently in their 2014 synthesis on early Homo, Antón and
colleagues dealt with the diversity of early Homo by categorizing
them into two different “groups” rather than into two different
species, named according to their most well-known representa-
tives. So, they define a KNM-ER 1813 “group” and a KNM-ER
1470 “group” of early Homo, differing in brain and body size as
116 march of the bipeds: the later years

well as in several cranial and dental features, but with overlapping

ranges of variation (177).1
The H. habilis vs. H. rudolfensis story highlights a perennial
problem in taxonomy about how much morphological variation is
present within living species and how to use this information to draw
species boundaries in the fossil record. It is sometimes difficult to draw
species boundaries even among living organisms, and where those
boundaries are drawn depends on how species are defined. Ernst
Mayr’s biological species concept (BSC), defined in various ways (see
[250] for a review), rests on the notion that species are interbreeding
groups of organisms with no (or negligible) gene exchange with other
groups. Such groups evolve independently of one another, maintaining
the integrity of the species. Species can also be defined morphologically,
in terms of groups of organisms that share distinctive features. But,
where one draws the lines among them on this basis may not reflect the
species as an interbreeding evolutionary unit, as Mayr’s definition does.
In the field of paleoanthropology, fossil species are generally
defined on the basis of morphological features. The morphological
definition of species is a particular problem in paleoanthropology
because, with small and sometimes tiny sample sizes, a fossil species’
full range of morphological variation is unknown. A future paleoan-
thropologist might uncover remains of our highly diverse single inter-
breeding species of modern humans and erroneously split them into
many species. So, when new species are named on the basis of a few
new fossils, it may be quite possible that they are in reality simply
variants of pre-existing ones (what Tim White argued about
Kenyanthropus platyops – see Chapter 1).
Furthermore, whether morphologically defined fossil species
were interbreeding evolutionary units that would fit Mayr’s biological
species concept is unknown (although, when possible, analysis of
ancient DNA offers insight into gene exchange in ancient popula-
tions). Regarding Antón et al.’s (2014) solution to the early Homo
1
Their two newly defined “groups” of early Homo do not correspond to exactly the same
set of fossil specimens formerly divided into Homo habilis and Homo rudolfensis.
 homo erectus and homo antecessor 117

taxonomy problem, naming “groups” of early Homo is useful because

it reflects our uncertainty about their status as separate species. In this
book, simply for ease of reference, these groups will be “lumped”
under the Homo habilis species name, although the diversity of non-
erectus early Homo will be recognized.
Still, the question of whether certain Homo habilis (including
H. rudolfensis specimens) should be included in the genus Homo at all
has frequently been raised (251), ever since Louis Leakey and collea-
gues announced the species and revised the definition of the genus in
1964. That year, the eminent paleoanthropologist Sir Wilfrid Le Gros
Clark opined that the differences of Homo habilis from
Australopithecus were trivial (252). A more substantive criticism
from Wood and Collard (47) highlights the finding of their cladistic
analysis in which Homo habilis (and Homo rudolfensis) do not form
a clade with Homo sapiens that is exclusive of australopiths.
On the other hand, Gonzalez-Jose et al. (44) in their modular
analysis of hominin crania find the opposite and suggest that the
entire Homo clade, including Homo habilis shares more “flexed cra-
nial bases, more retracted faces and an increase in neurocranial globu-
larity” (2008:776). In a similar vein, Antón and colleagues emphasize
that there are greater average brain and body sizes in non-erectus early
Homo (i.e., both 1470 and 1813 groups) than there are in
Australopithecus. Thus, while Homo habilis seems to hover at or
just beyond the threshold to the Homo genus, the rest of the species
discussed in this chapter, have clearly passed beyond it.

homo erectus and homo antecessor

Homo erectus approaches the human condition to a much greater
degree than any previous hominin species. In some ways it took
a quantum leap in the human direction. It was the first hominin
species to leave Africa, expanding into a wide range of habitats in
Asia and Europe (13). It was also the first hominin to have long legs
and short arms – limb proportions similar to those of modern humans
(13). Homo erectus possessed a significantly larger brain (on average)
118 march of the bipeds: the later years

than Homo habilis (13), had a larger body (253), made more sophisticated
stone tools, incorporated more vertebrate meat into its diet (13), and may
have been the first hominin to control fire (254–256). But Homo erectus
was not fully modern: its brain size was on average smaller than that of
modern humans and was housed in a distinctive cranium with large
brow ridges, receding frontal bones and an angled occipital region.
Dentally, Homo erectus comes closer to modern humans than do
previous hominins. The largest sample of Homo erectus teeth ever
recovered from a single location is from Zhoukoudian cave near
Beijing, China (15). This is the cave where the first Chinese Homo
erectus was discovered, at the time named “Sinanthropus pekininsis”
or “Peking Man.” (Unfortunately nearly all of the original fossils were
lost just before the outbreak of World War II.) The very first Homo
erectus fossils were discovered prior to the Peking Man discovery, on
the island of Java (hence “Java Man”) by anatomist/physician Eugene
Dubois in 1891. Dubois assigned these fossils to a species he named
“Pithecanthropus erectus.” It was not until 1950 that that these two
species were recognized as having such strong similarity that they were
subsumed into the species known today as “Homo erectus” (257).
A single well-preserved lower left molar has a special place of
honor in the discovery of “Peking Man.” It was the human-like mor-
phology of this molar that led anatomist Davidson Black to name
a new species of ancient hominin (258). On his lecture tour through
America and Europe during 1927–1928, Black reportedly carried this
precious molar in a small gold receptacle that hung from his watch
chain (13). Christening a new species on the basis of this single tooth
was controversial. Yet, subsequent excavations at Zhoukoudian cave
revealed a treasure trove of fossils (including several skull caps) repre-
senting 40–45 individuals (13) that supported Davidson Black’s inter-
pretation: he and his coworkers had indeed discovered an extinct
hominin species from China.
In 1933, Davidson Black (259) described the teeth of Homo
erectus from Zhoukoudian cave in magnificent detail. One of his
observations was that, as in modern humans, the first molar is the
 homo erectus and homo antecessor 119

largest tooth of the molar series and the third is smallest and often
much reduced in size. That is generally not the case in earlier homi-
nins (15), though molar size relationships are somewhat variable in
earlier Homo. The complete lack of third molar formation – called
“third molar agenesis”– occurs with high frequency in some modern
human populations (260). The earliest known case of third molar
agenesis in human evolution also appears in Chinese Homo erectus –
in a 600,000-year-old specimen found near Lantian (261).
Overall, the premolars and molars of Zhoukoudian Homo erec-
tus are smaller than those of Australopithecus and Homo habilis (15).
A prominent and distinctive feature of the upper incisors is that they
are shovel-shaped in having raised ridges along their edges (on the
lingual side of the tooth) together with a bulbous “eminence” at their
base (Figure 5.1). Shovel-shaped incisors similar to these are found in
living indigenous Chinese (262–264). Black further observed that simi-
lar to Neanderthals and unlike most living humans, the Zhoukoudian
teeth had enlarged pulp cavities with roots that separated at a greater
distance from the tooth crown. Such teeth are termed taurodont,
literally meaning “bull-like teeth” (see Figure 5.2 showing
a taurodont Neanderthal molar) (265). Taurodont roots may have had
an adaptive function in prolonging the life of teeth subjected to high
rates of wear (265). As wear progressed, the exposed pulp would pro-
duce additional dentine which would serve as a chewing surface.
The division between the roots would not be reached in a taurodont
tooth until wear became extreme (265).
Homo erectus spanned a huge geographic range and time period.
The earliest appearing Homo erectus specimens date to about
1.8 million years ago and are from East Africa, the site of Dmanisi
Georgia, and the island of Java (15). The species appears to have
persisted in Java to as late as 100,000 years ago and possibly less than
50,000 years ago (266). With such a wide distribution through space
and time, Homo erectus was quite variable in form, resulting in
numerous attempts to divide the genus into different species
(reviewed in [253]). Recent interpretations and fossil finds, however,
120 march of the bipeds: the later years

figure 5.1: High fidelity casts of two shovel-shaped incisors of Homo

erectus from Zhoukoudian Cave, China. There are two specimens shown
in different views. Specimen 1 is shown in occlusal view in 1O, in lingual
view in 1Li and in labial view in 1La. Specimen 2 is shown in occlusal
view in 2O, in lingual view in 2Li and in labial view in 2La. Images
courtesy of Song Xing, of the Institute of Vertebrate Paleontology and
Paleoanthropology in Beijing.
 homo erectus and homo antecessor 121

figure 5.2: Neanderthal first molar (left) compared to that of a modern

human (right). Drawing by Alyssa Starrett is based on a synchrotron micro
CT image of these teeth (Figure 5 in Macchiarelli et al., 2006). The enamel
cap has been made transparent to show the shape of the enamel-dentine
junction. Note the taurodont roots of the Neanderthal tooth (see text).
Adapted by permission from Macmillan Publishers Ltd: Nature:
Macchiarelli R, Bondioli L, Debenath A, Mazurier A, Tournepiche J-F,
Birch W, et al. How Neanderthal molar teeth grew. Nature. 2006;444:
748–751.

suggest that these geographic and temporal variants can reasonably be

lumped into the single species, Homo erectus (267).
The early 1.8 MY Homo erectus sample from Dmanisi, Georgia
offers a thought-provoking example of variation from a single site.
To date, five skulls have been recovered in a great range of shapes and
sizes that span the variation present in African H. erectus, H. habilis,
and H. rudolfensis (268). Four of these skulls are illustrated in
Figure 5.3. Such great variation from one location may suggest that
many of the specimens currently allocated to all three of these species
could be part of a single variable one, although (of course) not all
paleoanthropologists agree with this interpretation (177).
The Dmanisi fossils are also fascinating because they include
specimens with small cranial capacities in the range of Homo habilis,
but with several Homo erectus-like features including modern limb
proportions, well-developed brow ridges, and progressive reduction in
size from the first through third molars (269). Their small cranial
figure 5.3: Four of the skulls from Dmanisi redrawn by Alyssa Starrett from Figure 2 in Lordkipanidze David, Ponce de León
Marcia S., Margvelashvili Ann, Rak Yoel, Rightmire G. Philip, Vekua Abesalom, Zollikofer Christoph P.E. A complete skull from
Dmanisi, Georgia, and the evolutionary biology of Early Homo. Science. 18 OCTOBER 2013;342:328. Reprinted with permission
from AAAS.
 homo heidelbergensis 123

capacities overturned a long-held assumption that brains sizes beyond

the Homo habilis range, as Homo erectus from Java and China possessed,
were necessary for hominins to leave Africa and expand into new, less
hospitable climes. The Dmanisi hominins’ smaller brain sizes link them
to earlier African Homo. Dentally, they are similar to early East African
Homo erectus in their molar size and morphology, the more narrow
shape of their dental arcades, and their single-rooted upper premolars
(269). Modern humans often have two-rooted upper premolars (74).
Whether Homo erectus was present in Western Europe is unclear.
The earliest occupants there, having a combination of Homo erectus
and modern human features, have been placed in their own species:
Homo antecessor (270). They appear for the first time 1.2–1.1 million
years ago in Spain (271). The largest sample of this species is from an
800,000 year old site called Gran Dolina, where over a hundred fossils
have been recovered (272). These specimens have brow ridges and
cranial capacities in the Homo erectus range, but faces that are modern
in possessing a canine fossa: a sunken area above the canine tooth that
does not appear in Neanderthals because of the projecting faces of the
latter. The teeth retain some primitive morphological features and
appear to be more similar in size to those of African early Homo than
they are to European Middle Pleistocene hominins (273).
Homo antecessor brings us to the Middle and Late Pleistocene,
geologic time periods from approximately 781–126,000 years ago and
from 126–12,000 years ago, respectively. During this latest stage of
human evolution, there was continued regional diversification across
the continents of Africa, Asia, and Europe. But, mounting evidence
from DNA studies suggests that diverse lineages – Neanderthals,
Denisovans, and anatomically modern humans – may have retained
enough similarity to have interbred and exchanged genes, as described
below.

homo heidelbergensis
In the fossil-rich Mauer sandpit near Heidelberg, Germany a massive
jaw with disproportionately smaller teeth came to light in 1907.
124 march of the bipeds: the later years

One year later, a new species was named: Homo heidelbergensis

(274). While not catching on at first, the name has come to refer to
comparably aged European, African, and possibly Asian forms (274)
that had expanded crania relative to Homo erectus with
a less-angulated occipital region (among other cranial differences).
Along with its bigger brain, Homo heidelbergensis exhibited some
new behaviors, constructing shelters (on the beaches of the French
Riviera no less) and fashioning wooden spears (15). Spears and the
remains of large mammals at various sites suggest that Homo hei-
delbergensis was a formidable hunter.
While some authorities include middle Pleistocene Asian
hominins in the species Homo heidelbergensis (15, 275), others
limit the species to middle-Pleistocene African and European
forms, and view the Asian forms as later Homo erectus (276).
Dentally, like Homo erectus, Homo heidelbergensis had taurodont
teeth. But different from earlier species, Homo heidelbergensis
tended to have smaller posterior teeth (premolars and molars) and
larger anterior teeth (incisors and canines) (13, 275, 277).
Hypothesized selection pressures, some acting to reduce the size of
posterior teeth and others to increase the size of anterior teeth in
Homo heidelbergensis are discussed in relation to Neanderthals in
Chapter 8. In addition to being smaller, Homo heidelbergensis
molars also tended to be simpler, with a reduced number of cusps
(13). There are a number of other distinctive dental traits in Homo
heidelbergensis, including long anterior tooth roots, asymmetry of
the first lower premolar and “swelling” of the buccal face (side facing
the cheek) of the molars (275).
Generalizations about Homo heidelbergensis belie the diversity
of this species, which shows extensive variation in cranial, facial, and
dental form (15). Dentally there seems to be a divide between Asian
and African Homo heidelbergensis on the one hand and European
Homo heidelbergensis on the other (275). For example, a derived
reduction and simplification of the posterior teeth was more apparent
in European than Asian and African Homo heidelbergensis (275).
 homo heidelbergensis 125

European forms also had lower second premolars that were not
“molarized,” as were those of African and Asian contemporaries
(275). In the Jinniu Shan cranium from China, traits such as prominent
cheekbones, a broad nasal bridge, a form of incisor shoveling similar to
that of the Zhoukoudian teeth (13), seem to be derived in the direction
of modern people of Chinese descent.
By contrast, in Europe, especially from a site in the Atapuerca
mountains of Spain called “Sima de Los Huesos,” (translated “Pit of
Bones”), dated to 430,000 years ago (278) Homo heidelbergensis has
strong cranial, facial, and dental similarities to the Neanderthals that
succeed them in the European fossil record. The “pit” is a cave
chamber that lies at the bottom of a 43-foot-long natural shaft. From
this pit 6,500 hominin fossils from twenty-eight or more individuals
have now been recovered (278), along with the remains of cave bears.
How so many bones ended up at the bottom of this shaft is a mystery.
It’s possible these hominins disposed of their dead by dropping them
down the shaft, creating a bonanza for future paleoanthropologists
(278). This is the largest sample of Middle-Pleistocene hominin
remains from a single site ever found (272).
In the summer of 2014, Juan Luis Arsuaga and colleagues
published a new analysis of these remains (278). They found that
the Sima de Los Huesos remains are different from other European
Homo heidelbergensis specimens and so derived in the direction of
Neanderthals that they should be considered to form the base of the
Neanderthal clade as the earliest members of that lineage. The Sima
de Los Huesos hominins do not share all the derived traits of later
Neanderthals, although they appear to be dentally nearly identical
to them (see below for description of Neanderthal dental morphol-
ogy). The divergence of Neanderthals and modern humans has been
estimated at more than 500 KYA based on analysis of Neanderthal
DNA (279, 280). Arsuaga and colleagues point out that including
these specimens dated to 430,000 years ago as part of a Neanderthal
clade is consistent with that evidence.
126 march of the bipeds: the later years

neanderthals, anatomically modern homo sapiens

(amhs), denisovans, and homo floresiensis
Although remains now recognized as Neanderthal had been found as
early as 1829, Neanderthals are named for the remains of an individual
unearthed in 1856 from a quarry in the Neander Valley, Germany (281).
“Neanderthal” literally means “Neander Valley,” with the alternative
spelling, “Neandertal,” reflecting later revisions to the German lan-
guage (281). The bones of the skeleton were robust and the skull had
a peculiar shape: with heavy browridges, a receding forehead and low
cranial vault. In 1856, Charles Darwin’s paradigm-changing “Origin of
Species by Means of Natural Selection” was still three years away from
publication. Thinking outside of an evolutionary framework, the ana-
tomists who initially analyzed the remains thought they might repre-
sent a pathological individual, a member of an ancient barbaric tribe, or
even a horseback-riding deserter from the invading Cossack army (this
last interpretation based on the bowed thigh bones of the remains) (281).
Over the next decade, such ideas gave way to the view, bolstered by
additional Neanderthal finds, that these remains represented an
entirely new species. In 1864, paleontologist William King christened
them Homo neanderthalensis.2 But whether Neanderthals are viewed
as species separate from modern humans has vacillated throughout the
history of paleoanthropology and is a matter of continued debate today.
If one considers the Sima de los Huesos hominins to be
Neanderthals, then Neanderthals appear in the fossil record as early
as 430,000 years ago. After this time, morphological characteristics
typical of Neanderthals accrete gradually, until by 200,000 to 150,000
years ago, fossils are found in Europe with the complete package of
Neanderthal features (15). For the crania, these features include such
distinctive characteristics as double-arched brow-ridges, long and low
cranial vaults, occipital buns (protruding areas at the back of the

2
Homo neanderthalensis took priority over the name zoologist Ernst Haeckle proposed
for Neanderthals in 1866: Homo stupidus. (282). Wolpoff MH, Caspari R. Race and
Human Evolution: Simon and Schuster; 1997.
 homo sapiens (amhs), denisovans, and homo floresiensis 127

figure 5.4: Artist’s rendition of Qafzeh 9 (left) vs. Amud crania (right).
Qafzeh 9 is an anatomically modern human dated to approximately
90,000 years ago, from Qafzeh cave in Israel. Amud is a Neanderthal from
a cave on the wall of Wadi Amud, Israel, dated to approximately 60,000
years ago. Note the differences in cranial and facial form. Drawn by Alyssa
Starrett.

cranium), and projecting midfaces with large nasal apertures

(Figure 5.4). With their prognathic faces, Neanderthals lacked canine
fossae and had had tooth rows that had shifted forward, creating
a retromolar space, a space behind the third molar and the mandible’s
ascending ramus (Figure 5.5). In their post crania, Neanderthals were

figure 5.5: Artist’s rendition of Qafzeh (left) vs. Amud mandibles

(right). Retromolar spaces on Amud mandible are noted with arrows.
Drawn by Alyssa Starrett.
128 march of the bipeds: the later years

figure 5.6: Artist’s rendition of Neanderthal upper incisors in incisal

view. Note strong labial curvature and large tubercle at base of crown.
Drawn by Alyssa Starrett.

highly robust, with large and wide rib cages and pelves, and
thick-walled limb bones. Given these distinctive features, it is not
too hard to see why William King considered Neanderthals to be
a species apart from modern humans.
Dentally, Neanderthals were also quite distinctive. Their incisors
are generally quite large by modern standards and have long roots
(though their incisors reduced in size over time (283). Their incisors
also have a distinctive shovel-shape form that differs from that of
Homo erectus and modern Asian populations. The Neanderthal version
of the shovel-shaped incisor involves a very large tubercle at the base of
the tooth and strong labial curvature (Figure 5.6) (15, 284, 285).
The size and morphology of the anterior teeth have been seen, by
some, as evolutionary adaptations to resist heavy wear on these teeth
from their use as “third hands” or from diets high in abrasives (e.g.,
(286, 287). Many Neanderthal teeth show heavy anterior tooth wear
(Figure 5.7).
Anna Clement and colleagues (288) recently argued that the
Arctic Inuit, who subject their anterior teeth to high loads, such as
in processing animal hides, exhibit even higher rates of wear than do
Neanderthals but have smaller and less well-buttressed anterior teeth.
On this basis, Clement and colleagues reasoned that these features of
Neanderthal anterior teeth are not likely to represent adaptations to
excessive wear. Perhaps the size and buttressing of Neanderthal
anterior teeth represents an adaptation to tooth fracture under high
 homo sapiens (amhs), denisovans, and homo floresiensis 129

figure 5.7: Artist’s rendition of the extremely worn anterior teeth of the
La Ferrassie I Neanderthal. Drawn by Alyssa Starrett.

loads. But, this idea has been questioned as well, based upon estimates
of the bite force capacity of Neanderthals, which is smaller (289) or
comparable to that of recent and living humans (290).
Thus, the idea that the distinctive size and buttressing of
Neanderthal anterior teeth are adaptations to either excessive wear
or high loads is weakened by these studies. Regardless of the potential
adaptive significance of Neanderthal anterior tooth morphology, an
interesting behavioral question is what Neanderthals were actually
doing with their teeth, a topic taken up in Chapter 8.
Neanderthal lower second premolars are also different from
those of modern humans in that they have an asymmetric outline
(285). Neanderthal molars, though smaller than those of preceding
Homo species and within the modern human range of variation,
appear to be morphologically distinct from those of modern humans
in having cusps that are more closely spaced to one another, different
relative sizes of two of their principal upper molar cusps and in having
a crest (the mid-trigonid crest) connecting two of their principal lower
molar cusps (291). Their lower molars are also taurodont (Figure 5.2)
(292). Some of these traits occur in earlier Homo as well as in pene-
contemporary non-Neanderthal hominins from China (e.g., in the
early Late Pleistocene Xujiayao hominins of Northern China (293).
What makes Neanderthals dentally derived is not the presence of
these traits, which are in most cases primitive features of earlier
hominins, but the combination of these traits in high frequency (293).
130 march of the bipeds: the later years

As Neanderthals were the first hominins known to bury their

dead (15), they are better represented in the fossil record than any
previous hominin. But besides their bones and teeth, Neanderthals
left a rich archaeological record that has enabled inferences into their
behavior and culture. Neanderthal tools were of the Mousterian vari-
ety (named after a site in France called Le Moustier), consisting pri-
marily of stone flakes removed from a prepared core and fashioned
into such forms as “sidescrapers,” “points,” and “flake-blades” (15).
Some of these tools have use-wear that indicates their use on animal
hides, in turn suggesting the possibility that Neanderthals made
clothing (15). Neanderthals left widespread evidence of building
hearths, but not much evidence of building shelters, nor of artwork
(15). They do appear, however, to have been capable of symbolic
expression, as evidenced by a more than 39,000-year-old engraving
from Gibraltar cave (294).
Toward the end of the Neanderthals’ tenure in Europe ending
around 33,000 years ago, Neanderthal remains are associated with
more sophisticated technology and further artistic expression (15).
Neanderthals from 34,000-year-old site of Arcy-sur-Cure in France
had a well-developed bone and ivory industry that included grooved
animal teeth and ivory rings that appear to have been items of “perso-
nal adornment” (295). Finely worked bone and works of artistic
expression are common at the sites of anatomically modern humans
who inhabited Europe as early as 45,000 years ago (296). Whether late-
surviving Neanderthals developed these cultural advances indepen-
dently or borrowed them from their anatomically modern human
contemporaries is not clear (295, 297).
The anatomically modern humans who appeared in Europe at
this time had much earlier roots in Africa. Fossils considered to be
anatomically modern date back to 195,000 years ago from southern
Ethiopia (298). Other early anatomically modern remains are found at
diverse locations in Africa, including in South Africa and Morocco
(15). So, modern looking forms were present in Africa when
Neanderthals occupied Europe.
 homo sapiens (amhs), denisovans, and homo floresiensis 131

To be anatomically modern means to have a suite of derived

features. In the skull, this includes a cranial vault that is short from
front to back but tall, with a high forehead. It also includes a cranium
that is rounded at the back, the presence of a canine fossa (associated
with a midface that is not projecting), and a chin (15). Post cranially,
anatomically modern humans tend to have less robust limb bones
than did previous hominins, but these differences are not absolute;
they are a matter of degree (15).
But, “What does it mean to be dentally modern?” Entitling
a book chapter with this very question, Shara Bailey and
Jean-Jacques Hublin (299) argued that there is such wide variation in
modern human dental morphology that it is not possible to list traits
that all modern humans share. On the other hand, it does appear that
there are a variety of dental features that are present in some modern
human populations but are either not present or are much lower in
frequency in earlier hominins. These traits include flat (not curved)
incisors with no shoveling, lower second premolars that are dentally
simplified and more symmetrical in outline, upper second molars
with three cusps (rather than four), and lower first and second molars
that have four cusps (rather than five). Overall, in some populations,
modern human teeth became not only smaller but also morphologi-
cally simpler.
The hominin world of the middle-late Pleistocene became
a little more crowded in 2010, with the discovery of the Denisovan
hominins (300). These hominins were first identified on the basis of
DNA extracted from a finger bone and an upper second or third molar
(approximately 50–30,000 years old) recovered from Denisova Cave in
southern Siberia. Denisovans are the first hominins to be identified on
the basis of their DNA rather than on the morphology of their fossil
remains, which are meager. But the third molar plays an important
supporting role in the Denisovan drama.
DNA analysis suggests that Denisovans were distinct from
Neanderthals but shared a more recent common ancestor with them
than with modern humans. Neanderthal and Denisovan nuclear DNA
132 march of the bipeds: the later years

sequences, diverged, on average, some 640,000 years ago (300).

Neanderthal and Denisovan nuclear genomes on average, diverged
approximately 800,000 years ago (300). Here is where the Denisovan
upper molar comes in: it supports the distinction of Denisovans from
both Neanderthals and modern humans. The molar is huge. It is not
clear if it is a second or third molar. If a third molar, it is comparable in
size to those of early Homo and Australopithecus (300). If a second
molar, it is nevertheless larger than those of most Neanderthals and
early modern humans. Some details of the upper molar’s morphology
also differ from those of Neanderthals’ (300).
Last and also least – only in terms of size – is the tiny hominin
species from the Indonesian island of Flores, Homo floresiensis,
nicknamed the “Hobbit.” The hominin remains from this site indicate
a species that stood three feet tall with a cranial capacity equivalent to
that of Australopithecus afarensis but appearing very recently in
time – from 100,000 to 17,000 years ago (301, 302). The announcement
in 2004 of such a recent primitive species of hominin sent shock waves
through the paleoanthropological world and was predictably met with
skepticism among experts in the field. Many alternative explanations
were offered, some suggesting that the most complete specimen from
the site, LB1, simply belonged to a modern human with a pathological
condition. One such condition, Laron syndrome, entails a genetic
insensitivity to growth hormone and was asserted to have possibly
caused the Hobbit’s small brain and body size (303).
As paleoanthropologist Leslie Aiello (304) observed, however,
none of the pathological explanations accounts for the full set of
features exhibited by the Hobbit. These include lower first premolars
which were elongated and asymmetric, with large buccal cusps (305).
Plotting a shape index of the lower first premolar against that of
modern humans, and earlier hominins, Brown and Maeda (305)
found that the shape of the Homo floresiensis lower first premolar
falls outside the range of modern human variation but well within
that of early australopiths and early Homo. Coupled with these dental
finding are those of Debbie Argue’s (306) cladistic analysis in which
 origins of modern humans and issues of phylogeny 133

Homo floresiensis does not form a clade with Asian Homo erectus,
and branches off just before or after Homo habilis.
The teeth and cladistic analysis challenge the view that the
diminutive Homo floresiensis is a scaled down version of Homo
erectus. According to that view, Homo floresiensis is a product of
“insular dwarfism,” a reduction in size thought to occur in some island
habitats over many generations through natural selection. The lower
energy requirements of a small body size are thought to give animals an
advantage in survival and reproduction when island food resources
periodically dwindle. But, if Homo floresiensis is cladistically closer
to Homo habilis, then it may have been very small to begin with.
Instead of being a dwarfed version of Asian Homo erectus, it may be
a late-surviving descendant of an early migration out of Africa of
a small-bodied, smaller-brained hominin (307). Unfortunately, analyses
of teeth haven’t settled the issue, as a recent study of cranial shape allies
Homo floresiensis with Homo erectus (308). Why the teeth and cra-
nium give different signals is not clear and begs for explanation.

origins of modern humans and issues of phylogeny

within the genus homo
Ideas about relationships among fossil species of the genus Homo and
modern humans have traditionally fallen into three major camps.
The “Multiregional Continuity” camp holds that modern humans
gradually evolved from more archaic forms (Homo erectus in some
regions, Homo heidelbergensis or Neanderthals in others) that were
all in reality part of one global, interbreeding species (309, 310).
Proponents of this camp point to local continuity in a variety of
regionally anatomical features visible in both archaic and modern
humans in particular regions of the world. One of those features is
something noted earlier: shovel-shaped incisors occur in high
frequency in Chinese Homo erectus, Chinese Homo heidelbergensis
and Chinese modern humans (309), suggesting the continuity of genes
from ancient to modern populations within the region. This view does
not imply parallel evolution of populations (311), but instead suggests
134 march of the bipeds: the later years

that populations throughout the world that were linked by gene

exchange gradually evolved toward modern form.
At the other extreme is the “Recent African Origin” camp,
which holds that anatomically modern humans speciated from
African Homo heidelbergensis in Africa. They then expanded into
other parts of the world, and over time completely replaced more
archaic forms. A critical piece of evidence in support of this view has
to do with DNA variation in modern humans. Both mitochondrial3
(312, 313) and nuclear DNA analysis (313) suggest that the most
genetically diverse peoples today are in Africa. Assuming that muta-
tions in DNA are generally neutral with respect to natural selection
and accumulate largely as a function of time, the higher diversity of
African peoples than in other regions of the world suggests that AMHS
from Africa have a longer history, i.e., they are older, than AMHS in
other regions of the world.
Another point going for the Recent African Origins model is that
the earliest fossil evidence of anatomically modern humans, comes, as
previously noted, from Africa, dating to nearly 200,000 years ago (298).
DNA analyses suggest age ranges for the origin of AMHS that include
this date (312, 314). Dates and patterns of AMHS dispersal out of
Africa are controversial. Some studies suggest expansion out of
Africa around 50–60,000 years ago (315, 316) and others (317) find
evidence of an initial dispersal of anatomically modern humans into
Asia around 130,000 years ago, with a second dispersal into Eurasia
around 50,000 years ago.
It is possible that African populations may be more variable
genetically simply because they have been larger than other AMHS
populations throughout history, not because they are older (318).

3
Mitochondria are tiny structures within cells that break down sugar molecules into
small packets of usable energy. The DNA contained in mitchonrdria represents an
extremely small portion of our total genome, the vast majority of which is enclosed
within the nuclei of our cells. Nevertheless, because there are thousands of mitochon-
dria in each cell and only one nucleus, mtDNA is more easily obtained from ancient
bone than is nuclear DNA. Each of us inherits the mtDNA that resided in our mother’s
egg cells, so these genes are passed down the maternal line.
 origins of modern humans and issues of phylogeny 135

But, this explanation does not account for the apparent patterning
of genetic diversity across the globe: genetic diversity decreases
with greater distance from Africa (319). This pattern suggests that
as people moved out of Africa they carried only a fraction of the
original diversity present in Africa into new areas. As they moved
from these new areas into still more distant regions, they then
seem to have carried an even smaller fraction of that genetic
diversity with them.
The third camp falls in between these two extremes. One view
is that there was genetic continuity in some areas outside of Africa,
but not all. Another is that anatomically modern humans originated
in Africa but interbred successfully to varying degrees with more
archaic hominins when they encountered them (320). Alan
Templeton’s (320) analysis of modern human DNA variation sup-
ports this view. Templeton analyzed variation in twelve modern
human haplotypes (groups of linked genes) using a statistical method
that allowed him to assess the extent and direction of gene flow
during human evolution. His results showed that variation in the
human genome bears the stamp of three major migrations out of
Africa: one at 1.7 Ma, a second around 0.42–0.84 Ma, and third
around 0.08–0.15 Ma. The last of these corresponds to the dispersal
of anatomically modern Homo sapiens. His analysis indicates that
AMHS from Africa interbred with, but did not replace more archaic
forms.
Some years after Templeton’s study, studies of ancient DNA
from Neanderthals and Denisovans likewise pointed to interbreeding
with AMHS. By 2010, researchers had sequenced much of the
Neanderthal nuclear genome (279). Geneticist Richard Green and
colleagues estimated that 1–4 per cent of the DNA of some living
people (non-Africans) came from Neanderthals (279) (but see [321]
for an alternative interpretation of the evidence). Denisovans appear
to have contributed a small portion of DNA to modern Melanesians
and aboriginal Australians (300) as well as to mainland Asians and
Native Americans (322).
136 march of the bipeds: the later years

Recently, mitochondrial DNA from the Sima de los Huesos

Homo heidelbergensis fossils has been analyzed (323). Oddly, analysis
of their mitochondrial DNA places them closer to Denisovans than to
Neanderthals. This is hard to understand because, as noted earlier, the
Sima de los Huesos hominins are morphologically very similar to
Neanderthals. The Sima de los Huesos molars, in particular are
much more similar to those of Neanderthals than to the Denisovan
molars. However, mtDNA represents a small portion of the genome
that is inherited maternally and so it may not provide as clear a picture
of Sima de los Huesos affinities as dental morphology does or
autosomal DNA would.
Analysis of variation in modern and ancient DNA is greatly
advancing our understanding of modern human origins. Yet, when
ancient DNA cannot be recovered, morphological analyses remain
the only way to address questions of phylogeny within the genus
Homo. Teeth, once again, provide a useful tool. As will be explained
in Chapter 8, they have been useful in investigating the question of
who might be the last common ancestor of Neanderthals and modern
humans and as discussed in Chapter 9, they provide insight into
modern human origins and dispersal out of Africa.
This chapter marched its way through evolution within the
genus Homo. Broad trends over time within the genus include
expanding brain size, greater reliance on meat in the diet, and growing
use and improvement of cultural solutions to problems of survival and
reproduction. In this second part of the book, how teeth reflect and
respond to these trends begins once again with the fundamental
adaptation of diet.
6 Dentally-Derived Dietary
Inferences: The Genus Homo
and Its Diminishing Dentition

It is not much what is eaten but what is done to it beforehand.

– Brace CL
Krapina, “Classic Neanderthals,” and the Evolution of the European
Face

Chapter 4 left off on evidence of dietary divergence between

Paranthropus and early Homo, evidence that lends support to
Robinson’s Dietary Hypothesis. The present chapter considers how
dental evidence contributes to our understanding of dietary change
within the genus Homo, prior to the evolution of Neanderthals and
anatomically modern humans (AMHS). During this period of human
evolution, archaeological evidence becomes a crucial source of
information for dietary reconstruction. Faunal remains with evi-
dence of human alteration (e.g., butchery), stone tools and eventually
evidence of controlled use of fire supply crucial pieces of the dietary
puzzle in the Homo lineage. But teeth, too, yield important clues.
This chapter focuses on those clues within their archaeological
context.
In addition, this chapter reviews evidence and explores argu-
ments for the possibility that changes in culture – the use of tools
and fire – had an effect on dental evolution in Homo habilis, Homo
erectus, and Homo heidelbergensis. While a major reduction in the
size of the canine apparently occurred at or near the base of the
hominin clade (Chapter 3), posterior teeth did not reduce until much
later, arguably not until the appearance of Homo erectus (251, 324).
There were also changes in anterior teeth. Relative to estimated body
size, incisor teeth are larger in Homo habilis than they are in any
australopith, but then decrease in size with Homo erectus (325).

137
138 dentally-derived dietary inferences

The big question is why posterior teeth (and later anterior teeth)
reduced in size in the first place. Anthropological legend C. Loring
Brace1 and colleagues found that major reductions in tooth size
during the Pleistocene occurred relatively recently, during the last
200,000–300,000 years (commentary in Current Anthropology on
Wrangham and colleagues’ cooking hypothesis [52]). Brace argued
that the degree of dental reduction in different regions of the world is
proportional to the length of time people have been cooking in these
regions (326). Cooking would have had the effect of softening food and
thus relaxing the selection pressure on maintaining large teeth to
process hard and/or tough foods. Such changes in food preparation
are what Brace referred to in the aphorism that heads this chapter.
But, what is the nature of the evidence that cooking, as Wrangham and
colleagues (52, 57) argue, wrought a decrease in human tooth size
much earlier than this, at the time of Homo erectus? More generally,
what are some of the more plausible ideas for the causes and conse-
quences of dental reduction during this period of human evolution?
Toward the dual goals of this chapter–reviewing the dental
evidence for diet in the genus Homo as well as delving into hypotheses
for and consequences of dental reduction–we first examine the
archaeological record with respect to the antiquity of meat-eating
and the controlled use of fire.

a brief archaeological context

There is ample archaeological evidence of meat-eating in the Homo
lineage. What is less clear from the archaeological record, however, is
the quantity of meat incorporated into the diets of different species
and the primary means by which it was procured. The clearest
evidence for meat-eating in the early archaeological record comes
1
C. Loring Brace is an American anthropologist whose work showed that physical
features could not be used to define racial types and was an outspoken critic of the
race concept. His book “’Race’ is a Four Letter-Word’” is widely acclaimed and his
many influential contributions to physical anthropology, including his ideas on dental
reduction, were honored by the American Association of Physical Anthropology in
2006 with its prestigious Charles Darwin Lifetime Achievement Award.
 a brief archaeological context 139

from butchery marks on fossilized animal bones (327). Cut marks

made by flake tools leave distinctive marks that can be differentiated
microscopically from other markings on bone. It is possible to also see
evidence of percussion marks on bones, created when stone tools are
used to smash bones to remove their marrow (327).
The earliest widely accepted2 evidence of cut-marked bone is
from the 2.6-million-year-old site of Gona, Ethiopia (328). The first
Oldowan tools appear at about this time as well (327). Who made these
early tools and butchery marks is not clear (327), as several hominin
species existed at this time. Archaeologist Briana Pobiner (327)
considers Australopithecus garhi, and especially Homo habilis to be
the most likely culprits.
In the 1980s, archaeologist Pat Shipman (329–331) produced com-
pelling evidence that the majority of the cut marks on animal bones
dating to about 2 Ma from Olduvai Gorge were superimposed on marks
made by carnivore teeth. Hominins were primarily gaining access to
these bones after carnivores had had their fill–in other words, hominins
were scavenging this meat, not hunting it, as anthropologists pre-
viously assumed. The implication was that these hominins had entered
a new niche, as scavenging does not occur in modern chimpanzees and
presumably did not occur in our last common ancestor.
Scavenging, according to some, may have been hominins’ first
step into a meat-eating niche (commentary in Current Anthropology
on Wrangham and colleagues’ cooking hypothesis [52]). Recent evi-
dence, however, seems to push the antiquity of hunting as far back as 2
Ma (332). The evidence comes from the site of Kanjera, South Kenya
where there are abundant remains of whole small gazelle skeletons
with evidence of butchery and disarticulation, and with no evidence of
scavenging (332). Larger bovid remains were also found in the form of
leg bones and skulls that had been disarticulated and transported to

2
Recent evidence from East Africa may, however, push stone tools back to 3.3 million
years ago (the middle Pliocene). (31. Harmand S, Lewis JE, Feibel CS, Lepre CJ, Prat S,
Lenoble A, et al. 3.3-million-year-old stone tools from Lomekwi 3, West Turkana,
Kenya. Nature. 2015;521(7552):310–315.)
140 dentally-derived dietary inferences

the site. Percussion marks on the crania suggest these hominins were
eating fatty brains and marrow. Any carnivore tooth marks found on
these bones appear to have been made after the bones had been
butchered. The authors of this study, Ferraro and colleagues, suggest
that this is evidence that hominins were making more than occasional
use of meat in their diets, and may well have been hunting small game
at this time (332).
In his paleoanthropology blog of 29 April 29, 2013, Anthropologist
John Hawks characterized that question of scavenging versus hunting as
the “. . . tiredest chestnut in the anthropologists’ Oldowan arsenal.” He
argues that hominins from Oldowan sites probably did both. At Homo
erectus Acheuleian sites, stone tools became more varied and animal
bones more prevalent (15). The archaeological evidence therefore indi-
cates that meat, however acquired, was increasingly incorporated into
the diet of Homo species during the Paleolithic. Diets were adaptable, as
well, judging from the finding of freshwater shellfish remains beside the
bones of Homo erectus in Trinil, Java (333). By Homo heidelbergensis
times archaeological evidence in the form of spears and large mammal
remains strongly suggest that the quest for meat had progressed to
big-game hunting (15).
Of course, because plant foods decompose quickly, the
archaeological record is biased against finding evidence of them.
And, it is plant foods, particularly cooked plant foods, that form the
basis of the Cooking Hypothesis. When Wrangham and colleagues
introduced this hypothesis in Current Anthropology in 1999, they
argued that cooking began in earnest in Homo erectus (52). Part of
their argument rested on the marked reduction in tooth size paired
with the increase in brain and body size that occurred with the
evolution of Homo erectus. These changes, in their view, “signaled”
that humans were chewing softer, cooked foods (teeth became
smaller) that improved their energy intake (body and brain size were
able to increase). The actual archaeological evidence of cooking in
Homo erectus times, as commentators noted and as Wrangham and
colleagues openly acknowledged, was meager.
 a brief archaeological context 141

Wrangham and colleagues relied on evidence of 1.6-million-

year-old “reddened patches” at Koobi Fora in east Africa that had
been interpreted as hearths. They also cited evidence of burned
bones found together with hominin artifacts from Swartrkans
from around one million years ago (52). In his commentary,
Brace questioned this evidence. As he put it: “Fire happens!”
Whether the presence of fire at these sites indicates controlled
use of fire rather than a naturally occurring one is not clear.
Brace argued that the first “documented appearance of cooking”
occurs much later in the archaeological record, around 200–300
KYA. Wrangham and colleagues responded that the kinds of fires
that modern hunter-gatherers use to cook underground storage
organs (tubers) are “ephemeral” and may not leave an archaeolo-
gical record. In other words, absence of evidence is not evidence of
absence.
Since the publication of Wrangham and colleagues’ seminal
paper, new evidence pushes the controlled use of fire further back
in time–to 1 million years ago. The evidence comes from
Wonderwerk Cave, South Africa. A large quantity of burned bone
and the ashy remains of plants were recovered from within this
cave (256). In total, 675 burned bones or teeth were analyzed with
a method called Fourier transform infrared microspectroscopy,
enabling these researchers to determine the temperature to which
the material had been heated. That temperature is consistent with
a fire made with grasses and twigs. It is not likely that wildfire
produced the ashes and burnt bone, because they are found a fair
distance beyond the entrance of the cave. At another site, Gesher
Benot Ya’akov Israel – dated to some 800,000 years ago, clusters of
burned bones and charred wood suggest the presence of hearth fire
(255). In short, it now seems much more likely than it did in 1999
that Homo erectus had the ability to control fire.
With these archaeological points about diet and fire use in mind,
it is now time to turn to the dental evidence.
142 dentally-derived dietary inferences

dental evidence
In his 2012 review of dental evidence for diet in African early Homo
(325), Peter Ungar states: “The most obvious conclusion we can draw
from a review of the fossil evidence for diet in early African Homo is
that there is not much of it, and what we do have is not very compel-
ling” (2012:S325). As Ungar observes, the number of early Homo teeth
recovered is far fewer than it is for australopiths, limiting the power of
dental investigations into Homo diets.
Nevertheless, data on the chemical composition of enamel,
microwear, dental morphology, tooth chipping and tooth size
(especially in relation to bite force reconstruction) are accumulating
and are relatively congruent with one another. Altogether the dental
data are also fairly well-aligned with the archaeological record.
The dental evidence points to diets within the Homo lineage that
included meat, diverged from those of Paranthropus, were variable,
and, as compared to the diets of australopiths, had softer textures.
Consistency between microwear and chemical data on the one hand,
and certain aspects of tooth size and morphology on the other, seems
to denote that changing diets had begun to result in evolutionary
changes in teeth.
There is strong trace element support for meat-eating in early
Homo. Balter and colleagues’ (106) study of Sr/Ca and Ba/Ca ratios in
the teeth of south African early hominins (Chapter 2) revealed
a statistically significant mean difference between P. robustus and
early Homo with respect to both ratios. Means for both ratios were
lower in Homo than in P. robustus, indicating that there was more
meat in the diet of the former. The difference in means suggests
dietary divergence between these lineages, as Robinson envisioned.
There was not, however, complete separation in the ranges of trace
element values between the two groups of hominins, raising the
possibility of some dietary overlap between them.
Shifting the scene to East Africa, Cerling and coworkers’ (88)
study of carbon isotopes from the Turkana Basin hominins documents
 dental evidence 143

strong divergence in the consumption of C4 resources between early

Homo and Paranthropus by 2 million years ago. Average values for
their stable carbon isotope ratios indicate that the proportion of C4
resources in the Paranthropus boisei diet was 75% while that of its
Homo contemporaries was 35%. A strong isotopic divergence aligns
with the stark differences in the size of their facial buttressing, muscle
attachments, jaws and teeth as well as in the thickness of enamel (334)
of these two east African lineages. Antón and colleagues point out that
the difference in average carbon isotope values for Paranthropus
boisei and Homo erectus in East Africa at 2.8 ppm is close to the
average difference between Homo erectus and “non-erectus Homo”
at 2.9 ppm (177). This is interesting because, as they note, it suggests
the possibility of niche divergence within the genus Homo.
Aspects of tooth size and morphology also hint at increased meat
consumption in early Homo. Archaeologist Travis Pickering and
colleagues note that, when eating ribs, both humans and chimpanzees
hold the ribs in their hands while using their incisors to strip meat from
them and to “peel” back strips of bone (335). Tooth marks, butchery
marks, and evidence of such incisor bone “peeling” occur in fossilized
ungulate ribs dated to 1.2 MA from Olduvai Gorge (335). These authors
suggest that use of incisor teeth for this purpose may explain why the
anterior teeth of early Homo are broader (with wider incisal edges) than
those of its australopith ancestors (336). Perhaps these broader incisor
teeth were adapted to such uses as bone “peeling.” Peter Ungar’s (337)
work showed that in early Homo, molar chewing surfaces have greater
relief and cusps with steeper slopes than do those of Au. afarensis. This
finding may point to the ability of early Homo molars to shear through
tough foods, and one type of tough food is meat.
Microwear texture analysis points strongly to variability in the
diet of Homo erectus. In particular, the microwear complexity (see
Chapter 2) of Homo erectus teeth covers a wide range of values, greater
than that of any other Plio-Pleistocene hominin yet studied, with the
exception of Paranthropus robustus (325, 338). Both hard and tough
foods were likely present in Homo erectus diets, given that microwear
144 dentally-derived dietary inferences

analysis yields high complexity values (indicative of hard foods) as

well as small “adhesion pits” produced by the chewing of tough foods
(325, 338).
Ungar and coauthors in their 2006 review article (339) synthe-
size both dental and archaeological data on early Homo (Homo habilis
and Homo erectus) diets, emphasizing their “adaptive versatility.”
In their view, the mixed nature of the C3/C4 diets of these early
Homo species, their probable inclusion of both hard and tough food
items, and their ability to access high quality meat gave them the
dietary flexibility needed to meet the rapidly shifting environmental
conditions of the Plio-Pleistocene. These conditions encompassed
wide swings in temperature and moisture, as documented in the
East African paleoecological record (340). Ungar and colleagues’
conclusions support Rick Pott’s “Variability Selection Hypothesis”
for the evolution of Homo (340): the idea that environmental varia-
bility itself drove selection for flexibility in diet and behavior.
The size, and especially chewing area of posterior teeth
decreases from Homo habilis to Homo erectus, hinting at the
ingestion of softer – or softened– foods. Posterior tooth size in
Homo habilis appears to be similar to that of Au. africanus (247,
341). Yet, in relation to estimated body size the chewing area of the
postcanine teeth is smaller than that of any australopith, according
to an analysis by anthropologists Henry McHenry and Katie Coffing
(342). These researchers used an index of postcanine tooth area
relative to body size that paleoanthropologist Henry McHenry had
devised in an earlier paper. He called the index the “Megadontia
Quotient,” or MQ, and it is based on the positive relationship
between postcanine tooth area and body size in primates. This ratio
compares actual postcanine area to that predicted on the basis of
body size. MQs for modern humans and chimps are just below 1 –
that is, chimps and humans have slightly smaller postcanine areas
that would be predicted on the basis of their body sizes. The values of
H. habilis and H. rudolfensis were 1.9 and 1.5, respectively, which
 dental evidence 145

are lower than those of australoptihs, but higher than that of African
Homo erectus, at 0.9.
Notably, Homo erectus has an MQ equivalent to that of modern
humans. To some extent these estimates should be taken with a grain
of salt because of small sample sizes for some species and because
body size estimates are imprecise. Yet, estimated body size
increases from australopiths to Homo erectus (15) while posterior
tooth size decreases – opposite to the trend seen across primates.
A more recent analysis suggests that tooth size in Homo habilis
is not less than one would expect on the basis of its estimated body
size, but that for Homo erectus, tooth size is plainly less than one
would expect for its body size (324). Wrangham and colleagues (52)
refer to the reduction in tooth size in Homo erectus as one of the
“signals” that Homo erectus had begun to eat food softened by
cooking. Consistent with the idea that Homo erectus was chewing
less mechanically challenging foods is the trend of decreasing enamel
thickness in the genus Homo (334). From enamel thickness that is
quite variable in earlier Homo (343), enamel thickness is clearly
reduced in Homo erectus relative to earlier hominins (334).
Bite force also decreases in Homo erectus, but appears to do so in
Homo habilis as well (344). Using established methods to estimate
chewing muscle sizes from attachment areas on the skull, Carolyn
Eng and colleagues (344) found that maximum bite force decreased
from australopiths to both Homo habilis and Homo erectus.
Maximum bite force in both Homo species also decreased in relation
to molar area. This means that the amount of stress these two Homo
species could apply to food between their occluding teeth had declined
relative to australopiths.
A reduction in bite force during Homo habilis times is
consistent with evidence of an inactivating mutation in a myosin
gene (MYH16) in humans that appears to have arisen 2.4 million
years ago (345). Myosins are a group of proteins in muscle that,
together with actin proteins and the energy-yielding molecule ATP
(adenosine triphosphate) produce muscle contraction. The MYH16
146 dentally-derived dietary inferences

gene, in particular, is expressed in nonhuman primate head muscles,

including the temporalis, a crucial chewing muscle. The inactivation
of this particular gene 2.4 million years ago suggests loss of chewing
power in Homo habilis.
More evidence of a decline in bite force in Homo erectus is
apparent in Constantino and colleagues’ (81) study of tooth chipping.
The size of edge chips on the chewing surfaces of teeth is related to the
bite force that produced them (see Chapter 2). An equation linking
chip size to bite force reveals that Homo erectus exerted lower bite
forces than did Paranthropus species and Au. anamensis, Au.
afarensis, and Au. africanus. All of this evidence suggests that at
least in Homo erectus, and possibly in Homo habilis as well, softer
(or softened) foods were being eaten and had perhaps had already
relaxed the selection pressure for maintaining high bite force.

exploring the causes and consequences of dental

reduction in homo
The idea that relaxed selection pressures can explain the reduction,
vestigilization, or disappearance of traits dates back to Charles
Darwin, who observed many examples of such traits in nature (346).
Exactly how trait reduction occurs when selection pressures are
relaxed was less clear to Darwin, though he believed that selection
favored economy in energy use (347). Indeed the mechanisms and
consequences of relaxed selection are still not particularly well under-
stood today (347). What is also unclear is exactly when and why
selection pressures were relaxed on tooth size along the Homo lineage.
Regarding the mechanism of relaxed selection, Loring Brace
(348) believed that in the absence of selection, mutations bringing
about “physiological inactivation” would accumulate in the gene
pool. Such mutations, in his view, often bring about “structural
reduction.” He called this phenomenon the “Probable Mutation
Effect” (PME). The name refers to the probable effect – trait
reduction – of nonfunctional mutations on the size of body structures.
Such mutations, it was argued, were likely to disrupt the series of
 causes and consequences of dental reduction in homo 147

developmental steps that produced a body structure of the size

previously maintained by natural selection. Brace (348) attributed
molar reduction from australopiths to Homo erectus to a shift from
a more vegetarian diet to one with more meat, which he felt would
require less chewing. (But raw meat can be very tough, which is why
the Italian raw beef carpaccio is sliced so thinly and pounded!) In any
case, in Brace’s view, relaxed selection on molar chewing area then
brought about molar size reduction through the PME. Brace’s views
about technology and cooking in relation to dental reduction applied
to much later time periods and were based on the archaeological
record as then known.
As recounted by Jules Kieser (349), Brace’s PME concept was
criticized on several fronts. Most problematic was the assumption
that nonfunctional mutations would tend to disrupt developmental
processes. There was no clear evidence that this was true, and it was
argued that most mutations simply have neutral effects and accumu-
late too slowly for the PME to operate in any case (though see McKee
[350]). In sum, it was argued that structural reduction was not
a necessary consequence of relaxed selection.
Until recently, evolutionary biologists had not given a great deal
of attention to the topic of relaxed selection (347). In his and his
coworkers’ 2009 review, David Lahti and colleagues find that when
selection pressures previously maintaining a trait are relaxed, direct
selection for trait reduction is often happening simultaneously. For
example, many traits require maintenance costs, the most obvious
one being the energy it takes to build and/or sustain the trait. Lahti
and coauthors offer plant defensive compounds as an example.
Production of these compounds decreases under conditions of relaxed
selection while allocation of energy to growth and reproduction
simultaneously increases. Presumably, then, when these defensive
compounds are no longer needed, plants can increase their reproduc-
tive success by channeling the energy that was previously used to
make them into reproduction instead. In the end, Lahti and colleagues
conclude that it is the “. . . nature of the influences on a trait following
148 dentally-derived dietary inferences

the relaxation of a source of selection [that] determines whether the

trait will persist, be reduced to a vestige, or lost.”
Although selection pressures on maintaining large teeth may
have been relaxed during the transition from Homo habilis to Homo
erectus (and perhaps even earlier, depending on which estimates you
look at), there may have been concurrent direct selection for reduced
tooth size. In the words of Lahti et al. (347) perhaps there were
“constitutive” (inherent) costs to maintaining large teeth. Such
would be the case if growing large teeth required energy that could
be devoted elsewhere. This is the concept that Jules Kieser (349) called
the “Energetic Budget Effect.” No one knows exactly how much
energy it takes to grow teeth of different sizes. Needless to say
perhaps, it is also not known whether the energy saved by making
smaller teeth could have made a difference for survival and/or repro-
duction. But, it is worth remembering that with Homo erectus, appar-
ent selection for larger body and brain size coupled with fast rates of
somatic growth (see Chapter 7) would have put a premium on energy
economy.
Even if the energy savings of growing smaller teeth is negligible,
Peter Ungar (325) reminds us that it isn’t just teeth that reduce with
Homo erectus, but so too do the bones and muscles of the face and jaw.
These, it can be assumed, would add greater energetic costs to the
equation. Ungar suggests that there may be a genetic and/or develop-
mental connection between jaws and teeth, citing a study in mice in
which some of the same genes affecting tooth size also affected jaw
shape (351). In essence then, there is a possibility that tooth size
reduction was a genetically correlated consequence of selection for
reduced jaw size.
A similar correlational argument has been made (though not
involving constituitive energy costs) regarding the relationship
between the shape of the face and the size of first molars in modern
humans (352). Polychronis and Halazonetis (352) found that that in
modern humans, variation in the length of lower first molars is related
to variation in cranial shape. They conclude that evolutionary tooth
 causes and consequences of dental reduction in homo 149

size reduction might be explained, theoretically, as a passive

developmental result of changes in cranial shape. Whether the cranial
shape variables associated with molar length in this study are the
same as those that accompanied molar reduction from Homo habilis
to Homo erectus, however, is what would have to be determined with
respect to the problem we are considering here.
Beyond energy economy, a second cost relevant to having large
teeth is that of dental crowding and subsequent infection. In this case,
the cost can be considered a “contingent” one, as defined by Lahti and
colleagues (347), because the cost of large teeth arises from the change
in selection pressure. Here, the cost of having large teeth arises from
a change in diet to softer foods, leading to a chain of events that ends
with dental crowding. Bone growth is stimulated when subjected to
mechanical stress (353), as when chewing mechanically challenging
foods. Teeth, however, do not grow larger in response to mechanical
stress – they attain their final size and shape when they form during
childhood. Corruccini and Beecher (354) and Calcagno and Gibson
(355) reasoned that softer diets would result in less jaw growth during
childhood and adolescence, resulting in insufficient space for
later-erupting teeth. The consequences would include dental
crowding, displacement, rotation, or impaction of teeth. Indeed,
Corruccini and Beecher (354) demonstrated that nonhuman primates
who had been fed soft diets (lard) for an atherosclerosis study
frequently had crowded or malpositioned teeth (as in Figure 6.1).
Could such dental consequences as these entail costs to
reproductive success? Calcagno and Gibson (355) argue that they
most certainly could. Plaque containing disease-causing bacteria can
become easily trapped between crowded, malpositioned, or partially
erupted teeth. Wisdom teeth (or third molars) because they erupt late,
are a particular problem if the jaw has not grown large enough to
accommodate them. They may become impacted. They may erupt
only partially, trapping plaque and bits of food between the tooth and
the flap of overlying gum (the “operculum”), leading to infection and
inflammation of the soft tissues surrounding the tooth. Unchecked, as
150 dentally-derived dietary inferences

figure 6.1: Malocclusion in a baboon fed a soft diet during

development: underjet of the upper incisors. Sketch by Alyssa Starrett
based on baboon shown in: How Anthropology Informs the Orthodontic
Diagnosis of Malocclusion’s Causes by Robert S. Corruccini. Mellen
Studies in Anthropology, Vol. 1, Lewiston, New York, Queenston,
Ontario and Lampeter, Wales: The Edwin Mellen Press, 1999.
By permission of Mellen Press and Robert Corruccini.

they would have been before dentistry and antibiotics, such infections
could have progressed to life-threatening conditions. These include –
among other very unpleasant things – septicemia (blood infection),
infections of the cavernous sinus at the base of the skull, and Ludwig’s
angina– an inflammation and swelling in the mandibular region that
can cause asphyxiation.
For the most part, Calcagno and Gibson (355) applied these
ideas to the phenomenon of dental reduction in recent modern
humans, not in earlier hominins. There are a few cases of dental
pathology and tooth loss in Homo erectus. The Nariokotome boy
has a periodontal lesion on its mandible associated with the reten-
tion of deciduous tooth roots (356). Dental pathologies and tooth
loss are also present in the Dmanisi hominins (see Figure 5.3) (269,
357). But other than these cases, dental pathologies were not parti-
cularly common in Homo habilis or Homo erectus. The earliest
known case of third molar impaction occurs much later in time, in
the “Magdalenian Girl” from Cap Blanc rock shelter in France, that
is 13,000–15,000 years old (http://sciencelife.uchospitals.edu/2013/
 causes and consequences of dental reduction in homo 151

11/25/age-wisdom-teeth/). Thus, it isn’t clear that pathology asso-

ciated with dental crowing was prevalent enough to have acted as
a major “contingent cost” during Homo habilis or Homo erectus
times.
To Wrangham and colleagues (52), it was Homo erectus’s habit
of cooking food that brought about the change to eating softer foods
and subsequent reduction of jaws and teeth. On the other hand, there
is no evidence of controlled fire use in Homo habilis, but bite force
reduction was already underway (344) and the human MYH16
gene had mutated to its present nonfunctional form during Homo
habilis times as well. If eating cooked food doesn’t explain bite force
reduction in Homo habilis, then what might? Eng and colleagues
suggest that Homo habilis may have softened food with stone
tools – by cutting it up into small pieces and/or by pounding it. Still,
even if selection pressures on bite force were initially relaxed with
Homo habilis, dramatic reduction in molar size did not occur until
later, with Homo erectus (324). A delay in molar reduction in response
to eating foods softened with stone tools could simply represent evo-
lutionary lag time. But, it could just as well be that it was not until
Homo erectus began to cook food that selection pressures on tooth
size were sufficiently relaxed. So, the initial causes of bite force and
tooth size reduction during this period of human evolution remain
obscure, but they are most likely related to the use of stone tools in
preparing food, to cooking, or to both.
So far, this entire discussion has been predicated on relaxed
selection. There are other possible causes of (or contributors to)
dental reduction, as Bermúdez de Castro and Nicolas’s analysis of
the Homo heidelbergensis sample from Sima de los Huesos suggests
(358). This 430,000-year-old sample (278) exhibits molar tooth sizes
that are smaller than those of later Neanderthals, and are equivalent
to those of modern humans. Bermúdez de Castro and Nicolas (358)
assert that there are no cultural changes related to food preparation
during the Middle Pleistocene nor any increase in dental pathology
in this sample that might help explain why molars had reduced
152 dentally-derived dietary inferences

to such a degree. Indeed, Pérez-Pérez and Bermúdez de Castro

(359) interpret the microwear evidence for this sample as indicative
of eating “poorly processed,” plant foods. Perhaps, Bermúdez de
Castrol and Nicolas (1995) propose, tooth size reduced as a result of
genetic drift.
When populations are small and isolated, as they appear to have
been for long periods during the Middle Pleisotocene (358) the fre-
quencies of alleles (different forms of genes) can fluctuate dramatically
simply by chance. This is what is meant by genetic drift3 and it may
explain why teeth became small in the Sima de los Huesos sample, in
the absence of any other evidence that may explain it. So, it is
possible – and even likely given the long span of time and diverse
environments in which the genus Homo has existed – that several
different evolutionary forces and selection pressures have been
involved in dental reduction.
These questions are difficult to resolve. For now, it seems that
relaxed selection coupled with the constituitive energetic costs of
maintaining large jaws and teeth when eating food softened by some
means (tools and/or fire) is the most viable explanation for the
pronounced reduction of postcanine tooth size in Homo erectus.
Meanwhile, genetic drift may be a more likely cause of the human-
sized molars of the Sima de los Huesos sample.
When teeth reduce in size, they may change morphologically as
well. Bermúdez de Castro and Nicolas (358) observed that the later
forming hypoconulid tooth cusp was often absent from the Sima de los
Huesos lower molars, just as it often is it is in human molars. In these
teeth and modern human teeth, the number of cusps on molars tends

3
An analogy is flipping a coin – if it is flipped 100 times, the number of heads and tails
will likely be very close to 50:50. But if it is flipped 10 times, there will be many
occasions, when just by chance, you will get 7 heads and 3 tails, or some other skewed
result. If you imagine heads to be one form of a gene and tails to be the other, then it is
possible to see how in a small gene pool such skewed results could be common.
Furthermore, as soon as such a skewed result occurs in one generation, then because
the next generation draws its genes from this skewed pool, it is likely to diverge even
further from the 50:50 ratio. In this way, evolutionary trends, such as dental reduction,
can occur in small populations simply as a result of genetic drift.
 causes and consequences of dental reduction in homo 153

to be reduced relative to earlier hominins. Bermúdez de Castro and

Nicolas considered this to be a case of parallel evolution, and given
what we now know about how molar cusps form, the case for parallel
evolution becomes stronger.
Before teeth begin to mineralize, the pattern of the developing
tooth surface is mapped out in soft tissue through a series of transient
structures called “enamel knots” (360; Jurnvall and Jung) (Figure 6.2).
These structures produce molecules stimulating the folding of dental
epithelial tissue (precursor tissue to that which forms enamel) into the
shape of dental cusps. But, enamel knots simultaneously emit mole-
cular signals that inhibit the formation of enamel knots nearby and
which drop off in concentration with distance from the enamel knot
(Figure 6.2). Only at a certain distance with low-enough inhibitor
concentration, can a new enamel knot form. This understanding of
cusp formation is known as the “Patterning Cascade Model,” in
reference to the pattern of cusp positions established by the sequential
activation of enamel knots (360).
If enamel knots remain the same distance from one another but
tooth size reduces, then fewer enamel knots, and hence cusps, can
form. With my colleague John Hunter and our students, we showed
that distances among the principal cusps of a tooth relative to tooth
size could predict the formation of accessory (additional) cusps (361,
362). In this case, we were looking at the Carabelli cusp, a small
late-forming cusp sometimes present on the lingual (tongue) side of
upper first molars (and more rarely upper second molars). If molar size
decreased in Homo heidelbergensis to a greater extent than the
distances among cusps did, then there may have been no space outside
of the inhibition zones of previously formed enamel knots for the later
developing hypoconulid enamel knot to form. Put simply, as molars in
the genus Homo reduced in size, it makes sense from the perspective
of tooth developmental biology, that they became simpler as well.
It has been suggested (363) that developmental considerations
may help explain why hominin species that are more similar to
modern humans in their overall rates of development are like modern
154 dentally-derived dietary inferences

time

close enamel knot spacing

larger inhibitory zones

with wider enamel knot
spacing

close enamel knot spacing

with small tooth size

KEY
= Primary enamel knot = Inhibitiory zone

= Secondary enamel knot = Epithelial extent

= Downfolding epithelium at cusp tip

figure 6.2: Patterning Cascade Model for tooth formation for a human
upper molar. Top row shows growing dental epithelium with closely
spaced enamel knots at three successive points in time. The enamel knots
are superimposed over ghosted images of the form that the mineralized
cusps will eventually take. After the primary enamel knot forms,
secondary enamel knots form only when the dental epithelium grows
large enough to exceed the boundaries of the zone of inhibition around the
primary knot. As the epithelium grows larger still, exceeding the
inhibition zones of secondary enamel knots, additional enamel knots can
form. Middle row illustrates the same process, only with larger inhibitory
zones around enamel knots. These larger inhibitory zones prevent
formation of the fourth enamel knot that was able to form in the tooth
 conclusions 155

humans in having second and third molars that are especially reduced.
The idea is that if there is a delay in the initiation of second and third
molars in more slowly developing species but there is no change in the
age at which crown formation ceases (or in the rate of crown
formation), the period of crown formation in molars would be
abbreviated, resulting in smaller crowns. This interesting suggestion
could conceivably explain the differential reduction of molars in
Homo heidelbergensis, Neanderthals and modern humans as
a consequence of changing growth patterns in our ancestors (but it
remains to be seen if second and third molar initiation and total crown
formation times in the second and third molars of these three species
are in accord with this hypothesis).

conclusions
The present chapter reviewed dental evidence for changes in diet in
Homo, especially in Homo habilis and Homo erectus. Departing from
their australopith ancestors, these species appear to have consumed
diets that were variable, and that incorporated more meat as well as
softer (or softened) foods. Variable diets in Homo erectus are suggested
by this species’ variation in microwear complexity, indicating that
both hard and soft foods were eaten. Dental evidence of meat-eating
from trace elements is compatible with the archaeoglocial context and
with evidence of the greater molar occlusal relief and wider incisors of
Homo habilis in relation to australopiths. The changing morphology
of incisors and molars in Homo habilis points toward the conclusion
that teeth had already begun to adapt to this new diet. Softer (or

caption for figure 6.2: (cont.)

germ depicted in the top row (in which inhibitory zones were smaller).
Bottom row illustrates this process in a tooth of smaller overall size but
with enamel knot spacing equivalent to that in the top row. Here, tooth
size prevents the formation of the fourth cusp because there is not enough
space for the fourth enamel knot to form outside of the inhibitory zones of
the other cusps. Drawn by author.
156 dentally-derived dietary inferences

softened) foods are suggested by the reduction of bite force in Homo

habilis as well as by the marked reduction in molar size in Homo
erectus. Tool use in processing food as well as fire use may have
contributed to this softer diet.
With respect to dental reduction in Homo erectus, the case for
relaxed selection is plausible, but there may also have been direct
selection for dental reduction. Otherwise, if accumulating random
mutations do not necessarily lead to reduced trait size as per the
Probable Mutation Effect, it is difficult to see why individuals with
larger posterior teeth did not continue to pass along their genes for
large tooth size. Following relaxed selection for large teeth, one might
expect mean tooth size in a population to decrease as smaller-toothed
individuals would now be able to survive and pass along their
small-tooth genes. However, some factor other than relaxed selection
would seem to be necessary to explain why individuals with very large
teeth become so scarce, and the entire range of tooth sizes shifts
downwards. Here, I have suggested that the most promising place to
look for selection against large posterior tooth size in Homo erectus
may be found in the “constitutive” energetic cost of growing and
maintaining large jaws and teeth while simultaneously growing and
maintaining large brains and bodies.
Finally, with Homo heidelbergensis there is the possibility that
genetic drift can explain why this ancient hominin has postcanine
tooth sizes equivalent to that of modern humans. One idea reviewed
here, about the especially small size of Homo heidelbergensis second
and third molars, has to do with overall rates of development and
hypothesized associated delays in the initial formation of second and
third molars. This brings us to the next chapter, which explores the
topic of rates of development and the “pace of life history” in the
genus Homo prior to Neanderthals and anatomically modern humans.
7 Long in the Tooth: Life History
Changes in Homo

Last scene of all,

That ends this strange eventful history,
Is second childishness and mere oblivion;
Sans teeth, sans eyes, sans taste, sans every thing.

– Shakespeare
As You Like It

So ends Lord Jacques’s soliloquy “All the World’s a Stage,” summing

up human life history from infancy and childhood to toothless old age
and death. In Chapter 4, we saw that some australopith species may
have had juvenile growth periods shorter than or as long as those of
some modern apes, but none were quite equal to modern humans in
this regard.
Anthropologist Barry Bogin defined human childhood as the
period between weaning and puberty during which offspring continue
to depend on others for survival (180). For fossil hominins, the
existence of childhood as so defined would be hard to determine.
Applying Bogin’s definition would require information about ages at
weaning, which are difficult to acquire in fossil hominins, though not
impossible (see Chapter 10). It would also be necessary to ascertain the
length of time over which growing juvenile hominins actually
depended on others for survival, and that would be even more difficult
to determine. Nevertheless, through the study of teeth, the extension
of juvenile growth periods, if not childhood as Bogin defined it, can be
traced over the evolutionary history of the genus Homo. So too can the
evolution of “second childishness” – old age.
In this chapter, we will see that within the genus Homo, changes
in juvenile growth periods and longevity parallel each other in
direction, though it is not clear that these changes in growth periods

157
158 long in the tooth: life history changes in homo

and longevity occurred in lockstep with each other. A common trajec-

tory toward lengthening both juvenile growth periods and lifespans,
but with possible differences in their rates of change, is consistent with
the concept of “modular” life history evolution (186). The concept of
“modularity” as applied to life history recognizes that different aspects
of a species life history can respond to selection independently to some
degree. This would be the case if the genes and developmental path-
ways that affect length of juvenile growth periods, for example, are not
the same as those affecting longevity – or at least if not all of those
genes and developmental pathways are the same.
Much of the literature on primate life history considers broad
patterns across the order, arranging primate species on a continuum of
fast to slow life histories (186). Yet, consistent with the concept of
modularity, not all aspects of primate live histories can be arranged in
this way. For instance, the natural age at weaning is earlier in humans
than it is in chimpanzees, but humans reach sexual maturity and die at
later ages than chimpanzees do (205). Holly Smith (191) suggests that
humans can “afford” their late ages at sexual maturity by weaning
early, thereby reducing the time intervals between births and increas-
ing their reproductive rates. This example, and many others like it that
can be found among primates (202, 364), highlights the concept of
modularity as it applies to life history. Changes in species life history
features over evolutionary time scales are not necessarily linked.
Still, with respect to changes in juvenile growth periods and life-
span over the course of human evolution, there is a common direction
of change – toward lengthening both. This commonality suggests that
these life history features exerted evolutionary influences on each other
in some way. One possibility is that a long lifespan compensates for
a delay in reproduction caused by an extended growth period. So,
selection might have favored extended growth periods that increased
learning time only in those individuals who also lived longer. Another
possibility is that with reduced extrinsic mortality, natural selection
might have favored our investment in physiological mechanisms that
helped to extend our natural lifespans. In turn, longer lifespans may
 long in the tooth: life history changes in homo 159

have made it possible for extended growth periods, with consequent

delays in ages at first reproduction, to evolve. So, whether long growth
periods or long lifespans came first is not clear, but one can easily
imagine how these life history features might have coevolved.
The Grandmother Hypothesis (365) of human biologist Kristin
Hawkes is yet another idea about how life history features coevolved
over human evolution. In her work with the Hadza hunter-gatherers of
Tanzania, Hawkes observed that postmenopausal women work
intensively to provide for their daughters and granddaughters.
No longer able to produce their own offspring, they devote their efforts
to their existing children and grandchildren. If by so doing our female
ancestors improved the reproductive success of their children and
grandchildren, then natural selection would favor the lengthening of
their natural lifespans beyond menopause.
In Hawkes’ view, longer lifespans would enable females to
delay reproducing until they built sufficient body capital to sustain
the energetic demands of pregnancy, lactation, and offspring care.
The extra growing time, in turn, would function as a “pre-
adaptation” for longer periods of brain growth and learning.
Finally, with the food and childcare provided by their postmeno-
pausal mothers, ancestral females could wean their offspring ear-
lier, reducing the intervals between births and increasing their
reproductive rates.
Whether Hawkes’ scenario, or other ideas linking delayed growth
to longevity, is correct, the dental evidence suggests that within the
genus Homo, prolonged juvenile periods coevolved with the lengthening
of our natural lifespans. In this chapter, I detail this evidence and con-
sider its potential implications for human social evolution. Specifically,
I’ll discuss anthropologists’ speculations about whether longer juvenile
periods and lifespans may have had something to do with the evolution
of human “prosocial” behavior – behavior that benefits others (366, 367).
As in the previous chapter, this one focuses on the genus Homo prior to
the advent of Neanderthals and anatomically modern humans, which
are discussed in later chapters (Chapters 8 and 9, respectively).
160 long in the tooth: life history changes in homo

the nature of the dental evidence

As explained in Chapter 4, the primary evidence for gauging juvenile
growth periods in fossil hominins relies on associations between
dental growth and development and the overall pace of growth,
development, and life history in modern primates. The sources of
data discussed in that chapter included the dental development of
different tooth types relative to one another (a special case being
Schultz’s Rule). However, also in that chapter, estimates of the actual
timing of dental development were argued to provide more reliable
indicators of juvenile growth periods.
In terms of dental eruption, the age at which molar teeth erupt
most clearly differentiates modern humans from apes (368). Similarly,
a new review by dental anthropologists Christopher Dean and Helen
Liversidge finds that the age at which teeth begin to form (initiation)
and the length of time they take to grow does not differ much for the
anterior teeth of modern humans and chimpanzees, but does differ for
molar teeth (369). These chimp-human differences in the initiation,
tooth formation time, and eruption of molar teeth suggest that their
chronological development may provide the most useful yardstick for
assessing hominin juvenile growth periods.
Clues to longevity can be gained by estimating ages at death in
fossil assemblages. In juveniles, ages at death can be ascertained with
a fair degree of precision, using actual or virtual dental histology (see
Chapter 4). For adults, estimates of ages at death are unfortunately
much fuzzier, as any forensic anthropologist knows. To estimate ages
at death in adult fossil hominins, paleoanthropologists Rachel Caspari
and Sang-Hee Lee (370) applied the technique of “wear-based seriation”
(370), first developed in 1963 by AEW Miles (371). In this method, rates
of molar wear are estimated using average ages of eruption.
To illustrate, Figure 7.1 shows two australopith dentitions.
In the dentition on the right, the first molar (second from the last in
the tooth row) has become worn during the time between its eruption
and the eruption of the second molar (last molar in the tooth row).
 the nature of the dental evidence 161

figure 7.1: Wear seriation method of Caspari and Lee (2004; drawing by
Alyssa Starrett based on their Figure 1). See text for explanation. Caspari R,
Lee S-H. Older age becomes common late in human evolution.
Proceedings of the National Academy of Sciences USA. 2004;101:10895–
10900. Copyright (2004) National Academy of Sciences, USA.

The question is: How much time has occurred between the eruption
of these two molars? Caspari and Lee assumed that the first, second,
and third molars of hominins (including australopiths) erupted at
five, ten, and fifteen years of age, respectively. On that assumption,
the individual on the right would have been about ten years of age
when he or she died.
Now take a look at the other dentition, on the left. Here, all three
molars are in place, but the third molar of this individual is worn to the
same degree as the first molar of the individual on the right. Assuming
molars wear at the same rate, this would make the individual on the left
approximately twenty years of age at death, calculated as so: fifteen years
162 long in the tooth: life history changes in homo

for the eruption of the M3 and five more years for the M3 to reach the
degree of wear equal to that of the first molar of the individual on the
right.
Similar kinds of estimates can be made with rates of wear for
the second molars and matching these to worn third molars of other
individuals, yielding age-at-death estimates for older adults. Clearly
there is a large margin of error here owing to the assumption of
uniform ages at eruption for different hominin species and individuals
as well as the assumption of uniform rates of wear within a species.
Still, gross distinctions can be made with some confidence between
older individuals and younger ones.
Because dental development has been studied in the early
members of our genus, as have ages at death, it is possible bring
these two sources of evidence together to gain insight into life history
changes within the genus Homo. There is difficulty in teasing apart
these changes at the species level, however. The reasons is that some
studies provide evidence for Homo habilis (in the broad sense), while
others lump Homo habilis and Homo erectus into “early Homo” and
others specifically refer to Homo erectus. In this chapter, I will follow
the classifications used in specific studies, reviewing evidence for
Homo habilis, “early Homo,” Homo erectus, and Homo antecessor.

homo habilis and early homo: smart and fast

Holly Smith’s (1991) analysis of life history variation across living
anthropoids suggested a strong relationship between brain size and
life history features. Based on these analyses, she suggested that juve-
nile periods would have begun to lengthen in Homo habilis. Using the
regression line of brain size on first molar eruption, Holly Smith
predicted that first molars would have erupted at around 3 to 3.4
years of age in Australopiths (not so different from chimpanzees) but
around four years of age in the larger-brained Homo habilis. Larger
brain sizes together with later ages at first molar eruption would imply
that Homo habilis had moved in the direction of a more human-like
life history schedule.
 homo habilis and early homo: smart and fast 163

The dental data may support the view that changes in

a human-like direction were beginning in Homo habilis, but overall
they suggest relatively fast rates of dental development. To begin with
is Holly Smith’s analysis of relative dental development (195) in the
East African Homo habilis specimen KNM-ER (Kenya National
Museum – East Rudolf) 1590. When the developing teeth of this
specimen were aged according to chimpanzee dental age charts, they
gave relatively consistent ages, suggesting that at least relative to one
another, this specimen’s teeth were developing in a way that is similar
to those of chimpanzees. By contrast, using human charts of dental
development, some teeth gave ages that were half of that of other
teeth, suggesting that the specimen’s relative rates of dental develop-
ment were not at all similar to those of modern humans.
Absolute rates and periods of tooth formation also appear to be
fast in Homo habilis and in some specimens referred to as “early
Homo.” In their pioneering paper on dental development in hominins
suggesting chimpanzee-like first molar eruption times in
australopiths, Bromage and Dean (223) estimated an age at death for
the East African early Homo specimen KNM-ER 820. Using
perikymata counts, along with estimates of root growth based on
data from modern great apes, they obtained an age at death of 5.3
years but with a stage of dental development equivalent to that of
a seven-year-old child. Bromage and Dean concluded: “Unexpectedly,
the age calculated for early Homo, as represented by KNM-ER 820,
provides evidence that the trend for prolongation of the growth period
had not begun with this group” (1985: 826). Yet, the use of root growth
rates of apes to estimate root growth rates in the fossil specimen may
go some way toward explaining this result.
Other evidence also suggests rapid rates of dental development
in Homo habilis and some early Homo. In Tanya Smith and collea-
gues’ 2015 reassessment of hominin dental development (196), age at
death for the south African early Homo specimen DH (Drimolen
Hominin) 35 was calculated without recourse to estimates based on
modern great ape data, but from growth increments visible using x-ray
164 long in the tooth: life history changes in homo

synchrotron microtomography (“virtual histology”: see Chapter 4)

from the specimen itself. The resulting age-at-death estimate is 2.18
years, but the specimen has a dental age based on modern human
standards of more than 3.5 years. Fast dental development for early
Homo is also suggested by perikymata numbers on anterior teeth that
are generally lower than those of modern humans (225, 226).
Another indication of rapid rates of tooth formation in early
Homo comes from the analysis of enamel formation rates.
Christopher Dean and colleagues (226) counted daily increments at
100 μm intervals along enamel prisms of six early Homo specimens.
They plotted these counts against enamel thickness measurements at
these same intervals to obtain cumulative curves of occlusal enamel
formation. Rates of growth, as assessed by the slopes of these lines
revealed that none of the early Homo specimens formed occlusal
enamel as slowly as modern humans do. The fastest rates of all were
found in the Homo habilis specimen KNM-ER 1590.
There are a few striae of Retzius periodicities determined from
the early Homo specimens included in the Smith et al. paper (that
made use of virtual histology) in which the section plane is controlled:
two have a seven-day and one has an eight-day periodicity (196).
Meanwhile, a previous study from naturally fractured surfaces
estimated periodicities centering around eight days in early Homo
(372). On current evidence, then, early Homo does not appear to differ
from modern humans in periodicity. The same appears true of austra-
lopiths, as noted in Chapter 4.
These similar periodicities in different hominins species are
interesting insofar as there are moderate to strong relationships
between Retzius periodicity and life history features across the
primate order (Chapter 4). These findings may indicate that in neither
australopiths nor early Homo are periodicities reliable indicators of
developmental rates. Another logical possibility, of course, is that
these periodicities do indicate overall developmental rates in the
human range and/or a human-like life history schedule, but that
these hominins had unpredictably fast rates of dental development
 homo erectus and homo antecessor 165

(203). In early Homo, rapid rates of dental development could be out-of-

step with potentially slower rates of somatic growth, as they are in
Indriids (Chapter 4).
Finally, Christopher Dean and Helen Liversidge’s new compar-
ison of dental development in early Homo with a huge and diverse
sample of modern humans puts the concept of “rapid” rates of dental
development in perspective. These authors estimated ages-at-death in
three immature fossil hominins, two Homo erectus and one possible
Homo habilis specimen (STW 151). These hominins died when
their second premolars, second molars, and third molars were still
forming, so it was possible to put ages to the stages of development
these teeth had reached at the time of death.
Dean and Liversidge compared the “ages for stages” of these
three hominins to the ages at which 6,540 modern children from
across the globe reached these same stages of development. What
they found was that all three of these specimens fell within the
modern human range of ages for these stages, although at the “fast”
end of the spectrum. Dean and Liversidge interpret their results to
mean that growth prolongation may have already begun in Homo
habilis (and they suggest also possibly in australopiths). That the
two Homo erectus specimens fell within the modern human range is
much less surprising, though, given previous work on dental develop-
ment in this species.

homo erectus and homo antecessor: toward

a more human-like life history
There is even stronger evidence that rates of dental growth and
development shifted in a human direction in Homo erectus. For
starters, relative rates of dental development in this species are
human-like. Analysis of radiographs reveal that the sequence of
tooth development across the dentition is quite similar to that of
modern humans (373), although with some advancement of posterior
teeth relative to anterior ones (374). Of course, however, this does not
166 long in the tooth: life history changes in homo

mean that the actual length of time for tooth development to take
place was the same.
Christopher Dean and colleagues’ (2001) Nature study on
incremental growth in fossil hominins (226) included an estimate of
first molar emergence in Homo erectus. These authors made
histological sections of the Homo erectus specimen Sangiran S7-37
from Java and counted dental growth increments. Here is what they
did: they assumed that the first molar initiated crown formation
shortly before birth, as it does in apes and humans. On that reasonable
assumption, they counted growth increments in the histological
section to determine the age at which the first molar crown completed
formation – approximately 2.5 years of age.
Next, they calculated the rate at which the first molar root grew
in length – its “root extension rate” – using growth increments present
in root dentine. They noted that first molars erupt into functional
occlusion in hominins when about 8 mm of root is formed, suggesting
that emergence through the gingiva would have occurred somewhat
earlier, when about 7 mm of root had formed. They then applied the
root length extension rate they had calculated to 7 mm of root, obtain-
ing the length of time it took to form. Adding root formation time to
the age at which the first molar crown completed, they estimated that
first molar gingival emergence occurred at about 4.4 years of age.
The estimate is consistent with the M1 emergence age of 4.6 years
that Holly Smith predicted on the basis of brain size in early Homo
erectus (200). While this M1 emergence estimate indicates a growth
rate shift in a human direction, it does not quite reach average human
M1 emergence ages, with means as low as 4.7 years of age (Kenyan
girls) to means of six or more years of age in many human groups
(Liversidge in [238]).
Performing an analysis similar to this one, Dean and colleagues
(226) also estimated gingival emergence of Sangiran S7-37’s second
premolar. If it erupted as it does in modern humans along with the M2,
then M2 eruption would have been around 7.6 years of age. This is
higher than the mean of 6.7 years for M2 emergence in captive
 homo erectus and homo antecessor 167

chimpanzees (375), though it is encompassed within the chimpanzee

range in captivity of 5.6–7.8 years of age (375). The Sangiran
specimen’s M2 emergence estimate is quite low compared to modern
humans, whose second molars are often referred to as “12-year-old”
molars. The earliest mean M2 emergence ages in modern humans
appears to be around ten years of age (girls in Uganda) (Liversidge in
[238]), and even this is greater than the 7.6 years estimated for M2
emergence in Sangiran S7-37. So, it seems, the shift toward a more
human-like schedule of dental developmental in Homo erectus is
fairly modest.
Perhaps even more revealing is the analysis Dean and Smith
(374) performed of both dental and skeletal growth in WT 15000, the
Nariokotome Boy. This nearly complete 1.6 million year old skeleton
(Figure 7.2) has provided a wealth of information to paleoanthropolo-
gists. Smith and Dean (374) added to that wealth with their analysis.
These authors made use of perikymata counts, estimated periodicity
(it was not possible to section these teeth), and an estimate of root
length extension rates, to propose that the Narikotome Boy was in the
range of 7.6 – 8.8 years of age when he died. That estimate is critical to
evaluating his rates of dental and skeletal growth and development.
At death, the Nariokotome boy’s lower second molars were
already in functional occlusion, and based upon this as well as the
state of development in his other teeth, he was equivalent to a modern
human of 10.2 years of age. He was clearly dentally advanced, then,
but it turns out he was even more advanced skeletally. This boy, who
was at most nine years of age at death, had a state of elbow joint
ossification similar to that of a 13.5 year old modern human boy.
Furthermore, he had already achieved a stature of 5 feet 3 inches,
which in modern terms is extremely tall for such a young boy and in
Homo erectus terms almost as tall as the average adult, at five feet four
inches (based on nine specimens). Smith and Dean point out that even
when advanced, modern human adolescent boys do not reach this
percentage of adult stature until they are 17–18 years of age, or
16–17 years in the most advanced cases (376).
168 long in the tooth: life history changes in homo

figure 7.2: Artist’s rendition of the Nariokotome Boy (WT 15000)

skeleton. Drawn by Alyssa Starrett.
 homo erectus and homo antecessor 169

In sum, Dean and Smith (374) state “. . . it is clear that for a child
like Nariokotome, with skeletal age advanced by 34+ months over the
dentition, a pediatrician would be justified in sending the case to an
endocrinologist” (2009). Or, perhaps the pediatrician might send the
Narikotome boy to an evolutionary anthropologist, who would
helpfully point out that the boy shouldn’t worry because species can
differ in their “life history modes.” Evolutionary anthropologists
Steve Leigh and Greg Blomquist (186) define a “life history mode [as]
a distinctive pattern or arrangement of ontogeny with respect to the
rate and scheduling of growth for various organs, organ systems, or
modules” (2007:403). It seems that Homo erectus and Homo sapiens
differ from each other in this respect – with Homo erectus having rates
of skeletal growth and development that are more rapid in relation to
dental development than do modern humans.
Exactly what the selective pressures were that shaped Homo
erectus life history modes are a matter of speculation. Dean and Lucas
(192) suggest that growing to a large size relatively quickly could have
been advantageous in an environment where small offspring were at
high risk of predation. They also observe that achieving larger body size
at a relatively early age would also allow Homo erectus juveniles to
begin to provide for themselves and for others. What seems most clear
from Dean and Smith’s (374) analysis is that somatically, Homo erectus
juveniles grew more like modern apes, lacking the slow growth
between weaning and puberty that typifies modern human children.
Filling in more of the picture for Homo erectus life histories are
Caspari and Lee’s (370) longevity estimates in early Homo, in which
Homo erectus specimens were included. Using wear-based seriation
estimates as described earlier, they separated individual hominin
specimens crudely into groups of young (between 15 and 30 years of
age) and old (greater than 30 years of age) adults for each taxonomic
group. Australopiths (353 individuals) had an “old to young ratio” or
“OY ratio” of 0.12. For early Homo (208 individuals), the OY ratio
jumps to 0.25, a difference from australopiths that the authors found
to be statistically significant. If these OY ratios are taken at face value
170 long in the tooth: life history changes in homo

(though they clearly rely on many assumptions – see earlier

discussion) they suggest a strong shift, in which a little more than
twice the number of early Homo adults were living to ages of thirty or
greater as compared to their australopith predecessors. From Caspari
and Lee’s analysis, it isn’t clear if the trend began with Homo habilis
because Homo habilis and Homo erectus individuals were grouped
together into early Homo. At minimum, these data suggest that by the
time Homo erectus had come on the scene, more individuals were
living beyond the age of 30.
Still, given the small number of specimens of Homo erectus for
which we have information for both dental and somatic growth, the
crudity of OY ratio estimates, and the question of whether the fossil
assemblages on which OY estimates are calculated are truly
representative, it is not possible to determine whether human-
trending changes in longevity preceded changes in juveniles growth
periods or vice versa. Nor, unfortunately, is it possible to meaningfully
compare the magnitude of changes in longevity with the magnitude of
changes in dental and somatic development in Homo erectus. OY
ratios only provide two categories into which the remains of fossilized
individuals are sorted on the basis of their ages at death – even a small
average change in longevity could tip a sizeable number of individuals
from the young to old category. On the positive side, these data do
suggest that Homo erectus took a “small step” toward modern human
life histories, both in terms of juvenile growth periods (dentally if not
skeletally) as well as lifespan.
It has been suggested, though, that Homo antecessor took
a “giant leap”toward humanness around 1 million years ago (377).
José Bermúdez de Castro and colleagues assessed the pattern of
relative dental development in a mandible with mixed dentition
(both deciduous and permanent teeth) from the Gran Dolina Lower
Pleistocene cave site located in the Sierra de Atapuerca of Northern
Spain. They used microcomputed tomography to image portions of
the teeth contained within the mandible. Relative dental develop-
ment was similar to that of modern humans and not to chimpanzees.
 teeth, helping hands, and growing brains 171

In another individual from this site, the upper and lower first
molars had only recently erupted, judging from the minimal wear
present on the tooth crowns. Unable to apply histological techniques
to these fossil remains, the authors applied root length extension rate
data from chimpanzees and humans to the length of root formed in the
first molars at the time of death (8 millimeters). Doing so allowed the
authors to estimate how much time it took for the root to form if it
grew at either a chimpanzee or modern human rate.
To the chimpanzee-based root formation time estimate, they
added the average crown formation time for an Australopithecus first
molar to form. For the human-based root formation time estimate, they
added the average crown formation time for a human first molar to
form. On this basis, they bracketed their estimate between “fast” and
“slow” extremes for the time at which the first molars would have
emerged through the individual’s gingiva: 5.3–6.6 years. While there is
a good deal of estimation going on here, even the 5.3 M1 eruption
estimate is within the modern human range for M1 eruption, though
at the fast end of it. Whether all aspects of dental development fit
comfortably within modern human ranges is unclear, as only the devel-
opmental pattern and M1 eruption ages were studied here. However, in
relation to WT 15000, Homo antecessor seems to have moved farther
along the path toward extending the period of dental development.
The rest of the life history story in the genus Homo concerns
Neanderthals and the earliest anatomically modern Homo sapiens
(AMHS), the subjects of the chapters that follow. Before moving for-
ward to dental insights into Neanderthals and AMHS, I turn to what
the dentally-derived insights into life history in Homo erectus may
imply for the evolution of human prosocial behavior.

teeth, helping hands, and growing brains

Anthropologists hypothesize that there are connections between the
evolution of slow growth rates, the help of others in rearing offspring,
and the human ability to wean their offspring earlier than apes do.
Kristin Hawkes’ Grandmother Hypothesis considers the special role
172 long in the tooth: life history changes in homo

of grandmothers as helpers. In humans, help in rearing offspring also

extends to other members of the group, as well (378). In comparison
with many other primates, humans have been said to exhibit
“hyper-cooperation” (366). Humans help their relatives and trusted
allies, just as chimpanzees do. However, apparently unlike
chimpanzees and other great apes, humans also show “proactive
prosociality” – they spontaneously act in ways that benefit others,
even when assistance is unsolicited (366).
Judith Burkart and colleagues (367) designed an experimental
apparatus in which primate and human subjects could help conspeci-
fics reach a food treat they could not reach themselves. Chimpanzees
did not behave helpfully, but human children did. The only other
primates who spontaneously helped others were those who belonged
to species who routinely “allomother.”
Allomothers are individuals other than the mother who help
raise offspring. Species in which allomothering is habitual and
extensive – where siblings, other relatives, and even nonrelatives
regularly help parents to raise offspring – are known as “cooperative
breeders” (378). Within the primates, only the callitrichids (marmo-
sets and tamarins) and humans satisfy this definition of cooperative
breeders (378), though many other primates exhibit allomothering to
a lesser degree. In common marmosets, for example, allomothers,
which include an infant’s siblings as well as the males with whom
the mother has previously mated, carry infants and may provide them
with food (small prey)(378).
Infant-carrying and provisioning by allomothers is characteristic
of humans: it does seem to “take a village” to raise a human child.
Furthermore, the help of others may enable mothers move on to their
next pregnancy. Human biologist Barbara Piperata showed that in the
Brazilian Amazon, women who receive the greatest level of social
support – help from others in the community – lose the least amount
of weight when they are nursing their babies (379). Energy balance – the
relationship between energy taken in and energy expended – is related
to the length of time it takes for women to resume ovulatory cycles
 teeth, helping hands, and growing brains 173

after they give birth (380). In other words, the amount of energetic stress
a mother sustains when she is nursing her offspring affects when she
can become pregnant again. So, Piperata hypothesizes that women who
receive the most social support may be able to become pregnant sooner
than they otherwise wood. Piperata and I (381) argued that that during
human evolutionary history, social support may have been a critical
adaptation, enabling female hominins to reduce the intervals between
births and therefore to have more children. Slowing of juvenile growth
rates may have made it possible to support more than one dependent
child at a time, because it reduced the total amount of energy needed to
support them (382).
Based on an earlier suggestion by evolutionary biologist WD
Hamilton (383), Primatologist Sarah Hrdy (378) theorized that
cooperative breeding itself allows delayed maturation. She pointed
out that in birds (in the passerine order, specifically) fledglings of
cooperatively breeding species continue to depend on parents for
twice as long as they do in those that do not breed cooperatively (citing
work by Langen [384]). Essentially, as helpers take over feeding
responsibilities, mothers are free to breed again, reducing the pressure
on fledglings to become independent. Extending the argument to
humans, longer periods of learning may simply be a by-product of
prolonged periods of childhood dependency that followed from
a system of cooperative breeding. This idea is consistent with
Kristin Hawkes’ (365) view that extra growing time served as
a “pre-adaptation” for longer periods of brain growth and learning.
Differing in emphasis, these explanations all suggest that in some
way cooperative breeding, extended growth periods, slow growth rates,
and early weaning coevolved. Teeth come into this picture by offering
evidence as to when the lengthening of juvenile growth periods began as
well as when “grandmothers” could have been around to help. By the
time of Homo erectus, rates of dental development had begun to slow.
Rates of somatic development, however, may still have been quite
rapid, judging from the Narikotome boy.
174 long in the tooth: life history changes in homo

With Homo erectus, both body and brain size increased,

presumably increasing the energetic demand of growing offspring as
well as the energetic demands on pregnant and nursing mothers (385).
It would seem, therefore, that during this period of our evolutionary
history, there would have been a need for allomothers to help provi-
sion offspring (192). Fast rates of somatic growth – if the analysis of the
Narikotome boy proves to representative of Homo erectus – may have
exacerbated the energetic demands of offspring, further increasing this
need. According to one recent study, viable population sizes in large-
brained Homo erectus could not have been sustained without
a system of cooperative breeding (386). Caspari and Lee’s (370) study
of dental wear rates suggests that in Homo erectus, more than in any
previous hominin species, a greater number of grandmothers were
available to help.
Children are not the only humans who need a lot of help. On the
basis of dental evidence it was suggested that care for older individuals
occurred in the 1.8 MA hominins of Dmanisi, Georgia. One of the
Dmanisi skulls is missing all but one tooth (see Figure 5.3), with the
sockets showing nearly complete bone resorption (357). The resorption
indicates that this individual lived for a long period of time without his
or her teeth. This specimen represents the earliest such case of such
a toothless or “edentulous” individual in the hominin fossil record.
How did this individual survive? Lordkipadnze and colleagues think
that the individual probably relied on softer foods and possibly the help
of other individuals to supply these soft foods (357).
While assistance from others is a plausible explanation, the survi-
val of the toothless does not necessarily imply it. Primatologists Frank
Cuozzo and Michelle Sauther (387) studied ring-tailed lemurs in
Madagascar who lose plenty of teeth, owing to their feeding-
dependence on hard and tough tamarind fruit that they do not appear
to be dentally adapted to eat (they have thin enamel, for one thing). Their
reliance on tamarind fruit may be a relatively recent phenomenon in
their evolutionary history, resulting from human disturbance of their
habitat. These lemurs tend to lose the very teeth they use in masticating
 concluding thoughts 175

this fruit. Yet, individuals with extensive tooth loss survive, without the
active assistance of others. Cuozzo and Sauther attribute their survival
to “unintentional” assistance from others in the group.
Being part of a social group allows lemurs to make use of shared
knowledge about the location of food resources. Interestingly, Cuozzo
and Sauther have seen toothless individuals pick up and eat tamarind
fruit that other have that partially chewed and discarded. So, these
authors make the excellent point that if toothless lemurs can survive
with such “passive” assistance, then toothless hominins may have
been able to do the same. And of course, as Cuozzo and Sauther also
point out, the Dmanisi individuals had stone tools, so a toothless
individual may have been capable of processing his or her own food,
making it more chewable.

concluding thoughts
This chapter brought together dental evidence for the evolution of two
defining life history features of modern humans: prolonged growth
periods and long lives. Dentally, Homo erectus evinces a step toward
a longer period of development. First molar eruption was intermediate
between that of chimpanzees and humans (226), and the ages at which
particular stages of development were reached (second premolars,
and second and third molars) were within the modern human
range (369).
Still, the advanced state of skeletal development in the
Narikotome boy implies somatic growth rates more like that of
chimpanzees than like that of modern humans. The Narikotome
analysis may signal a life history “mode” in Homo erectus quite
unlike that of modern humans – with a different combination of
developmental rates in the dentition and skeleton. Why that
combination differed, i.e., what particular selection pressures may
have been involved, is not clear. However, the story of human life
history evolution in the genus Homo is likely to be more complicated
than a series of simple shifts toward a modern human pattern.
As emphasized in Chapter 4, different species may have been subject
176 long in the tooth: life history changes in homo

to different sets of selection pressures shaping their own particular life

history modes. Expanding the comparative context from living
primates – understanding how their life history modes vary in
response to diverse selection pressures – will help in interpreting the
life history modes of fossil hominins.
By the time of Homo erectus, lifespans appear to have length-
ened to some degree, taking the OY ratios from dental wear-seriation
at face value. If so, then older individuals would have been available to
help provision fast-growing, large-brained Homo erectus children.
The overall picture that studies of teeth have helped to paint is that
the beginnings of extended development, longer lives, and cooperative
breeding can be traced back to Homo erectus. By 1 million years ago,
with Homo antecessor, first molar eruption seems to have entered the
modern human range (377). Whether this was so in Neanderthals and
the earliest anatomically modern humans is considered in the next
two chapters (respectively) as are other questions about Neanderthal
and AMHS biology and into which teeth yield insights.
8 Knowing Neanderthals through
Their Teeth

We cannot avoid recognizing these late Neandertals as the same sort of

creatures as ourselves: upright, talking apes with a capacity for technolo-
gical innovation and symbolic behavior. Questions about interfertility
take on a lesser importance in the light of that admission.

– Cartmill M and Smith F

The Human Lineage

Ever since Neanderthals were discovered more than 150 years ago (see
Chapter 5), scientists have debated just about every aspect of their
biology. Based on the distinctive features of Neanderthals (Chapter 4)
is easy to see why King considered Neanderthals to be a different
species from humans, christening them Homo neanderthalensis.
Like other scientists of his time, King also inferred mental capacity
from the shape of the cranium, considering Neanderthals to be low-
brows in more than one sense of the word. Between 1911 and 1913,
paleontologist-artist Marcelin Boule published illustrations depicting
Neanderthals as stooping hairy beasts with grasping toes. This too did
not help Neanderthals with their image problem. Boule’s conception
held sway until 1957, when Straus and Cave showed that Boule had
misread the evidence, and that Neanderthals walked upright just as
we do (281).
Ideas about Neanderthals began to change in the 1950s, in part
because the field of physical anthropology itself was transforming. In
the wake of World War II, physical anthropologists repudiated the idea
that there are races or types of humans with distinct physical and
mental attributes. Instead, the consensus view was, as it is today, that
there are no clear physical or mental divisions among human popula-
tions along racial lines, that mental attributes are not linked to phy-
sical attributes, and that there is no evidence that human populations

177
178 knowing neanderthals through their teeth

differ in intelligence. Racist thinking, it was argued, had led to a

serious misunderstanding and Neanderthals were welcomed back
into our species. Our modern understanding of species rests on evolu-
tionary biologist Ernst Mayr’s concept of reproductive isolation –
species evolve independently of one another and become distinct if
they do not exchange genes. As part of our species, the implication
was that when and where Neanderthals and anatomically modern
humans coexisted, they could have interbred to produce fertile off-
spring. By extension, today’s humans (though in need of a time
machine to do it) could have mated with Neanderthals and had chil-
dren who themselves were fully capable of reproducing.
This shift in our understanding of Neanderthals did not last. In
1997, we were back to the “two species” place where we started, but
this time on what seemed to be firmer, i.e., genetic, grounds.
Geneticist Matthias Krings and coworkers successfully extracted
mitochondrial DNA (mtDNA) from the original Neanderthal
remains, and compared it to the mtDNA of people living today (388).
What these researchers found was that the mtDNA differences
between Neanderthals and modern humans were three times greater
than those between any two groups of modern humans. It now seemed
that Neanderthals were only very distantly related to modern humans
and that Neanderthals had no direct genetic input into our modern
genomes. Still, this was mtDNA, which is such a small part of the
genome and represents only maternal genetic input. More definitive
evidence would be sought in Neanderthal nuclear DNA.
By 2010, researchers had sequenced much of the Neanderthal
nuclear genome. Geneticist Richard Green and colleagues estimated
that 1–4% of the DNA of some living peoples came from
Neanderthals (279). Those living people are Europeans, Asians, and
Australasians, but not Africans. This finding suggests that in some
region(s) of the world, Neanderthals and our ancient human ancestors
interbred to produce viable offspring whose living non-African
descendants retain a small percentage of Neanderthal DNA. Yet in
2012, evolutionary biologists Anders Eriksson and Andrea Manica
 knowing neanderthals through their teeth 179

published a paper suggesting that this 1–4% Neanderthal contribu-

tion might not be specifically Neanderthal but could have been
inherited from a common ancestor of both Neanderthals and modern
humans (321). And so debate rages about whether we and
Neanderthals are a single species and to what extent we carry
Neanderthal genes within us.1
The question of just how different Neanderthals were from us,
and in what ways, underlies most research on Neanderthal biology
and culture. The question is not only integral to defining
Neanderthals but also to shedding light on why modern humans
survived and Neanderthals did not. Neanderthals inhabited Europe
and the Middle East from as early as 430,000 years ago, if the Sima de
los Huesos Homo heidelbergensis fossil cache represents the base of
the Neanderthal clade (see Chapter 5). Their existence spanned cold,
glacial conditions to more temperate, interglacial times.
Anatomically modern humans, those who look like us, moved into
Europe (coming originally from Africa) about 40,000 years ago (296).
They appear to have overlapped in time and space with Neanderthals
(though see [389] for a different view) but generally had more
sophisticated tools and produced copious artistic cultural remains in
the form of cave paintings and carvings. These cultural advances
associated with modern humans constitute the Upper Paleolithic,
the last period of the “old stone age.”
This chapter highlights what the evidence from Neanderthal
teeth tells us about our similarities and differences from Neanderthals
and considers what their evolutionary implications might be. The
study of teeth has specifically provided insight into the ancestry of
Neanderthals as well as made significant contributions to understand-
ing their diets, behavior, experience of physiological stress, and life
history. Neanderthal teeth offer some surprises, some confirmations,

1
Part of the problem in assessing species status based on gene flow is that gene flow can
occur between species. Interspecific gene flow can occur by the process of introgres-
sion, when the hybrid offspring of two different species mate with one (or both) of the
parent species.
180 knowing neanderthals through their teeth

and some contradictions. But, the contradictions, like the debates about
Neanderthal DNA, are ultimately moving us toward a more refined
knowledge of Neanderthal nature.

what can teeth tell us about neanderthal

phylogenetic relationships?
As noted in Chapter 5, Neanderthal teeth have numerous morpholo-
gical differences from those of modern humans. Among these are their
taurodont roots (Figure 5.7) large and labially-convex shovel-shaped
incisors, asymmetric lower second premolars, and upper molars with
enlarged hypocone cusps (Figure 8.1). Yet, many of these features can
be found, although at different frequencies, in earlier hominins. The
“bulging” hypocone, once thought to be a derived Neanderthal
feature, is present not only in the likely progenitors of Neanderthals
– the Sima de los Huesos Homo heidelbergensis group – but also in
Homo heidelbergensis specimens from other regions of Europe (390).
Other dental features typical of Neanderthals (e.g., a continuous mid-
trigonid crest) appear to be present in Homo antecessor and even
Homo erectus (from Zhoukoudian China and in site from Java) (391).
As paleoanthropologist Song Xing and colleagues put it, many
typical “Neanderthal-traits” are simply those that Neanderthals
exhibit at higher frequencies than previous hominins (293). Elevated
frequencies of these traits, some of which have no demonstrated
functional significance, suggests the operation of genetic drift.

paracone paracone

protocone
protocone

metacone metacone

hypocone hypocone

figure 8.1: Anatomically modern human (left) vs. Neanderthal (right)

upper first molars. After Gómez-Robles et al. (2007), Figure 7. Note the
bulging hypocone of the Neanderthal molar. Drawn by Alyssa Starrett.
 what can teeth tell us about neanderthal? 181

If Neanderthals existed at low population densities (392) and were

relatively isolated from other contemporary hominins, it follows
that their dental trait frequencies would drift in this way. It turns
out the genetic drift is the most likely explanation for the distinctive
features of Neanderthal cranial morphology (393).
What this patterning of dental trait frequencies might mean for
Neanderthal phylogenetic relationships is the more interesting question
though. Using the Krapina Neanderthals as an outgroup, Stringer and
colleagues (394) performed a cladistics analysis to assess how modern
humans from different regions of the world appeared to be related. Their
analysis indicated that modern Africans were first to branch off on the
modern human line after its divergence from Neanderthals. This result
challenged an earlier notion that Neanderthals were the direct ancestors
of modern Europeans (395, 396). It may seem difficult to reconcile this
result with DNA evidence of Neanderthal gene flow into non-Africans
(279). However, the percentage of Neanderthal genes introduced into
living non-Africans is small (1–4%). The cladistic analysis of dental traits
therefore primarily reflects the accumulation of genetic differences
(through genetic drift and possibly natural selection) arising after
Neanderthals and these modern human groups diverged.2
Rather than focusing on Neanderthal relationships to modern
humans, Maria Martinón-Torres and colleagues performed cladistics
analysis based on the dental traits of Neanderthals in the context of
earlier and contemporary hominins (391). Their analysis revealed two
clusters – one with African hominins (including Homo habilis,
African Homo erectus, and Middle-Pleistocene north Africans) and a
second with Asian Homo erectus (from Zhoukoudian, China and from
sites in Java), Homo antecessor, Neanderthals and middle Pleistocene
Homo sapiens. They believe their results show population continuity

2
Shara Bailey found that early anatomically modern humans from Qafzeh cave, Israel
(dated to 90,000 years ago) appear to be more similar to sub-Saharan Africans in their
dental morphology than to Neanderthals. (284. Bailey SE. Dental morphological affinities
among late Pleistocene and recent humans. Dental Anthropology. 2000;14:1–8). She
suggests that if there was admixture between Neanderthals and anatomically modern
humans in Middle East, it did not appear to have influenced Qafzeh dental morphology.
182 knowing neanderthals through their teeth

between Europe and Asia during the Pleistocene, with a deep division
between Eurasia and Africa. In other words, they attribute the
similarity between middle Pleistocene Europeans (including
Neanderthals) and Asian Homo erectus to extensive gene flow. Of
course, more recent common ancestry between Asian Homo erectus
and middle Pleistocene European hominins – as per a standard reading
of a cladogram – could also explain their results.
Whatever the explanation, the Martinón-Torres et al. study
presents a challenge to previous notions that Asian Homo erectus
represents a remote and isolated side branch of the hominin evolu-
tionary tree (276). Furthermore, teeth older than 60 KYA from the site
of Xujiayao, Northern China (Xing et al., 2015) exhibit high degrees of
incisor shoveling and labial convexity (293), traits that Martinon-
Torres and colleagues (391) identified as part of a “Eurasian dental
pattern.” On the other hand, a recent study of middle Pleistocene
Homo erectus specimens from another site, that of Hexian in
Eastern China, finds no Neanderthal dental traits in these hominins
(397). Thus, if there were gene flow during the middle Pleistocene
between Europe and Asia, there was at least one pocket of people in
Asia into which Neanderthal genes – or, at least those genes coding for
dental traits – did not arrive.
Paleoanthropologist Aida Gómez-Robles and her coworkers
attempted to reconstruct the dental features of the last common
ancestor of Neanderthals and modern humans (398). These researchers
then used those features to assess whether any known fossil hominin
species fit the dental description of this common ancestor. To do this,
they quantified dental morphology using geometric morphometric
analysis, a method in which a series of points (landmarks) are placed
in homologous positions on either photographs or 3-D scans of similar
skeletal elements. In this case the elements were teeth, and 2-D
images were used. Various statistical techniques were applied to
these data to analyze shape differences. From the “shape variables”
obtained in this analysis, the authors used another statistical method
 what can teeth tell us about neanderthal? 183

(a generalized linear model) to estimate the state of these traits in the

last Neanderthal-modern human common ancestor.
Next, the authors compared their reconstructed “dental
ancestor” with the dental shape attributes of species that are potential
candidates for the Neanderthal-modern human last common
ancestor, such as African Homo erectus, Homo antecessor, and
Homo heidelbergensis. The surprising result was that the dental
morphology of none of the fossil samples matched the reconstructed
dental ancestor. The earliest European species, Homo antecessor at 1
million years ago, was already dentally derived in the direction of
Neanderthals. Gómez-Robles et al. argue that that the last common
ancestor between Neanderthals and modern humans must therefore
predate Homo antecessor and suggest that its remains are most likely
to be found in Africa (though, according to their analysis, it is not
represented by any currently known Homo erectus groups). Their
results are seemingly at odds with nuclear DNA analysis that puts
the divergence of Neanderthal, Denisovans, and modern human DNA
around 800,000 years ago, on average (300). The genetic and dental
data could conceivably be reconciled if differences in dental
morphology among these groups arose earlier than their average
DNA divergence dates.
Altogether then, dental evidence is helping to refine our under-
standing of Neanderthal evolutionary relationships. Consistent with
genetic evidence, the dental evidence controverts the idea that
Neanderthals are more closely related to modern Europeans than
they are to other modern human groups. The dental evidence from
middle Pleistocene hominins raises the possibility that some popula-
tions of Asian Homo erectus may have had more to do with the
evolutionary history of middle Pleistocene Europeans, including
Neanderthals, then previously supposed. Finally, the reconstruction
of the last common dental ancestor of Neanderthals and modern
humans reveals that Homo antecessor at 1 million years ago was
already derived in the direction of Neanderthals, pushing the initial
184 knowing neanderthals through their teeth

divergence between Neanderthals and modern humans back in time.

While such phylogenetic questions go to the heart of Neanderthal
research, a good deal of work on Neanderthal teeth goes more toward
the stomach – that is, what and how did Neanderthals eat?

real neanderthals did not eat quiche, but did they

eat much besides large mammals?
In July 2012, the scientific journal Nature announced that
“Neanderthals ate their greens.” (http://www.nature.com/news/nean
derthals-ate-their-greens-1.11030). The evidence came from teeth.
That was breaking news because Neanderthals have traditionally
been considered big game hunters, eating such large mammals as
woolly mammoths, woolly rhinos, and bison. These are the
predominant animal remains found at Neanderthal sites throughout
Eurasia and across the timespan of Neanderthal existence.
Neanderthals actually hunted (vs. scavenged) these large mammals.
They fashioned thrusting spears and javelins, some with stone-tipped
points (399). Neanderthal weapons have even been found in the bones
of prey animals: a wooden spear amongst the ribs of a straight-tusked
elephant (a site in Germany) (400), and a stone point embedded within
one of the neck vertebrae of a wild ass (a site in Syria) (401).
Furthermore, studies of stable isotopes suggest that
Neanderthals occupied a top carnivore niche (402–404). Of great uti-
lity in these studies is N-15 (nitrogen-15), a rare isotope of nitrogen
(the much more common form is nitrogen-14). The protein we ingest
is rich in nitrogen, which becomes incorporated into the protein of our
own tissue. Along the food chain, N-15 (nitrogen-15) becomes more
concentrated, increasing by three to five parts per thousand at each
step. Plants contain very little N-15, herbivores have more N-15, and
carnivores have the most. Thus, the hair of vegans tends to be depleted
in N-15 compared to those who include meat in their diets (405).
Whereas hair does not preserve well in the fossil record, bones
and teeth do, and their main protein component, collagen, contains a
lot of nitrogen. Collagen in a tooth (specifically its primary dentin)
 real neanderthals did not eat quiche 185

reflects diet at the time a tooth was forming, while collagen in bone
reflects the average protein portion of the diet over the course of
several years before death. For this reason, unless a researcher is
specifically interested in childhood diets, most studies of N-15 focus
on bone collagen. We’ll return to the starring role of teeth later, but for
entirely different reasons.
Neanderthals appear to have had levels of N-15 high enough to
suggest that almost all of their dietary protein was obtained from
animals and not plants (402–404). Paleoanthropologist Hervé
Bocherens is an author of several of these studies, and in 2009 he
synthesized data from the most reliable studies to date (406). For six
Neanderthals from northern Europe (France and Belgium), he reported
N-15 values that were one to two parts per thousand higher than those
found in contemporaneous fossil carnivores, such as hyenas, wolves,
and cave lions. The high N-15 levels can be explained if Neanderthals
were primarily eating herbivores such as woolly rhinoceros, large
bovids, and woolly mammoth, which themselves had higher N-15
levels than other animals around at the time. Furthermore, these six
Neanderthals spanned a 65,000 year time frame, suggesting stability,
if not rigidity, in Neanderthal diets.
Aquatic species tend to have even higher levels of N-15, and a
while a few freshwater fish might have elevated these Neanderthal’s
N-15 levels, they are not as high as would be expected if fish were a
major component of Neanderthal diets. Sources of marine protein can
also be ruled out because levels of Carbon-13 make it possible to
differentiate between marine and terrestrial sources of protein. By
contrast, stable isotope studies suggest that anatomically modern
humans with whom Neanderthals shared Europe (between 40,000
and 28,000 years ago) had wider ranges of isotope values suggesting
a more varied diet, and one that included both freshwater and
marine animals (403). Archaeological data support the idea that ana-
tomically modern humans during this time period had broad diets
that included fish and fleet prey such as birds and small mammals
(407). The tool kits of anatomically modern humans of the European
186 knowing neanderthals through their teeth

Upper Paleolithic have long been known to have been quite diverse,
contributing to the ability to make use of varied resources.
The archaeological and isotopic data clearly tell us that
Neanderthals were eating large terrestrial mammals, but do they
necessarily imply that Neanderthal diets were limited to these food
sources? The answer to this question is critical because our under-
standing of Neanderthal behavioral complexity, extinction, and social
organization may hang in the balance. If Neanderthals rarely ate
plants or small, hard-to-capture prey, is this because they lacked the
ability and or technology to do so? Did their narrow diets lead to their
extinction in competition with more adaptable anatomically modern
humans? And, if they relied nearly exclusively on large game for
subsistence, did this mean that Neanderthal women were not
spending their time gathering plant foods or hunting small animals,
as they do in modern foraging societies?
These questions have been discussed at length. Neanderthals
appear to lack such implements as crushing and grinding stones (408)
that are necessary to obtain maximum nutritional benefit from seeds
and nuts. Large mammals, although rich in energy, are unpredictable
food sources. Without other sources of foods to fall back on, such as
small animals and plants, Neanderthals would have been likely to
experience periodic famine. Anatomically modern humans would
have had a more uniform supply of food, perhaps contributing to
lower mortality and higher fertility. Anthropologists Steven Kuhn and
Mary Stiner, in their creatively entitled “What’s a Mother to Do?,”
suggested that Neanderthal women may have helped in the pursuit of
large game, but that they did not provide the plant foods and small
mammals that allowed anatomically modern humans to buffer and
enrich their food supply, and thus gain a competitive edge (408).
Clearly depending on just how limited Neanderthals diets were
relative to those of modern humans, these ideas about Neanderthal
behavioral inflexibility, extinction and the division of labor by sex
may require rethinking. To be fair, plant remains do not preserve well
in the archaeological record. Also, a significant plant component of
 real neanderthals did not eat quiche 187

the diet may be hidden by isotopic studies. The high values of N-15 in
the diets of Neanderthals are produced by their reliance of large herbi-
vores. Yet, according to paleobiologist Hervé Bocherens (the author of
many of these stable isotope studies), if low-nitrogen plants had con-
tributed up to 50 percent of the dry weight of Neanderthal diets, they
would not have altered these values (406). Thus, the archaeological as
well as the isotopic evidence are biased against plant foods. In recent
years, evidence is beginning to mount suggesting that Neanderthal
diets were more diverse than previously thought. The archaeological
record is filling in, and with it, evidence of Neanderthal consumption
of fish, birds, and a variety of plant foods at different times and places
is accumulating (409).

Into the Mouths of Neanderthals

Although archaeological evidence places such diverse food sources at
Neanderthal living sites, the dental evidence puts these foods right
into Neanderthal mouths. At Bolomor Cave in Spain, archaeologists
Ruth Blasco and Josep Peris found 202 bird remains dated to about
150,000 years ago, a time when only Neanderthals were in Europe
(410). The remains belong to diving ducks, from the genus Aythya.
Besides the stone tool cut marks and burnt areas on these bones, there
are human tooth marks. The authors identified these tooth marks as
human by comparing them to human tooth marks made by modern
foragers as well as to tooth marks made by other animals. Like human
tooth marks, those on the Aythya bones are small. They are concen-
trated around the broken edges of bones, and in some cases are asso-
ciated with the kinds of longitudinal fractures produced by human
gnawing. None of the tooth marks appear similar to those made by
carnivores or to the kinds of marks made by large birds of prey.
However persuasive these results may be, even more substantial
evidence of diverse foods in Neanderthal mouths comes from plant
microfossils trapped in Neanderthal dental calculus. In 2011, anthro-
pologist Amanda Henry and colleagues found phytoliths and starch
grains in the dental calculus of a 44,000-year-old Neanderthal from
188 knowing neanderthals through their teeth

Shanidar cave in Iraq and two 36,000-year-old Neanderthals from Spy

Cave in Belgium (411). As explained in Chapter 2, different plants
have differently shaped phytoliths, so it is possible to identify the
plants that produced them. Starch grains are the tiny granules some
plants use to store starch, and like phytoliths, they have diagnostic
features. In the Shanidar teeth, Henry and her coworkers found starch
grains from a tribe of plants that includes the wild relatives of wheat
and barley. Some of these had changes consistent with having been
cooked. Other starches appear to have come from legumes, while the
phytoliths were a match to those of date palms. As for the Belgian
teeth, they contained starch grains which appear to have come from
the tubers of water lilies.
But even more surprises came from the Neanderthal dental
calculus that formed the basis of Nature’s 2012 “Neanderthals ate
their greens” story. In their study of teeth from five 47,000–50,000-
year-old Neanderthals from El Sidron Spain, anthropologist Karen
Hardy and colleagues not only found starch granules, but they also
chemically identified organic compounds suggesting the consump-
tion of nuts, grasses, and even green vegetables (412). Furthermore,
they discovered the presence of compounds found in bitter-tasting
plants, such as yarrow and chamomile, which have little nutritional
value. It is known that Neanderthals had a gene allowing them to taste
such compounds, and Hardy’s team thinks that Neanderthals may
have used these plants as medicines. That’s not such a stretch of the
imagination because herbalists today used them as antiseptics and
anti-inflammatories. Even chimpanzees seem to have learned to
self-medicate. Tanzanian chimpanzees swallow whole bitter-tasting
leaves of the genus Aspilla that contain thiarubine A, a compound
that kills bacteria, fungi, and parasitic worms (413).
These two studies of dental calculus have clearly demonstrated
that diverse plant species were present in the mouths of Neanderthals
from different times and places. Yet, they represent only a handful of
individuals, and the presence of plant microfossils embedded in calcu-
lus does not attest to what degree Neanderthals relied on plant foods.
 real neanderthals did not eat quiche 189

New evidence from the study of dental wear, however, suggests that
plant use was neither restricted to a few individuals nor that plants
were eaten only occasionally.
Dental macrowear on permanent teeth (wear observable on teeth
without the use of microscopes) reflects the cumulative effect of
chewing different types of foods over an adult’s lifetime. In 2011,
anthropologist Luca Fiorenza and colleagues analyzed macrowear
patterns on nineteen Neanderthal teeth from as many individuals and
compared it to that of twelve early modern humans (414). They did not
find macrowear pattern differences between Neanderthals and modern
humans from similar environments, implying that where Neanderthals
and early modern humans had similar foods available, they ate similar
things. Where they both occupied deciduous woodland environments,
their macrowear patterns matched those of today’s humans who
include abrasive plants in their diets. And where they both inhabited
steppe and coniferous forests, their macrowear patterns matched those
of today’s humans who are predominantly meat-eaters. Similarly,
studying microscopic wear3 on Neanderthal teeth, anthropologist
Sireen El Zaatari’s team in 2011 concluded that Neanderthals from
wooded habitats included more plant material in their diets than did
those from steppe environments (415).
These dental findings, from tooth marks on bird bones to cooked
plant remains in Neanderthal dental calculus and geographic
variability in Neanderthal dental wear all weaken the assumption
that Neanderthal diets were narrow and inflexible. They suggest
instead that in some places, Neanderthals made use of a wide variety
of food types. If this is the case, then ideas discussed earlier about what
Neanderthal diets reveal about Neanderthal behavioral complexity,
extinction, and the sexual division of labor will, at the least, require
modification. Perhaps some of these ideas are more applicable in steppe
rather than in woodland or temperate environments. Yet, the similarity
in Neanderthal and Upper Paleolithic modern human macrowear

3
Microwear texture analysis, used in this study, is described in Chapter 2.
190 knowing neanderthals through their teeth

from similar habitats suggests that habitat, rather than differences in

behavior and technology, was the primary determinant of both of these
hominins’ diets. To paraphrase archaeologist Omar Bar-Yosef, both
types of hominins appear to have been “eating what was there” (416).

insights into behavior: anterior teeth as

“third-hands,” neanderthal table manners
and right-hand dominance
Analysis of tooth wear enlightens us not only about what
Neanderthals ate but also aspects of their behavior, specifically about
how they used their anterior teeth. Today, some of us use our
front teeth as “third-hands” in such tasks as popping caps off of aspirin
bottles. More talented (and thirsty) individuals use them to open beer
bottles. (There are detailed instructions on www.wikihow.com about
how to do this – with a warning about broken teeth.)
We know that Neanderthals used their anterior teeth in ways
that caused them to exhibit massive wear (Figure 5.6). The biting
surfaces of Neanderthal anterior teeth show “beveled” wear (417),
rounded wear, and are in general more worn than the biting surfaces
of their posterior teeth (418). In Neanderthals from such disparate
regions as Iraq (Shanidar I) and France (La Ferrassie), some anterior
tooth crowns were worn away completely (419, 420). Neanderthal
anterior teeth are also often chipped or fractured (421). Assuming
Neanderthals weren’t opening beer bottles with their front teeth,
what were they doing with them?
Considering this question (among others relating to tooth wear)
Steven Molnar noted that “nondietary” functions of anterior teeth
are often associated with heavy wear in several cultures (418). Such
functions include cracking or splitting bones, opening mollusk shells,
softening animal hides, using front teeth to clamp an object while
twisting the free ends with one’s hands, or using them to tear and
cut seal meat. Eskimos, who have extensive anterior tooth wear and
chipping, are noted to use their teeth in some of these ways and more,
such as tightening a harness by clamping the end between the
 insights into behavior: anterior teeth 191

anterior teeth and pulling backwards. Perhaps Neanderthals, too,

were using their anterior teeth to do more than just eat.
Kristin Kreuger and colleagues’ (422–424) comparative studies of
dental microwear have helped to answer this question. These research-
ers used microwear texture analysis to determine associations between
microwear texture variables and the diets and behavior of well-studied
archaeological groups. Krueger found that two microwear texture
variables – anisotropy and texture fill volume – were able to differenti-
ate among the anterior tooth microwear patterns of these groups (423).
As explained earlier (Chapter 2) anisotropy refers to the orientation of
features – high anisotropy means high directionality, while low
anisotropy is the reverse. High anisotropy reflects dietary uses, as
abrasive particles are dragged along the surface of incisors in the same
direction when biting into an object. Texture fill volume (Tfv) measures
feature depth. High Tfv is associated with high applied force or with
repeated use (loading) of anterior teeth, while low Tfv indicates the
opposite – low applied force or infrequent loading.
Ipiutak Eskimos of Point Hope Alaska have low anisotropy and
high Tfv, consistent with the customary of their use of their anterior
teeth as a “third hand” for softening hide. Sixty-five Neanderthals from
diverse regions were studied in Krueger and colleagues newest work
(424). Neanderthals from cold-steppe regions had microwear textures
similar to the Ipiutak, strongly suggesting they were employing their
teeth as “third hands,” as the Ipiutak did. Perhaps these Neanderthals
too were using their anterior teeth to process animal hides to survive
frigid, ice-age, conditions. By contrast, those Neanderthals from
warm/woodland regions had high anisotropy and lower Tfv, suggesting
that nondietary uses of teeth were far less frequent. As with the evident
environmental influences of Neanderthal diets, here, environmental
influences are associated with differences in Neanderthals’ use of ante-
rior teeth as “third hands.”
One of the other wear-related attributes of Neanderthal anterior
teeth are prominent long scratch marks visible with the naked eye
(Figure 8.2). Marie-Antoinette De Lumley first noted these striations
192 knowing neanderthals through their teeth

figure 8.2: Left: Oblique striations on the upper left central incisor of
Hortus 8. Right: Lines showing the approximate angles and length of
these striations on the same tooth. Illustration by author.

in the Hortus Neanderthal teeth in 1973, attributing them to a habit

seen in some Eskimos and Inuit, whereby a piece of meat is put into the
mouth, and then cut close to the mouth, frequently causing scratches
on the enamel surfaces of incisors and canines (425). Loring Brace
dubbed this eating tradition the “stuff and cut school of eti-
quette” (426).
The Sima de los Heusos hominins (427, 428) and Neanderthals
over a 100,000-year span seem to have had table manners similar to
those of Eskimos and Inuit. The long scratches on their anterior teeth
have the same appearance under a scanning electron microscope (SEM)
viz. parallel margins with an internal groove marked by tiny longitudi-
nal microstriations (427). Most convincingly, Lozano-Ruiz and collea-
gues (429) were able to generate these same markings experimentally.
They glued incisor teeth to buccal protectors (like those worn by ath-
letes) and had subjects wear these while they made cuts on them with
flint flake tools. Like the cuts on the fossil teeth, these cuts had a similar
appearance under the SEM – with the same diagnostic features.
Most intriguing about these scratches, though, is that they
are often oblique, in most cases coursing from the top left of the
tooth to the bottom right (here right and left refer to the perspective
 insights into behavior: anterior teeth 193

of the person whose mouth the teeth are in). In their experiment,
Lozano-Ruiz and colleagues had left-handed and right-handed people
make cut marks, and as you would expect, the right-handers predo-
minantly made scratches traversing the tooth surface from top left to
bottom right, while left-handers predominantly made scratches that
went from top right to bottom left (429). Taken together, of twenty-
nine Sima de los Huesos and Neanderthal individuals with anterior
tooth scratch marks, twenty-seven of the twenty-nine exhibit the
“right-oblique” marks made in high frequency by right-handers.
Only two exhibit the predominant “left-oblique” marks of left-han-
ders (430). Like modern humans today, most Neanderthal individuals
were right-handed. Although archaeological analysis of stone tools
also suggests a right-hand bias (perhaps as far back as the lower
Pleistocene), Frayer and colleagues point out that these analysis do
not reflect the population frequency of right-handedness, as stone
tools obviously don’t count as individuals (430).
A species-wide tendency toward right-hand preference is unique
to humans among primates. Although some great apes do show hand
preference, Frayer and coauthors (430) comment that population fre-
quencies of right handedness do not come close to approaching the 90%
frequency present in modern humans worldwide. Right-hand domi-
nance is a decidedly human trait that we shared with Neanderthals,
and one that goes back nearly 500,000 years. Whether right-hand dom-
inance indicates brain lateralization and language ability is debatable
(431), but David Frayer thinks it might be. The argument is based on the
fact that language ability is left-lateralized in humans and the left side
of the brain controls the right-side of the body. Hence, humans are
mostly right-handed, presumably because their brains have “left-cere-
bral dominance” (430). By extension, Frayer and colleagues argue that
this is one more piece of evidence (including others, such as the Kebara
2 hyoid bone ([432]) that Neanderthals were language-competent (430).
When David Frayer came to give a talk at Ohio State, he asked
me if I had noticed these oblique striations in any Neanderthals he had
not studied. When I looked back at my notes, I saw that had noticed
194 knowing neanderthals through their teeth

them in the Regourdou 1 Neanderthal, from southwestern France.

I showed him the dental replicas from this specimen and he was
intrigued because our colleagues Virgine Volpato, Roberto
Macchiarelli, Ivana Fiore, and Luca Bondioli had documented differ-
ences in the cross-sectional area of cortical bone in the skeleton
of Regourdou 1. The right upper limb of Regourdou 1 had a greater
cross-sectional area, indicating that it had been subject to higher
biomechanical loads, strongly indicating exactly what the oblique
striations did: Regourdou 1 was right-handed. In 2012 we published
these results, adding one more individual to the preponderance of
right-handed Neanderthals (433). Since then, still more have been
added to the list: 11 of 11 of the El Sidrón Neanderthals from Spain
also appear to have been right-handed (434).

stressed-out neanderthals?
Although the gap between the diets of Neanderthals and their early
modern human contemporaries is closing, this of course does not
mean that these two kinds of hominins were equally able to meet
their energy needs. For one thing, Neanderthals (as inferred from their
bones) were far more muscular than early modern humans. Greater
muscle mass may have been an adaptation to cold climates, giving
Neanderthals an ability to generate more internal body heat and pro-
viding them with better insulation. But, greater muscle mass also
takes more energy to maintain. Evolutionary anthropologists
Andrew Froehle and Steven Churchill estimated that primarily as a
result of their larger muscle masses, Neanderthals would have
required 100–350 kcal per day more than modern humans inhabiting
similar climates (435). (This begs the question of whether early mod-
ern humans were as capable as Neanderthals of resisting cold stress,
but some archaeological evidence suggests they might have done so by
making better-insulating clothing than Neanderthals did.) Froehle
and Churchill argue that the higher energy needs of Neanderthals
could have put them at an evolutionary disadvantage, as it takes
energy both to survive and to reproduce.
 stressed-out neanderthals? 195

figure 8.3: Linear enamel hypoplasias (denoted by arrows) on the upper

incisors and upper left canine of a juvenile specimen from Point Hope,
Alaska. (American Museum of Natural History Specimen 385.)
Photograph by author.

Unambiguous evidence of energetic stress does not exist in

skeletons and teeth, but two irregularities of teeth – linear enamel
hypoplasia and fluctuating asymmetry – are broadly indicative of
physiological stress. Physical anthropologists use the term “physiolo-
gical stress” to refer to external demands on the body that tax its
ability to maintain its normal state. Such stress include, but are not
limited to, nutritional stress. Linear enamel hypoplasias (LEHs) man-
ifest as grooves, of varying width and depth, in the hard enamel cover-
ing of teeth (Figure 8.3) (436). When physiological stress is severe
enough, it will disrupt enamel formation, leaving behind these linear
deficiencies in enamel thickness. Enamel does not repair itself after it
is formed, so these grooves become a permanent fixture of a tooth.
The other irregularity, fluctuating asymmetry, manifests as random
departures from symmetry in paired biological structures, such
as right- and left teeth. Normally, development proceeds equally
on both sides of the body, but physiological stress can disrupt
196 knowing neanderthals through their teeth

symmetrical development. Teeth do not grow in size after they have

formed, so differences in size between right- and left teeth represent
the cumulative result of such stresses during the tooth formation
period (437).

Personal Dental Impressions

I have studied both of these irregularities in Neanderthal teeth, but
began with linear enamel hypoplasia because in living humans, LEH is
most often associated with caloric deficiency, illness, or the combina-
tion of the two (436). In one prospective study, Mexican children who
received nutritional supplements were found to have half the fre-
quency of LEH of those who were not given supplements (438).
Some years ago, my colleague Zeynep Benderlioglu and I found ele-
vated levels of LEH in rhesus monkeys that grew up in a medical
colony before a consistent feeding program was established (439).
This is the colony on Cayo Santiago, a small island off of the cost of
Puerto Rico, where regular provisioning of monkeys was not estab-
lished until 1956.
Given the links between LEH and malnutrition, I traveled to
Israel and throughout Europe one summer, courtesy of the Leakey
Foundation, in part to study LEH in Neanderthals and early modern
humans, but also to collect data on Neanderthal fluctuating asymme-
try and enamel growth. This was a lot of fun because Neanderthal
remains are spread out across museums from various countries. So,
with my husband Dan Steinberg coming along for the ride (or actually
providing the ride, since, as he said, “Somebody had to drive the car,”),
I went from Tel Aviv to London, and from Berlin to Rome. Dan also
served as a French-English translator. With his two years of high
school French, Dan pled my case with Madame Marie-Antoinette de
Lumley (of the Institut de Paléontologie Humaine) to allow me to
study the Hortus fossils in Marseilles.
Previous studies suggested that Neanderthals had frequencies
of LEH that were at the top of the range found in archaeological
and living modern human populations. However, I wanted to get a
 stressed-out neanderthals? 197

more accurate read on Neanderthal LEH by applying some methods

previous studies had not. For one, I wanted to be sure that when I
counted an individual as being affected by LEH, the individual had
defects appearing on more than just one tooth. When LEH appears on a
single tooth it could be because of local causes (trauma, infection)
acting on that single tooth during development. When LEH appears
on two or more teeth at approximately the same time during tooth
development, it is more likely that the defects were caused by a
systemic stressor, such as malnutrition or illness.
I also wanted to get an estimate of the duration of the stress
episodes these LEH defects represented. Some grooves are wide, and
some are quite narrow, and to some extent their width is related to the
period of time enamel growth was disrupted. To get an even better
estimate of the length of stress events, it is possible to count enamel
growth increments within LEH defects. As described in Chapter 4,
microscopically observable enamel growth increments, perikymata,
cover the sides of teeth. Dental anthropologist Tanya Smith and col-
leagues determined that in Neanderthals, perikymata generally repre-
sent seven to eight days of growth (440). In modern humans, research
by dental anthropologists Donald Reid and Christopher Dean indi-
cates that the length of time represented by a perikyma (singular)
centers around eight to nine days (217). Through microscopic investi-
gation, dental anthropologist Simon Hillson and microscopist Sandra
Bond determined that LEH grooves usually take the form of V-shaped
furrows (441). Perikymata are more widely spaced than normal in the
top half of the furrow, reflecting the period of disrupted growth.
To count these growth increments, I made high-resolution impres-
sions of these teeth, followed by making high-resolution replicas, and
examined them under an SEM.4

4
I also used replicas of the Krapina Neanderthals, kindly provided by Clark Spencer
Larsen and Dale Hutchinson, who were included as coauthors in this study. (442.
Guatelli-Steinberg D, Larsen CS, Hutchinson DL. Prevalence and the duration of linear
enamel hypoplasia: a comparative study of Neanderthals and Inuit foragers. Journal of
Human Evolution. 2004;47(1–2):65–84.)
198 knowing neanderthals through their teeth

I compared the Neanderthals to a recent human foraging group

that inhabited a cold environment and that, like Neanderthals
included large mammals as an important component of their diets.
These were the coastal whale-hunting people known as the Tigara of
Point Hope Alaska, who occupied this region between AD 1300 and
1700. Of 18 Neanderthal individuals (from Krapina and southern
France), 7 were affected by LEH, which was quite similar in frequency
to the 8 of 21 Tigara individuals who exhibited LEH. Neanderthals
showed a range of defect durations, including defects with just 2
perikymata to a defect that had 12 perikymata in the top half of the
V-shaped furrow. Assuming that each perikyma represented 7 to 8
days of growth, the latter defect represents a growth disruption that
lasted from 84 to 96 days. But when I compared the average number of
perikymata in the top half of the “V” between my Neanderthal and
Tigara samples, these didn’t differ much.
To summarize, both Neanderthals and Tigara appeared to have
experienced a fairly high level of physiological stress, each with more
than a third of the individuals in their respective samples exhibiting
one or more enamel growth disruptions (442). Some of these disrup-
tions were of short duration and some were quite long, but the average
durations were not that different between the two groups. On the one
hand, this means that my research supports previous findings showing
high stress load in Neanderthals. On the other hand, it also suggests
that Neanderthals may not have been all that exceptional, as these
Tigara foragers inhabiting a cold climate were similarly stressed.
Of course, it would have been interesting to compare
Neanderthal LEH to that of their Upper Paleolithic modern human
contemporaries. That was something I had wanted to do, but I had too
few Upper Paleolithic teeth to work with. As the fossil record fills in,
it may be possible to eventually perform this comparison.
In a later study, my collaborators Chris Barrett, Paul Sciulli, and
I compared fluctuating asymmetry in the teeth of Neanderthals
and several archaeological groups, some of which were agricultural
and others of which were foragers, and once again we included the
 neanderthal development, growth, and death 199

Tigara (437). Although previous studies had suggested high levels of

fluctuating asymmetry in Neanderthal teeth, we felt that certain
methodological issues detracted from these studies, and we wanted
to correct them in our own. Yet, we confirmed these previous findings.
Neanderthals had higher levels of fluctuating asymmetry than our
comparative samples, and they were, not surprisingly, most similar
to the Tigara. Neanderthals do seem to have been sustaining high
levels of physiological stress during development, and this might
have had something to do with their high energetic demands.
Whether it has anything do with Neanderthal extinction is extremely
unclear. It may, however, have had an effect on the pace of
Neanderthal life histories.5

neanderthal development, growth, and death

Teeth have made a major contribution in recent years to the area of
Neanderthal life history, but the road to understanding has been full of
twists and turns. Along that road, Neanderthals at some points
seemed to have grown up more quickly than modern humans do; at
others, not so differently at all. Of all primates, humans take the
longest to grow up and reproduce, and they have the longest natural
lifespans. As discussed in the previous chapter, signs of protracted
dental development within the genus Homo are most clear for
Homo erectus, although this species rates of somatic growth may
been quite rapid, if analysis of the Nariokotome boy is an indication
(374). By the time of Homo antecessor, about 1 million years ago,
dental development seems to have shifted more toward the human
direction (377). But what about Neanderthals? In this book, I have
stressed the modular nature of development as well as the point that
one shouldn’t necessarily expect gradual shifts toward a modern
human life history over the course of human evolution. The complex
combination of selection pressures influencing a hominin species’ life

5
“Life history,” as discussed in Chapter 4, refers to the key benchmarks and stages in the
lifetime of an organism. For mammals, this includes gestation length, age at weaning,
age sexual maturity, age at first birth, the intervals between births, and finally death.
200 knowing neanderthals through their teeth

history can theoretically result in unique life history modes, and

has resulted in unique life history modes in living primates (186).
Viewed through the lens of life history “theory,” it isn’t clear
what to expect a priori for Neanderthals. Consider what one major
theoretical perspective, introduced by evolutionary biologists Eric
Charnov and David Berrigan (182), might mean for Neanderthal life
histories. According to these theorists, there are two countervailing
selection pressures affecting the optimal age of primate sexual matur-
ity. The first of these is adult mortality due to “extrinsic factors,”
meaning the risk of death by such causes as predation, disease, or
accidents. If that risk is high, the earlier a primate can start reprodu-
cing, the better for leaving lots of offspring. However, there is a limit to
how young a primate (especially a female) can be when she becomes
sexually mature and ready to have babies. Primate females, to varying
degrees, make use of fat stores as body “capital” to supply the energy
needed to gestate and nurse offspring. They cannot stint too much on
the time it takes to grow their bodies to a size large enough to sustain
pregnancy and lactation.
By this reasoning, if Neanderthals had a higher risk of dying
during adulthood than do modern humans, as some studies have
suggested, they would have been expected to grow up faster than
we do. Yet, if they were energetically challenged compared to
modern humans, they might have required a longer time to reach a
reproductively-competent adult body size.
Maybe we can gain more insight into what to expect by con-
sidering Neanderthal brain size and brain growth rates. In Chapter 4,
much was made of the relationship between brain size and the pace of
life history in primates. Whatever the connection, large-brained pri-
mate species take a long time to grow, and with brain sizes as great as
those of their anatomically modern human contemporaries and
greater than those of today’s humans, Neanderthals could be expected
to have taken just as long to grow up as we do.
Furthermore, rates of Neanderthal brain growth during the first
two years of life are estimated to have been quite rapid (443). Based on
 neanderthal development, growth, and death 201

Steve Leigh and Greg Blomquist’s maternal energetics hypothesis

(see Chapter 4), Neanderthal females could be expected to have had
long growth periods during which they achieved body sizes capable of
sustaining the energetic demands of nursing infants with fast growing
brains. And of course, if Neanderthal biology was characterized by all
of these factors: high adult mortality, high energetic stress and fast
brain growth rates, the predicted “life history outcome” would depend
on the magnitude of these factors, which are difficult to estimate with
precision.

What Do Teeth Have to Tell Us?

As previously explained (Chapter 4 and Chapter 7), the chronology
of tooth growth is preserved in incremental growth markings within
the enamel – the microscopic daily increments (cross-striations)
and the longer-period increments, striae of Retzius, that emerge
onto the enamel surface as perikymata. This chronological record
has been the subject of multiple studies on Neanderthal teeth over
the last twelve years.

Personal Dental Impressions

When I made high resolution dental impressions of Neanderthal teeth,
part of my plan was to count the total number of perikymata on each
tooth. I used anterior teeth – incisors and canines – because 85–90% of
their crown formation time is accounted for by perikymata on the
enamel surface. The remainder of their crown formation time is hid-
den at the tip of the crown – the cuspal region – where the internal
striae of Retzius do not emerge onto the tooth’s surface as perikymata.
Posterior teeth – premolars and molars – have a much greater portion
of hidden growth, and so I did not study these initially. By counting
perikymata in anterior teeth, and by using estimates of the number of
days perikymata take to form, I could obtain estimates for the time it
took for Neanderthals to form their anterior tooth crowns (actually for
85 to 90% of that time). Figure 8.4 shows perikymata on the surface of
a Neanderthal incisor.
202 knowing neanderthals through their teeth

figure 8.4: Montage made by author from scanning electron

micrograph (SEM) images taken at 20x magnification of a Neanderthal
lower I2 replica (Krapina 90).
 neanderthal development, growth, and death 203

When reading previous studies, I had been surprised that a

large-scale study of Neanderthal perikymata had not yet been under-
taken. After all, dental anthropologist Christopher Dean and
others had pioneered these methods in early hominins like
Australopithecus (223, 226). But, it turned out that a similar project
was indeed underway by anthropologists Fernando Ramirez-Rozzi
and Jose Maria Bermúdez de Castro. In 2004, these researchers
published a paper in Nature on 146 Neanderthal teeth from 55
individuals, concluding that Neanderthals formed their anterior
teeth more rapidly than did anatomically modern humans who
lived during and just after the Upper Paleolithic (444). The basis of
their conclusion was that the number of perikymata in comparable
divisions of Neanderthal and anatomically modern human teeth was
lower in Neanderthals. Their conclusion assumed that perikymata
in Neanderthals did not take any longer, on average, to form than
those of modern humans, which later research by Tanya Smith and
colleagues would substantiate (440). Ramirez-Rozzi and Bermúdez
de Castro interpreted the difference in anterior tooth formation
times between Neanderthals and these anatomically modern
humans as a species-level difference in growth rates. Neanderthals
grew their teeth quickly and must have grown up fast.
One year later, my colleagues and I published our results (445).
We compared fifty-five teeth from thirty Neanderthal individuals to
my Tigara samples from Alaska, and to my colleague Don Reid’s
samples from England and southern Africa. When compared to teeth
of these geographically dispersed modern humans, the numbers of
perikymata on Neanderthal teeth were not exceptional. The average
number was less than that of the Tigara teeth, variable by tooth type
when compared to that of the sample from England, and generally
greater than that of the sample from southern Africa. We considered a
range of possible estimates, based on modern humans, for the number
of days it took Neanderthal perikymata to form, concluding that
Neanderthals could not be definitively shown to have formed their
anterior teeth any faster than did some of these modern humans.
204 knowing neanderthals through their teeth

Lower incisor teeth, again based on a range of periodicity estimates,

even seemed likely to have formed more slowly in Neanderthals than
they did in the southern Africans. Clearly our findings weakened the
conclusion of a species-level difference between Neanderthals and
modern humans. Our study did not exactly endear us to the authors
of the Nature paper, who engaged us in a vigorous exchange in the
Journal of Human Evolution a few years later. But studies of periky-
mata on the surfaces of anterior teeth were about to be eclipsed.

Going beneath the Surface

Just one year after our study was published, dental anthropologist
Roberto Macchiarelli and coworkers published a study on how
Neanderthal teeth grew that involved sectioning a Neanderthal
tooth to actually determine the number of days it took to form the
internal striae of Retzius in enamel (446). They could also make use of
similar incremental growth lines that are present in the tooth root.
The tooth was an adult first molar, which is known to begin forming
right around birth. Given these pieces of information, it was possible
to determine the age at which the entire tooth (crown plus root) had
completed formation in this individual, which was close to the aver-
age age of nine years when this happens in modern humans. Based on
how much of the root is usually formed when teeth erupt into the oral
cavity, these authors estimated that this Neanderthal individual’s
first molar would have erupted at around 6.7 years of age, which is
no different from modern humans.
Although only based on a single Neanderthal individual, this
was stronger evidence of similar timing in dental development
between Neanderthals and modern humans than our study because
(1) the number of days it took to form growth increments was actually
determined by cutting into the tooth, and (2) the tooth was an adult
first molar. First molars have a special place in studies of primate life
history because of the foundational studies (discussed in Chapter 4)
establishing a strong association between adult first molar eruption
ages and the pace of primate life histories. That relationship is perhaps
 neanderthal development, growth, and death 205

a functional one, as adult first molars generally erupt around the time
primates are weaned, giving them more chewing power (but see
Chapter 4). No one has ever bothered to see if anterior tooth develop-
ment has such a strong relationship with primate life histories across
the order. As noted in previous chapters, anterior tooth crown forma-
tion times in chimpanzees are greater than those of modern humans
(196), suggesting that at least within the great and hominin clade,
anterior teeth may not be particularly reliable indicators of life
history.
Yet Macchiarelli and colleagues did not have the final word.
Tanya Smith and colleagues published three papers in succession that
seemed to settle the question once again in favor of rapid Neanderthal
dental development (440, 447, 448). Using x-ray synchrotron microto-
mography (see Chapter 4) these researchers could peer inside
Neanderthal teeth to determine how long it took for growth incre-
ments to form without having to slice into precious fossils. That
allowed them to look at more than just one tooth. For six immature
Neanderthal individuals who had not yet finished forming all of their
teeth, Tanya Smith and colleagues were able to count dental growth
increments to determine how old each individual was at the time of
death (449). This was possible by counting growth increments from the
neonatal line (an accentuated marking within the enamel that forms at
birth) to the last increment of growth that formed when the individual
died. They then scored the Neanderthal individuals for how far along
they were in their state of dental development when they died. It turned
out that Neanderthals had completed more of their dental development
than do modern humans at comparable ages. The Neanderthals’ entire
dentitions were developing at an accelerated pace.
End of story? Not quite. Two years later, Laura Shackelford and
colleagues published a paper asserting that there are several sources of
variation that need to be taken into account when using modern
human dental charts. Smith and coworkers had used modern human
dental aging charts to convert the stage of each Neanderthal’s dental
development into a “dental age” based on modern human standards.
206 knowing neanderthals through their teeth

These “dental ages” – i.e., the ages at which modern humans achieve
certain stages of crown and root development – were compared to the
actual ages of death as determined from the growth increment data.
Since their modern human dental ages were older than their actual
ages, Neanderthals were growing faster than modern humans do.
When Shackelford and colleagues incorporated the uncertainty
involved in converting stages of dental development into dental
ages, the dental ages of the Neanderthals spanned age ranges that in
four of six cases included their actual ages at death (451). The two
Neanderthals which are not encompassed by the 95% confidence
intervals were the older individuals: Scladina and Le Moustier.
Shackelford et al. note that for Le Moustier, estimated dental age
rests on the third molar (with half the root formed), as all the other
teeth are complete. That Le Moustier is advanced in M3 development,
is consistent with previous evidence suggesting that third molars are
advanced in both Neanderthals and early modern humans (450).
All of this leads to uncertainty about whether the Neanderthals
were as dentally advanced compared to modern humans as it first seemed
in the Smith et al. 2010 study. And, it is important to point out that the
ages at first molar eruption in the Smith et al. study, as well as that of the
Macchiarelli et al. study, were estimated to be within modern human
ranges (446, 449). My own view is that Neanderthals were not categori-
cally different from modern humans in their dental development, but
were simply at the fast end of the human developmental spectrum.
Finally, we have to remember that not all body systems may
develop at the same rate. It’s possible that this might be happening in
Neanderthals.6 Anthropologist Jesús Martín-González and collea-
gues’ in 2012 constructed height vs. age growth curves for
Neanderthals during infancy and early childhood for ten individuals
(453). They plotted the estimated heights (based on the skeleton)

6
In fact, this was first suggested by anthropologists Jennifer Thompson and Andrew
Nelson (452. Thompson JL, Nelson AJ. The place of Neanderthals in the evolution of
hominid patterns of growth and development. Journal of Human Evolution. 2000;38
(4):475–495.)
 neanderthal development, growth, and death 207

of these individuals against their chronological ages at death as

determined from modern human dental standards (and in a few
cases, based on more accelerated estimates of rates of dental develop-
ment in Neanderthals). Their result: Neanderthals were growing in
height much more slowly than modern humans. This difference
would make sense if Neanderthals were energetically stressed and
could not support rates of brain and body growth equivalent to those
of modern humans. It’s not clear whether their slow growth was an
evolutionary adaptation or an individual-level response to energetic
stress. Furthermore, the extent to which these ten individuals repre-
sent Neanderthals in general is not clear, particularly because they all
died at young ages. That is to say, did they die at young ages in part
because they were particularly nutritionally stressed? In any case,
children eventually do grow up, reproduce and die, and it’s that last
life history event where teeth again emerge into the limelight.

Dying Young
As explained in Chapter 7, Rachel Caspari and Sang-Hee Lee compared
the number of young versus old individuals in fossil assemblages from
Australopithecus to modern humans using wear-based seriation (370).
They defined “old” adults (thirty years of age) as those that were twice
the age at which sexual maturity is reached (assumed to be fifteen
years of age) because they were interested in how many potential
grandparents might have been around. The existence of overlapping
generations is thought to give modern humans the benefit of learning
from their wise and experienced elders. Furthermore, grandmothers,
according to Hawkes’ Grandmother Hypothesis provide much needed
assistance as allomothers (366). In addition, with long lifespans, mod-
ern humans have many years over which to produce children, which is
an evolutionary plus. Caspari and Lee found that 30,000 years ago,
during the Upper Paleolithic, the number of older versus younger
individuals in modern human fossil assemblages took a quantum
leap. Neanderthals, by contrast appeared to have died young (though
not as young as did earlier hominins).
208 knowing neanderthals through their teeth

A few years later, Anthropologist Erik Trinkaus confirmed that

there is a high ratio of young to old individuals in Neanderthal fossil
assemblages, but contrary to Caspari and Lee, he found similar ratios
in Upper Paleolithic modern humans (454). About 75 % of both types
of hominins died before reaching the age of forty. The reason for
the discrepancy in these two studies isn’t clear, though it may have
to do with subtle differences in their methods and samples. But if
Neanderthals and Upper Paleolithic modern humans both died
young, then the Neanderthals’ anatomically modern human contem-
poraries did not have the evolutionary advantages of a long lifespan
associated with people today. Surely, modern medicine has length-
ened human lifespans, but the question is whether even prior to
medical advances, our modern human ancestors were living longer
than their Neanderthal cousins.
Still, all of this discussion must be tempered by the fact that no
one really knows the extent to which the ratio of old to young indivi-
duals in fossil assemblages resembles that of the once- living popula-
tions they came from. As Trinkaus points out, these could differ for a
variety of reasons, including biases produced by burial practices favor-
ing a particular age class or by the preservation potential of older
versus younger skeletons. There are problems then, but at present, it
seems that Neanderthals, and maybe also modern humans of the
Upper Paleolithic, died young relative to the generally longer-lived
(366) hunter-gatherers of today.

chewing on neanderthal debates

Science is in a never-ending process of revision, so we will probably
never know the whole truth about Neanderthals. But we can
consider where the different lines of dental evidence lead us. In terms
of Neanderthal origins, analysis of dental morphology suggests even
greater time depth (more than 1 million years ago) than do genetic
studies regarding the initial divergence between Neanderthals and
modern human. Yet, as revealed by dental studies, several aspects of
Neanderthal biology do not appear so different from those of modern
 chewing on neanderthal debates 209

humans. In terms of right-hand dominance, Neanderthals were like

modern humans. Evidence from tooth marks, dental calculus and
tooth wear of Neanderthals suggests that their diets were not radically
different from those of their anatomically modern human contempor-
aries. Their experience of physiological stress during childhood appears
to have been high relative to other modern humans prehistoric groups,
but it is not clear that Neanderthals were completely outside the range
of “stress levels” these groups experienced (see also [455]).
Neanderthals were on the fast end of the human range in their dental
development, but they may have had slower rates of skeletal growth
during infancy and childhood. They probably did not often live to see
their grandchildren, but that also may have been true of the anatomi-
cally modern humans with whom they coexisted.
The differences seem subtle, but even seemingly subtle differ-
ences can influence evolutionary outcomes. One might speculate that
with extensive dietary overlap, Neanderthals would have competed
for resources with their modern human contemporaries. Resource
competition might have put energetically challenged Neanderthals
at a disadvantage. With less energy available for growth, their skeletal
and somatic growth rates during childhood would have been slow, and
they may have reached sexual maturity at later ages than do modern
humans. Coupled with young ages at death, delays in sexual maturity
might have meant that Neanderthals produced fewer offspring during
their lifetimes than did their modern human competitors. That’s one
scenario. But speculative scenarios like these, which abound in the
Neanderthal literature, are only useful for pointing out that subtle
differences in life history could have had evolutionary ramifications,
not whether they actually did.
Speculation about the Neanderthal extinction question will
probably continue for as long as humans are around to think about
it. To me, what is more interesting is that through dental studies we
have gained some surprising insights into what life was like for
Neanderthals. Neanderthals now seem to have been smart enough to
have captured and eaten elusive prey, to have eaten a variety of plant
210 knowing neanderthals through their teeth

foods, and to have used plants as medicines. They experienced

elevated levels of physiological stress, had somewhat faster rates of
dental development and somewhat slower rates of skeletal growth,
and probably died young. This vision of Neanderthal lives comes into
focus through the unique attributes of teeth: unlike other parts of the
skeleton, they interact directly with food and they chronicle their own
growth in real time. Here, as is evident throughout this book, teeth
have given us an exclusive source for understanding the lives of our
ancient predecessors. While the present chapter highlighted multiple
insights into Neanderthal nature that teeth provide, the next chapter
focuses on dental insights into modern humans.
9 Insights into the Origins of
Modern Humans and Their
Dental Diseases

They [wisdom teeth] do not cut through the gums till about the
seventeenth year, and I am assured by dentists that they are much more
liable to decay, and are earlier lost, than the other teeth.

– Darwin CR
The Descent of Man and Selection in Relation to Sex, Vol.1

In 1871, in the “Descent of Man,” Charles Darwin speculated that

human third molars, or “wisdom teeth,” were evolving into rudi-
mentary structures (115). Such structures, he explained, tend to be
highly variable and reduced in size or even “wholly suppressed.”
Wisdom teeth fit this definition well in that they show great varia-
bility in size, shape, and development. Furthermore, although the
congenital absence of third molars is extremely rare in great apes
(456), it is quite common in humans, with a worldwide frequency (at
least one missing third molar) of 22.63% according to a new meta-
analysis (260).
The reduction or absence of third molars can be viewed as part of
the larger trend of dental reduction in recent human evolution, one of
several aspects of modern human biology that the study of ancient
teeth illuminates. Dental studies also give us insight into the phylo-
genetic origins and patterns of dispersal of anatomically modern
humans (AMHS) out of Africa, our long developmental periods, and
the evolutionary history of our dental diseases. In detailing these
insights, I develop two main themes. The first is that some of these
aspects of modern human biology are interrelated. As one example,
our present long lifespans may give us a reproductive payoff in off-
spring number and/or offspring survival, but longer lifespans require
teeth to function for longer periods of time, increasing the risk of
dental disease.

211
212 origins of modern humans and their dental diseases

The second theme is the dynamic relationship between culture

and biology in the evolution of modern human dental reduction and
dental disease, both of which have been influenced by changes in diet,
food processing, and eating habits. Nevertheless, much remains to be
understood about the extent to which differences among cultures over
time and space can be linked to population patterns of dental reduc-
tion and dental pathology. In Chapter 7, I discussed the case of dental
reduction in the Sima de los Huesos Homo heidelbergensis hominins,
which José Bermúdez de Castro’s analysis suggests has more to do
with genetic drift than with culturally-induced relaxed selection on
tooth size. Cultural variation over time and space has surely had
a great impact on patterns of modern human dental reduction and
pathology, but as with the case of the Sima de los Huesos hominins,
there are limits to how much culture can explain.
But before exploring these topics, we first address dental
insights into two other aspects of modern human biology: (1) What
do teeth tell us about modern human origins and dispersal out of
Africa? and (2) Can teeth tell us whether the first anatomically mod-
ern humans were like people today with respect to the length of their
childhoods?

teeth and modern human origins

In Chapter 6, different models of human origins were reviewed.
These range from the Recent African Origins model, which at one
extreme posits a replacement of archaic hominins by anatomically
modern humans from Africa, to the Multiregional Evolution model
at the other, which hypothesizes evolution from earlier hominins
into modern form in multiple regions of the world. In their review
of these models, Weaver and Roseman (457) explain that the
genetic evidence for the importance of sub-Saharan Africa in
the origin of modern humans is now widely accepted, but that
there is dispute about how much admixture with earlier hominins
occurred as anatomically modern humans from Africa dispersed
into new regions.
 teeth and modern human origins 213

The number of dispersals of anatomically modern humans out

of Africa is also disputed. Some genetic analyses suggest a single dis-
persal (315, 319). Other genetic and craniometric analyses find evi-
dence of multiple dispersals (317, 458, 459). The recent genetic and
craniometric study of Reyes-Centeno and colleagues suggests an early
dispersal out of Africa, via a southern route across the Arabian penin-
sula, into Asia around 130,000 years ago (317). Based on analyses of
both their DNA and crania, indigenous Australians appear to be
directly descended from these initial migrants (317, 460). A second
dispersal of out of Africa, through the Levant region, and into northern
Eurasia appears to have occurred around 50,000 years ago (317).
I have repeatedly asserted that comparisons of dental morphol-
ogy among species provide insight into their phylogenetic relation-
ships. Biological anthropologist Amelia Hubbard (together with
dental anthropologist Joel Irish and me) recently confirmed that
DNA and dental morphology data produce similar answers about
population relationships within a single species – humans.
Specifically, we found that for living people in Kenya, both genetic
and dental data taken from the same individuals clearly differentiated
populations of “Swahili” origin from populations of “Taita” origin
(461). So, what does the evidence from dental morphology say about
modern human origins and dispersal out of Africa and is it consistent
with genetic and craniometric lines of evidence?
Based on his comprehensive analyses of teeth from thousands of
modern people, the late dental anthropologist Christy G. Turner (462)
concluded that of all people in the world, Southeast Asians are the
“least specialized” dentally. Essentially what this means is that
Southeast Asians exhibit crown and root traits at frequencies that
are intermediate between those of other peoples of the world. Turner
referred to their “generalized” dental pattern as “Sundadonty,” after
the Sunda shelf, an extension of the continental shelf of Southeast
Asia that was exposed during the last ice age when sea levels receded.
Mainland Southeast Asia would have been connected to the islands of
Java, Borneo, and Sumatra, facilitating gene flow, and presumably
214 origins of modern humans and their dental diseases

s
al
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si
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ea

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M lia
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Ea e
in

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Au a

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figure 9.1: Cladogram redrawn by author based on Figure 1a from
Stringer et al. (1997). See text for explanation.

resulting in the common dental morphology of people in this region.

Turner argued that because Sundadonty is generalized, it is the closest
to the ancestral dental pattern of anatomically modern humans.
Southeast Asia, rather than Africa, he then concluded, would be the
most likely place of origin for modern humans. Based on phenetic
analyses, Turner additionally found a close connection between sub-
Saharan Africa and Australia (463), a connection which he seemed
unable to explain.
Stringer and colleague’s cladistic analysis of modern human den-
tal morphology (introduced in the previous chapter) made it possible to
separate primitive (ancestral) and derived traits and so to provide much
needed clarification about biological relationships among modern
human populations. Using the Krapina Neanderthals as an outgroup,
these researchers found that sub-Saharan Africans branched off from
our common ancestor with Neanderthals earlier than did other modern
human groups. Next to branch off – i.e., the second “least-derived”
group – were Australians. Europeans and people from Northeast Asia
(China, Japan, and Siberia) were more derived in their morphology,
branching off later (Figure 9.1). The analysis suggested that the modern
human “dental ancestor” had, among other characteristics, low fre-
quencies of upper incisor shoveling, low frequencies of third molar
reduction, and a high frequency of upper first molar fifth cusp.
 teeth and modern human origins 215

Different from Turner’s phenetic analysis, Stinger et al.’s cladis-

tic one suggested that Southeast Asians did not have the greatest
frequency of ancestral dental features – instead, Africans and
Australians did. Furthermore, the affinity between sub-Saharan
Africans and Australians that Turner noted was now shown to be
simply the result of shared ancestral features.
Dental anthropologist Joel Irish and I performed a follow-up
study to that of Stringer and colleagues, building on Irish’s previous
work on sub-Saharan dental morphology. Irish had previously con-
cluded that sub-Saharan Africans retained a greater number of ances-
tral features than other peoples of the world (464). Using Irish’s data on
dental morphology from modern peoples, together with my data on
dental morphology from australopiths and early Homo, we found that
sub-Saharan Africans were least far removed from “gracile” hominins
(Australopithecus combined with early Homo) in their dental mor-
phology. Australians and Melanesians, likewise, retained many ances-
tral features and were therefore also relatively close to early hominins
(Figure 9.2).
Our analysis reinforced Stringer and colleagues’ conclusion of
an African origin for anatomically modern human dental morphology.
Our analysis also showed that as distance from Africa increases, den-
tal morphology becomes more derived, with East Asian and European
populations diverging in different ways. This result is evident in
Figure 9.2, where Europeans and East Asians are most distant from
the combined “gracile hominins” and are also widely separated from
each other. These results – from Stringer et al. and Joel Irish and
me – are consistent with the now overwhelming genetic evidence of
African origins for modern humans. They are also consistent with the
great antiquity and retention of ancestral features in Australian popu-
lations that the multiple-dispersal model posits. Australians therefore
appear to retain genetic, cranial, and dental signals of an early disper-
sal out of Africa.
Although the idea of an early migration of anatomically modern
humans from Africa via a southern route across the Arabian Peninsula
216 origins of modern humans and their dental diseases

1.5
EUR WSA
1.0 NAF

1.0
SSA

1.0 AAR POL MEL “gracile”

CHM MIC
NES
–0.5 AUST
NSA
“robust”
–1.0

–1.5
–2 –1 0 1 2 3

figure 9.2: Multidimensional scaling graph (redrawn by author) based

on biodistance measures in Irish and Guatelli-Steinberg (2004).
Abbreviations are as follows: EUR = Europe, NAF = North Africa, WSA =
West South Asia, SSA = sub-Saharan Africa, POL = Polynesia, MEL =
Melanesia, MIC = Micronesia, AUST = Australia, AAR = American
Arctic, CHM = China-Mongolia, NES = Northeast Siberia, NSA = North
and South America. “Robust” = robust australopiths and “Gracile” =
sample of nonrobust australopiths and early Homo. Details regarding
these samples and methods used to generate the graph are in Irish and
Guatelli-Steinberg (2004).

into Asia and Australia is supported genetically, cranially, and den-

tally, it is less well-supported by direct fossil evidence. As Reyes
Centeno et al. note, there is, as yet, no fossil evidence of modern
human presence in the Arabian Peninsula around 130,000 years ago
that would support this idea (317). On the other hand, in China,
a fossilized mandible with a chin, a distinctive modern human feature,
was recovered from the site of Zhiren Cave (465) dated to more than
100,000 years ago. Furthermore, 70,000–127,000 year old teeth from
the sites of Luna Cave (Guangxi) (466) and 81,000–101,000-year-old
teeth from Huanglong Cave (Hubei) (467) have size and shape affinities
to recent modern human teeth. Evidence of an early dispersal from
Africa into Asia is therefore accumulating.
It may be recalled from Chapter 6 that the high frequency of
shovel-shaped incisors in East Asian Homo erectus and later East
Asian hominins, including anatomically modern East Asians, has
 dental development and growth 217

been cited as support for the “Multiregional Continuity” hypothesis.

In particular, it was argued that high frequencies of “marked” shovel-
ing are specific to East Asian fossil hominins and are also prevalent in
peoples of East Asian descent today(468).1 Incisor shoveling is not the
only dental trait to show apparent continuity in East Asia. Wu Liu, of
the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP)
in Beijing, identified seven dental traits typically present in modern
East Asians that were also present to varying degrees in fossil homi-
nins from East Asia (468). These include marked incisor shoveling,
third molar agenesis (or reduction), and three-rooted lower molars, all
of which are less common in other areas of the world. But these
observations do not lend exclusive support to the “Multiregional
Continuity” hypothesis. Interbreeding between archaic East Asian
hominins and anatomically modern people dispersing from Africa
can also explain the persistence of these dental traits over time.
The analysis of dental morphology is therefore entirely consis-
tent with an African origin for anatomically modern humans, coupled,
at least in East Asia, with genetic input from archaic hominins. As we
turn to next, the analysis of growth increments in teeth shows that
dentally, these early African anatomically modern humans had
achieved modern human developmental rates.

dental development and growth in early

anatomically modern humans
Dated to approximately 160,000 years ago (470), the Jebel Irhoud hominin
remains from Morocco share several derived features with anatomically
modern humans (471) but also retain some primitive features.
Paleoanthropologist Jean-Jacques Hublin suggests that the combination
of primitive and derived traits in these fossils remains reflects the gradual
1
Shovel-shaped incisors were critical to elucidating the East Asian origins of Native
Americans. Aleš Hrdlička, founder of the American Journal of Physical Anthropology,
was the first to note the high frequency of shovel-shaped incisors in both East Asians
and Native Americans and grasp their importance as indicators of ancestry. (469.
Hrdlička A. Shovel-shaped teeth. American Journal of Physical Anthropology.
1920;3(4):429–465.)
218 origins of modern humans and their dental diseases

evolution of anatomically modern form in Africa (472).

Paleoanthropologists Matt Cartmill and Fred Smith (15) consider the
Jebel Ihroud hominins to be part of an “African Transitional Group,”
that is “. . . considerably more like modern humans than Neanderthals,
though they retain some archaic features” (2009:422).
The Jebel Irhoud fossil remains include a complete cranium (Jebel
Ihroud I), but from the standpoint of development, the more exciting
remains from this site are the teeth and jaws of the juvenile, Jebel Irhoud
3. In 2007, Tanya Smith and colleagues used synchrotron x-ray micro CT
to image incremental markings in the juvenile’s teeth establishing its
stria of Retzius periodicity (ten days), crown and root formation times,
state of dental development and age at death (470). With large crowns that
the authors term “macrodont,” Jebel Ihroud’s crown formation times are
at the long end of the modern human spectrum. Jebel Irhoud 3 was
estimated to have died at 7.78 years age. Its state of dental development
is just what would be expected of a modern human child of equivalent age
in that its premolars and second permanent molar had begun to form
their roots. Modern Europeans in this stage of development are between
7.2 and 7.6 years of age. The lateral incisor is nearly fully erupted, an
event that usually occurs between seven to eight years of age in European
children (470).
Despite the modernity of its state of dental development, Jebel
Ihroud 3 appears to have had extremely accelerated rates of root forma-
tion relative to that of living humans. The authors estimate root forma-
tion rates in this specimen to be twice what they are today (470). Smith
and coworkers suggest that the juvenile’s longer periods of crown forma-
tion coupled with its fast rates of root formation result in eruption
timing comparable to that of living humans. If this is so, then Jebel
Ihroud 3’s dental eruption schedule is like that of living Europeans but
is not achieved in quite the same way. The modern scheduling of Jebel
Irhoud 3’s dental development indicates that prolonged juvenile growth
periods were present in anatomically modern humans 160,000 years ago,
but that not all aspects of human dental growth and development had
reached their current state.
 dental development and growth 219

Other early anatomically modern humans also retain some

dental growth differences from modern humans. Overall, the
90,000– 100,000 year old hominins from Qafzeh in Southwest Asia
have been said to exhibit an anatomical pattern of “derived modern
human features with a minority of retained archaic features” (473).
These hominins are thought (by some) to represent an early migra-
tion out of Africa that did not give rise to living humans today (317,
459). Smith et al. found that Qafzeh 10 did not differ from living
humans in the scheduling of its dental development (449).
However, my colleague Donald J. Reid and I found that the distribu-
tion of perikymata on the enamel surface of Qafzeh anterior teeth
tends to differ from that of living people today from diverse regions of
the world – South Africa, Europe, and Alaska (474). Thus, with both
Jebel Ihroud 3 and the Qafzeh anterior teeth, there are some aspects of
dental growth that are not quite modern even though the scheduling
of dental development does seem to be.
As has emerged in previous discussions in this book, skeletal
growth and development also require consideration in assessments of
developmental periods. We have seen that it is possible for the pace of
skeletal and dental growth to differ, and if they do, then interpreting
what they mean for the overall length of juvenile growth periods
becomes unclear. Recall that the “life history mode concept” charac-
terizes a species’ life history strategy in terms of its particular
combination of developmental rates and scheduling in different sys-
tems – dental, somatic, and reproductive – in recognition that natural
selection can act independently on these different systems (186).
Characterized in this way, a fossil species unique combination of
developmental rates becomes the subject of further inquiry. The life
history mode concept therefore provides a more productive approach
to understanding fossil species life histories, and we currently do not
have the evidence to reconstruct rates of skeletal growth in these early
hominins to help fill in the picture
Though moving in a modern direction developmentally, the
teeth of Jebel Irhoud 3 are nevertheless quite large by modern
220 origins of modern humans and their dental diseases

standards (470) as are those from Qafzeh (326). Dental reduction in

anatomically modern humans happened later in time, as we turn to
next.

dental reduction redux

When we last encountered paleoanthropologist C. Loring Brace it was
in the context of dental reduction at an earlier stage in the genus
Homo. Brace and colleagues devoted even greater effort to understand-
ing patterns of dental reduction in more recent times. In 1987, Brace,
Rosenberg, and Hunt published a major paper in the journal Evolution
in which they calculated rates of tooth size reduction in multiple areas
of the world since the onset of the last glaciation, 100,000 years ago
(326). Before this time, throughout the Middle Pleistocene, tooth size
remained relatively stable. In their analyses, Brace et al. used
a summary measure of the cross-sectional area of all teeth of the
dentition. From 100,000 to 10,000 years ago (the end of the
Pleistocene), the mean of this summary measure reduced gradually
at a rate of 1% per 2,000 years. Since the end of the Pleistocene,
though, and coincident with the beginnings of agriculture, the rate
of dental reduction doubled to 1% per 1,000 years in diverse regions of
the world. The exception was Australia, where tooth size remained
relatively stable up until the end of the Pleistocene, only undergoing
reduction more recently.
Brace and his coauthors explained these trends in relation to
cultural changes that relaxed selection on tooth size. In their view,
during glacial times, survival in northern regions required the
ability to cook frozen food “. . . if for no other reason than simply
to thaw it to the point where it can be eaten” (1995: 715). Such
“obligatory cooking,” as Brace called it, had the effect of softening
food. In Brace’s view, dental reduction then followed as
a consequence of relaxed selection on tooth size and the Probable
Mutation Effect (see Chapter 6). In support of this explanation,
Brace and colleagues (1987) observed that dental reduction has
been greatest in the areas of the world where cooking has been
 dental reduction redux 221

routine for the longest periods of time – in the northern regions of

Europe and Asia. As Brace put it “. . . the fossil record shows
a degree of dental reduction strictly proportional to the length of
time that the ancestors of the sample had been dependent upon
cooked food for their survival” (1995:715).
The accelerated rate of dental reduction over the last 10,000
years was attributed to the development and use of pottery and
“pounding, grinding and milling” tools (326). Such tools softened
plant foods that were otherwise to hard or tough to eat. Pottery made
it possible for foods to be processed to “drinkable consistency.” Brace
et al. point out that for the first time in human history, sizeable
numbers of people were surviving to old age with few remaining
teeth in their jaws. Teeth were becoming almost nonessential. In the
view of Brace and colleagues, these changes further relaxed selection
pressures, quickening the pace of dental reduction via the Probable
Mutation Effect (PME).
These are fascinating observations because they imply that cul-
tural evolution has strongly influenced dental evolution. On the other
hand, not all changes in dental reduction can be clearly chalked up to
culture. In his review of Brace’s studies, the late Jules Kieser pointed
out that “technological sophistication” and tooth size are not inver-
sely related. As an example, he offers the hunting and gathering south-
ern African San, who employ a hunting and gathering set of tools but
who nevertheless have incisor teeth smaller in size than those of most
other peoples (349). In a similar vein, commenting on one of Brace’s
papers in Current Anthropology, dental anthropologist Patricia Smith
asked, “Do Brace and Hinton seriously consider that the presence of
Middle-Pleistocene teeth in recent populations as diverse as
Amazonian Indians and Australian Aborigines means that they have
Middle Pleistocene technologies?” (1981:561).
Peter White of the University of Sydney in Australia notes that
food processing tools such as seed grinders go back 17,000 years in
Australia, but that the greater part of dental reduction in Australian
aborigines occurred much later, around 6,000 years ago. There seems
222 origins of modern humans and their dental diseases

to be a mismatch between technological change and dental reduction

that is difficult to explain based on the cause-effect relationship
between the two that Brace and colleagues hypothesized. Some evolu-
tionary lag time is to be expected but it is not clear how much to allow
before rejecting their hypothesis.
These criticisms do not negate the importance of culture in
relaxing selection pressures on teeth. They, do, however, suggest
that patterns of tooth size variation across the modern world must
also reflect other influences, such as genetic drift, gene flow, and/or
currently unidentified selection pressures. Roberto Macchiarelli and
Luca Bondioli suggested that tooth size could have reduced simply as
a consequence of body size reduction (475). Their evidence came from
the rapid reduction in both stature and tooth size across the transition
from Pleistocene hunting and gathering to sedentary agriculture
10,000 years ago. The problem with this view, as many have noted,
is that other studies find very low correlations between body size and
tooth size in humans (349).
While Brace saw the PME as the mechanism underlying den-
tal reduction in modern humans, others have made a compelling
case for tooth-jaw size mismatch as a strong selection pressure
(355). The idea (see Chapter 6) is that softened foods do not stimu-
late jaw bones do to grow to a size large enough to accommodate
big teeth. Consequences include crowded, malpositioned, and
impacted teeth, all of which increase the risk of dental disease
and in some cases, can lead to death.
A skeletal series from the Iron Gates site of Vlasac, Serbia span-
ning the years from 6300 to 5300 BC offers correlational evidence of
this mechanism in action. In this study, archaeologist Gloria
Y’Edynak found that diet did not change over the thousand year per-
iod, but technology did: flint “microliths” with sharper edges were
becoming used more frequently over time (476). Concurrently, jaw
dimensions decreased. In the earlier period of this 1,000 year span,
anterior teeth exhibited high frequencies of crowding and rotation.
In the later period, tooth size decreased. Y’Edynak’s data are
 dental reduction redux 223

consistent with a cause-effect relationship: decreased jaw size with

dental crowding precedes the reduction in tooth size.
The selective mechanism, in Y‘Edynak’s view was periodonti-
tis – a severe gum infection. Tooth crowding can create pockets
around teeth in which the bacteria causing periodontitis proliferate.
The infection triggers the immune system’s inflammatory response
in which blood plasma and white blood cells seep into the infected
area. As a result, the tissues that anchor a tooth in its socket – the
periodontium – become loose. Bone is resorbed and the tooth can
be lost (74). Y‘Edynak maintained that tooth loss itself could have
affected survival, but the extent to which this was true isn’t clear.
There are no data in this study on the numbers of individuals surviv-
ing to old age with missing teeth that would give some indication of
the effects of tooth loss on survival.
Still, there are other reasons besides tooth loss to think that
periodontal disease might affect reproductive success. Recent studies
suggest that periodontitis is associated with heart disease (477) and
premature birth (478). Severe dental infections can lead to life-
threatening sequelae, such as septicemia (blood infection) or caver-
nous sinus thrombosis (a blood clot in the cavernous sinus, at the base
of the brain). Y’Edynak’s study provides a circumstantial case that
changes in culture (here changes in stone tool technology) can pre-
clude jaws from growing large enough to accommodate large teeth,
resulting in dental infections that decrease the reproductive success of
large-toothed individuals. In this situation, genes for smaller teeth are
preferentially passed down to subsequent generations.
Third molar agenesis would seem to be related to the overall
trend of dental reduction. The third molar is particularly vulnerable to
impaction, as it is the last tooth to erupt into the oral cavity. Wisdom
teeth that have trouble erupting can trap food and plaque, resulting in
severe infection (see Chapter 6). According to one study, there is
evidence that selection acted specifically on a gene mutation asso-
ciated with third molar agenesis in humans – the Ala240Pro mutation
of the PAX 9 gene (479). The authors of the study suggest that natural
224 origins of modern humans and their dental diseases

selection would have favored individuals who harbored this mutation.

While that is certainly possible, the worldwide distribution of this
mutation does not coincide with worldwide patterns of third molar
agenesis. The Ala240Pro mutation is more common in Europeans
than it is in Asians (479), but Asians have a greater frequency of
third molar agenesis than Europeans do (260).
It is possible that third molar agenesis in modern humans is, in
part, a genetic or developmental correlate of overall dental reduction.
There is a connection between reduced tooth size and third molar
agenesis (480) – individuals with smaller teeth are more likely to
have congenitally absent third molars. Why might the size of other
teeth have anything to do with third molar agenesis? An answer might
be found in the “Inhibitory Cascade Model” of tooth formation.
The model relies on the elegant experimental work of Kavanagh and
coworkers (481). These researchers grew mouse tooth germs in vitro,
finding that molecular inhibitors made by the first molar tooth germ
caused a delay in the initiation of the second molar tooth germ.
The delay reduced the time available for the second molar tooth to
form, producing a second molar of smaller size than the first or even
a completely missing second molar. When Kavanagh and colleagues
cut the connection between the first and second molar tooth germs,
the second molar was “rescued” from this inhibition.
From first to second to third molars, there is a “cascade” of
inhibition, whereby first molars inhibit second molars, and second
molars inhibit third molars. The magnitude of inhibition depends on
the strength of activating and inhibiting molecular signals emanating
from tooth germs. Kavanagh et al. developed a mathematical model
for predicting the size of molars based on the strength of activation and
inhibition and the position of molars along the tooth row. The model
predicts that greater inhibition relative to activation causes
a progressive decrease in molar size from first to second to third
molars. The model further predicts that when the second molar falls
below one-half the size of the first, the third molar does not form at all.
 dental reduction redux 225

While the inhibitory cascade model offers a proximate explana-

tion for how third molar agenesis occurs and relates it to the relative
size of other molars, it is not currently known whether the model can
explain variation in third molar agenesis among modern human popu-
lations. The model is not able to explain third molar agenesis in the
Callitrichine subfamily of New World monkeys (482). This subfamily
always lacks third molars, but the second molar is not less than one-
half the size of the first. In other words, the Inhibitory Cascade Model
would predict that the third molar should form in this subfamily, but
it does not. Mutations in the PAX 9 gene do not explain third molar
agenesis in Callitrichines either, because both Callitrichines and
squirrel monkeys have identical mutations, and squirrel monkeys
have third molars.
Another factor to consider in third molar reduction and agenesis
was first alluded to in Chapter 6 – this is the idea, proposed by
Bermúdez de Castro (483) that prolonged developmental periods in
modern humans may have resulted in a delay in the initiation of the
M3. All other aspects of tooth growth held constant, delayed initiation
of the M3 would result in less time for tooth formation, with smaller
tooth size or simply absence of the M3 as a consequence. While this
explanation might work for the high frequency of third molar agenesis
in humans in general, it is not clear if variation in M3 initiation timing
can explain patterns of variation in third molar agenesis among living
human populations. Moreover, all of the factors discussed here may
interact in complex ways, influencing the high frequency of third
molar agenesis in modern humans and its variable expression among
modern human populations. We are still far from understanding the
relative importance of these factors in producing patterns of human
third molar agenesis.
Dental reduction, including third molar agenesis, is an impor-
tant trend in recent human evolution, the causes for which, at both
proximate and ultimate levels are still being worked out. Changes in
diet and food-processing not only influenced this trend but also had
a dramatic impact on the evolution of bacteria causing dental disease.
226 origins of modern humans and their dental diseases

the relatively recent rise of dental disease

A few cases of dental pathology pepper the hominin fossil record.
Malocclusions – when upper and lower teeth do not come together
correctly – were present in the Nariokotome boy and the Dmanisi
hominins (see Chapter 6). Cavities in fossil hominin teeth have been
found in Paranthropus robustus (484)– but only in about 3% of over
100 teeth. There are a handful of Neanderthal teeth with cavities
(485). Bone loss associated with periodontal disease occurs in a few
Australopithecus africanus individuals, but is somewhat more com-
mon in the Dmanisi hominins and in Neanderthals (485, 486).
The loss of teeth before death, antemortem tooth loss (AMTL),
has been reported in just eleven hominins (487). AMTL can occur
through different pathways. One way AMTL can occur was described
earlier, through periodontal infections that destroy the periodontal
tissues tethering teeth to their sockets. Another way AMTL can
occur is through exposure and subsequent bacterial infection of the
dental pulp (pulpitis). Pulp exposure can occur when cavities are very
deep or when teeth are heavily worn. Whatever the pathways leading
to it, AMTL in earlier hominins was rare.
A 2014 FDI World Dental Federation report [http://www
.worldoralhealthday.com/wp-content/uploads/2014/03/FDIWhitePa
per_OralHealthWorldwide.pdf] estimates that worldwide, between
60–90% of children are afflicted with dental caries – the disease pro-
cess resulting in cavities. Up to 5 to 20% of the world’s populations are
afflicted by periodontitis, which the FDA states is the leading cause of
tooth loss. How did we go through so much of our evolutionary history
with so little dental pain, only to experience so much of it today?
In 1984, anthropologists Mark Cohen and George Armelagos
published a collection of studies from around the world documenting
increases in pathology – including dental pathology – during the tran-
sition from a hunting and gathering to an agricultural way of life (488).
As that transition took place, and people began to eat large quantities
of carbohydrate-rich cereals, caries rates increased. Caries is a disease
 the relatively recent rise of dental disease 227

caused by a group of oral bacteria called mutans streptococci. These

bacteria live in the plaque that bathes our teeth, and live off of the
fermentable carbohydrates (starches and sugars) that we ingest. In the
process of fermenting sugars, caries-causing bacteria produce lactic
acid, which demineralizes teeth causing cavities in them (74).
In North America, caries rates increased in multiple regions as people
became reliant on maize agriculture (488). Increases in caries during
the transition to agriculture have also been noted in South Asia (489),
South America (490) and Nubia (491), among other places.
Thanks to the work of Christina Adler and colleagues (492), we
now know there was a shift in the composition of oral bacteria during
the transition to agriculture. These researchers sequenced bacterial
DNA from the dental plaque of hunter-gatherer- and early agricultural
European dental remains. Hunter-gatherers had few disease-causing
bacteria but the agricultural Europeans, who ingested large quantities
of wheat and barley, were hosts to disease-causing bacteria that lived
off of bits of these cereals in their mouths. Otzi the Neolithic iceman,
who died in the Italian alps around 3300 BC, suffered from rampant
caries and periodontitis (493).
I am slightly overstating the case though, making it seem as if
there were near identity between agriculture and dental disease. Even
the diets of foragers, if they contain high quantities of fermentable
carbohydrates, can be associated with high caries rates. Louise
Humphrey and colleagues (494) recently published evidence of high
caries rates – 51% of teeth affected – in the adult teeth of 15,000-year
old foraging North Africans who included a high proportion of wild
acorns and pine nuts in their diets. Meanwhile, archaeologists Marc
Oxenham and Nancy Tayles (495) found little evidence for an increase
in oral disease (including caries) with intensifying rice agriculture in
Southeast Asia. By themselves starch rich foods are actually much less
cariogenic than sugary foods, or foods that combine both starch and
sugar (74).
Where agriculture and high caries rates are linked, females seem
to bear the brunt of the burden (496). Dental anthropologist John
228 origins of modern humans and their dental diseases

Lukacs (who happens to have been my dissertation adviser) performed

a meta-analysis of caries in both prehistoric and modern societies.
Females were found to often have higher rates of caries than males
do (496). Bioarchaeologist Clark Spencer Larsen (who happens to be
my Department Chair) reported high rates of caries associated with
Native American maize agriculture in Georgia, with females being
more often afflicted than males (497). He suggested that higher rates of
caries in females had to do with sex differences in food preparation and
consumption, with females consuming larger quantities of
carbohydrates.
John Lukacs (496), together with Leah Largaespada (498) coun-
tered that the higher rates of caries in females might have more to do
with their biology than with culturally constructed gender roles. For
example, experimental studies in rats associate high concentrations of
estrogens (but not testosterone) with increased caries formation (499).
Estrogens reach their highest concentrations in women when they are
pregnant (496). Moreover, there is evidence that saliva biochemistry
changes during pregnancy, so that it is less able to buffer increases in
acidity (500, 501) On the basis of these findings (and others), Lukacs
suggested that increases in fertility associated with agriculture
“accentuated” the difference in caries rates between males and
females. Lukacs maintains that in agricultural societies, where multi-
ple pregnancies occur over the life course, caries rates increase with
age at a faster rate in females than they do in males. Females are also
more susceptible to periodontal disease and tooth loss than males
(502). There seems to be truth in the adage “A child, a tooth” common
to many cultures (502).
While dental disease began to rise during the transition to agri-
culture, it soared with the introduction of refined sugar into our diets
during the Industrial Revolution. The Adler et al. study of bacterial
DNA in dental calculus found that caries-causing bacteria became the
dominant species of oral bacteria only after the medieval era (492).
They suggest that the industrial production of refined sugar and flour
changed oral environments, providing caries-causing bacteria with
 the relatively recent rise of dental disease 229

ample simple sugars to ferment. In the process, these bacteria pro-

duced lactic acid that demineralized enamel and caused cavities.
Simple sugars are the primary molecules on which cariogenic bacteria
act. In England, the greatest increase in caries rates occurred from
1800 to 1850, when sugar began to be imported from the West Indies
in large quantities (503).
Today, when Western diets replace traditional ones, caries
rates rise dramatically. Researchers Andrea Cucina and Elma
Vega Lizama studied young adults living in an area of the
Yucatan peninsula. Those who lived in the town area, where
sodas and other sugary foods were available had three times the
number of cavities as those living in a nearby village, who did not
have access to these items (503). Western diets not only bring about
higher caries rates but also higher rates of malocclusion. Soft diets
do not stimulate jaw growth, and teeth, especially third molars,
become impacted. Precontact Australian aborigines, for example,
had fewer malocclusions than postcontact groups (504). Third
molar impaction became ten times more common after the
Industrial Revolution than it was previously (503).
It might seem strange that natural selection, acting over millen-
nia, has not selected for individuals who are more resistant to dental
disease. The reason this has not happened has to do with evolutionary
mismatch – our current diets, with soft, processed, and sugary foods
are nothing like the hunting and gathering diets to which we are
adapted. It is estimated that 99% of our evolutionary history was
spent eating wild foods that were gathered or hunted. Agriculture
and the Industrial Revolution are recent phenomena in our long evo-
lutionary history. Essentially, natural selection has not prepared us
well for the kinds of foods we eat today.
A less often appreciated contributor to our current dental
malaise is our long lifespans. Caries is an “age-progressive” disease –
the longer you live the more caries you can accumulate. Cassandra
Gilmore recently compared human hunter-gathers and apes in their
frequencies of antemortem tooth loss (487). She found that AMTL is
230 origins of modern humans and their dental diseases

higher in human hunter-gatherers than it is in chimpanzees, but that

this difference is not related to differences in rates of wear or caries
between them.
What explained the difference in human hunter-gatherer versus
chimpanzee rates of AMTL was simply age. The odds of losing a tooth
tripled for every ten years of age. Living longer than chimpanzees,
hunter-gatherers simply have greater opportunity to lose teeth. Still,
Gilmore found that even when age was accounted for statistically,
hunter-gatherers had somewhat elevated frequencies of AMTL as
compared to chimpanzees. She therefore suggests that some aspect
of human behavior – the ability to use tools to soften foods or the help
of others – must contribute to the human ability to survive with few
teeth. (Divine intervention is probably out as an explanation, because,
according to cartoonist Matt Groening, “God often gives nuts to
toothless people.”)

our teeth, ourselves

In sum, the study of ancient teeth provides multiple insights into
modern human biology. Analysis of dental morphology is consis-
tent with a two-wave dispersal of anatomically modern humans
from Africa. The retention of ancestral dental traits in sub-
Saharan Africans and in Australians can be explained by the two-
wave dispersal model. Similarly, the continuity of dental features in
East Asia from Homo erectus to early anatomically modern humans
in this region around 100,000 years ago, suggests admixture
between more archaic hominins in Asia with the first dispersers
out of Africa. Early anatomically modern humans, such as Jebel
Ihroud 3 from Morocco and the Qafzeh 10 from Israel, appear to
have modern human schedules of dental development, but are not
quite modern in some of the details of their root (Jebel Ihroud 3) and
enamel (Qafzeh hominins) growth. Their modern developmental
schedules suggest that their overall pace of growth during childhood
was similar to that of living people today, but we lack information
about their rates skeletal development to complete the picture.
 our teeth, ourselves 231

Modern humans have much smaller teeth than their anatomi-

cally human ancestors, such as Jebel Ihroud and Qafzeh. Calculating
rates of dental reduction through time, Loring Brace and colleagues
highlighted the roles of cooking, tool use, and eventually pottery in
relaxing selection pressures on maintaining large teeth. Brace
explained the decrease in tooth size as a result of the Probable
Mutation Effect. Calcagno and Gibson’s (355) tooth-jaw size mis-
match hypothesis may be a more promising explanation for dental
reduction at this stage in human evolution. Both explanations attri-
bute changes in tooth size to changes in culture, although as noted,
not all cases of dental reduction can be clearly linked to culture
change. It is hard to imagine that cooking, tools, and pottery did not
have a tremendous influence on the overall modern human trend
toward dental reduction – yet, more careful studies such as
Y‘Edynak’s study of the Iron Gates site are needed to test hypothesized
correlations and the mechanisms that underlie them.
Finally, from the study of ancient teeth, it is clear that only in
our very recent history has dental disease become so widespread.
Caries and malocclusions were very rare in earlier hominins.
Bacterial DNA recovered from dental calculus testifies to shifts in
the composition of oral bacteria coincident with the transition to
agriculture and the Industrial Revolution. Our long lifespans also
contribute to our dental plight. Perhaps there are lessons to be learned
here for how dental practitioners treat teeth today. A 2013 meeting of
dental anthropologists and dental practitioners at the National
Evolutionary Synthesis Center pondered this question. Conclusions
from that meeting as well as other ways that an evolutionary perspec-
tive can inform the dental present are considered in the final chapter.
 10 Every Tooth a Diamond

“. . . for I tell thee Sancho, a mouth without teeth is like a mill without
a millstone, and a tooth is much more to be prized than a diamond.

– Cervantes
Don Quixote

So lamented Don Quixote when shepherds bearing slingshots took

out several of his “grinders.” He had attacked their flock of sheep,
which he mistook for an army (easy mistake). However misguided, the
noble knight-errant clearly understood the value of teeth.
To paleoanthropologists, the value of teeth lies in the wealth of
information they preserve about our past. Morphological analyses of
fossil teeth elucidate biological relationships among species and popu-
lations within them. Studies of the chemical composition of enamel
and of dental wear inform us about the diets of our ancestors and close
relatives. And, investigations of dental growth and development
enlighten us about their life history modes. These are some of the
more vital contributions of teeth to understanding our evolutionary
history. Here, I will synthesize dental insights into human evolution
discussed throughout this book and consider what’s next for what can
be called “dental paleoanthropology,” the subfield of paleoanthropol-
ogy that makes use of fossil teeth to understand hominin biology.
Finally, I will reflect on how an evolutionary perspective on our dental
past helps us understand how we view and treat teeth today.

putting in all together: the whole tooth

If we were to draw up a list of differences between humans and our
chimpanzees relatives, that list would include – among other things –
our differences in brain size, language ability, ability to adapt to new

232
 putting in all together: the whole tooth 233

environments, our reliance on cultural solutions to problems of sur-

vival and reproduction, the length of our periods of juvenile growth
and dependency, and the length of our lifespans. Fossil teeth give us
a record of the origins and evolution of several of these and other
unique human attributes.
The origins of human adaptability can be traced back to the
teeth of our australopith ancestors. Stable carbon isotope analysis of
their dental enamel (Chapter 2) reveals that, unlike modern chimpan-
zees whose diets even in savanna environments are limited to C3
plants, australopith species were in most cases incorporating both
C3 and C4 resources into their diets (83). As dietary “generalists”
australopiths would have had the ability to survive a wide range of
environmental conditions, as resources waxed and waned.
Australopiths had to contend with rapid oscillations from wet to dry
environments over time. They had to be able to adjust to the patch-
work of local habitats that characterized the African Plio-Pleistocene.
According to Rick Potts’ “Variability Selection Hypothesis,” these
unstable and diverse environments selected for our ancestors’ dietary
and behavioral flexibility (505).
Data gleaned from marine cores and ancient soils tells us about
the varied environments in which australopiths evolved. Chemical
signatures in their teeth reveal that they survived within these envir-
onments by diversifying their diets. This is not to say, of course, that
australopiths were perfectly adapted to these conditions. There is
a fair amount of linear enamel hypoplasia in australopith teeth, sig-
nifying physiological stresses that were severe enough to disrupt
enamel formation (506, 507). We descended from those able to survive
these stresses and pass along the genes that made them successful.
In Darwinian terms, we therefore owe some part of our hallmark
human adaptability to the “struggle for existence” of our australopith
ancestors.
Evidence from teeth further suggests how two very different
hominin lineages – Paranthropus and Homo were able to coexist.
Chemical and microwear analyses bolster John Robinson’s “Dietary
234 every tooth a diamond

Hypothesis,” which postulates that the two lineages occupied differ-

ent niches. In East Africa, Paranthropus boisei consumed much
greater quantities of C4 plants that did its Homo erectus contempor-
ary (88). The featureless microwear on Paranthropus boisei teeth is
consistent with a diet of tough C4 plant parts that required repetitive
chewing to break down into digestible pieces (338). Meanwhile, in
South Africa, trace element analysis of Sr/Ca and Ba/Ca ratios in tooth
enamel point to the incorporation of significant quantities of meat in
the diet of Homo habilis, with Paranthropus robustus remaining
primarily vegetarian (106).
We can also trace the origins of our small canine teeth back to
australopith times. Our diminutive canines are unique among our
living great ape cousins, and multiple hypotheses have been proffered
to explain them (Chapter 3). Here, I argued that the small degree of
canine sexual dimorphism at in Ardipithecus ramidus at 4.4 Ma (19) is
hard to explain on the basis of current dietary hypotheses for canine
reduction. That is because Ar. ramidus was primarily a C3 resource
feeder, like chimpanzees, and lacked the craniodental adaptations to
eating the mechanically challenging foods consumed by later austra-
lopiths. For Ar. ramidus, it is most plausible that minimal canine
sexual dimorphism signifies either decreased male-male competition
for mates or that competition among males had ceased to involve
canine teeth. Peter Lucas’ (123) and William Hylanders’ (124) biome-
chanical analyses indicate that dietary-associated reduction in jaw
gape in later hominins would have constrained the evolution of large
canines.
If the origins of our dietary flexibility and our small canine teeth
can be found in our australopith ancestors, do our prolonged periods of
juvenile growth, so intimately tied to our large brains and flexible
behavior, also originate with them (Chapter 4)? The answer to this
question has changed over time, as our understanding of the range of
variation in human and ape dental development has broadened and as
x-ray synchrotron microtomography has provided a clearer picture of
hominin dental development than ever before. It now seems that in
 putting in all together: the whole tooth 235

some australopiths, periods of dental development were longer than

those of chimpanzees. This is even true of some individuals of
Paranthropus robustus (196), a species generally considered to repre-
sent a side branch of our evolutionary tree. Perhaps the first steps
toward lengthening growth periods were taken in the common ances-
tors of Paranthropus and Homo, as brain sizes and dietary breadth
began to expand. Perhaps these lineages were also evolving larger
brains and longer developmental periods in parallel.
In their recent synthesis of research on early Homo, Susan
Antón and colleagues (177), argued (as had Peter Ungar and co-
authors earlier [339]), that variability selection drove the further evo-
lution of dietary and behavioral flexibility in the genus Homo. A broad
range of complexity values characterizes Homo erectus dental micro-
wear, indicating a diet that spanned soft as well as hard foods (338).
The decreasing size of premolar and molar teeth reflects increasing
reliance on cultural solutions for survival. We know from the archae-
ological record that stone tools became more sophisticated during
Homo erectus times, and that there is a good possibility that Homo
erectus controlled and used fire. Foods softened with stone tools and/
or with fire would have significantly relaxed selection for growing and
maintaining large posterior teeth and jaws at this time in our evolu-
tionary history. It is possible that the steep reduction in the size of
posterior teeth and jaws in Homo erectus was a result of selection for
energy efficiency in this large-brained, large-bodied hominin
(Chapter 6).
Periods of dental development lengthen in Homo erectus
(Chapter 7), possibly signifying a further step along the way to prolong-
ing juvenile dependency and time available for learning. Greater
opportunity for learning would be consistent with the large brains
and flexible behavior of Homo erectus. Unexpectedly though, skeletal
growth rates, as assessed by using teeth to age the Narikotome boy,
may have been quite rapid. If that is so, then perhaps our protracted
periods of dental and skeletal development evolved in a mosaic
fashion, with dental development slowing down first. Why this
236 every tooth a diamond

dissociation between dental and skeletal development would have

occurred is unclear, but such dissociations characterize the life history
modes of some living primates (186). Filling in the life history picture
for Homo erectus is Caspari and Lee’s wear seriation analysis indicat-
ing that Homo erectus also enjoyed longer lifespans than any hominin
species that came before it. That evidence is consistent with the view
that cultural adaptations in Homo erectus reduced the risk of extrinsic
mortality in adults (177). Under this condition, biological investment
in prolonged juvenile growth periods and extended natural lifespans
would have been possible.
The human trends that teeth reveal continue to be traceable
through later stages of human evolution (Chapters 8 and 9). Although
for many years Neanderthals had been viewed as meat specialists,
new work on Neanderthal dental calculus, microwear, and macrowear
clearly shows that Neanderthals were including plant foods in their
diets (411, 412, 414, 415), perhaps in some cases for medicinal pur-
poses (412). They also tended to eat foods similar to that of their
anatomically modern counterparts where they occupied similar habi-
tats (414). These dental data are consistent with recent archaeological
evidence, all of which suggests that Neanderthals were flexible
foragers.
Evidence from the study of linear enamel hypoplasia and fluc-
tuating dental asymmetry indicates that Neanderthals experienced
relatively high levels of physiological stress, but not necessarily
greater than that of recent anatomically modern human foragers
(Tigara) who occupied marginal habitats (437, 442). Elevated levels of
physiological stress are consistent with the notion that maintaining
large and muscular bodies in cold environments was energetically
costly (435), and may have led to slow rates of skeletal growth (453)
in Neanderthals, either as an evolutionary adaptation or as a plastic
(flexible physiological) response.
In contrast to rates of skeletal growth, rates of dental devel-
opment and age at first molar eruption in Neanderthals are at the
“rapid end” of modern human variation, but are both generally
 putting in all together: the whole tooth 237

encompassed within the modern human range. Laura Shackelford and

colleagues showed this for Neanderthal dental development (451),
while M1 eruption estimates from two studies placed Neanderthals
among modern humans (446, 449). Third molar development and
eruption may have been accelerated in Neanderthals (449), but what
this may mean, if anything, for other aspects of Neanderthal life
history is obscure (508). All of these findings add up to that conclu-
sion that Neanderthals were more like us than the earliest paleoan-
thropologists imagined. Analysis of oblique striations on Neanderthal
anterior teeth suggests that like us, most Neanderthals were also
right-handed.
Study of dental morphology puts the initial divergence between
Neanderthals and anatomically modern humans around 1 million
years ago, earlier than the 800,000-year estimate from genetic studies
(Chapter 9). Evidence from dental morphology is consistent with that
from DNA indicating a two-wave migration of AMHS out of Africa: an
earlier migration into Asia around at around 130,000 (as estimated
from genetic studies) and a later one into northern Eurasia around
50,000 years ago (again estimated from genetic studies). As I write
this chapter in late 2015, new evidence has come to light from a cave
in Daoxian (Hunan Province) China, where forty-seven teeth with
modern human morphology dated to at least 80,000 years ago were
recovered (509).The presence of such old modern-looking human
teeth in Daoxian (and from other sites in China, as reviewed in
Chapter 9) is consistent with genetic evidence of an early migration
of AMHS from Africa into Asia.
Finally, with early anatomically modern humans, such as Jebel
Ihroud (approximately 160,000 years old) and Qafzeh (about 90,000
years old), overall rates of dental development are not distinguishable
from those of living people (449, 470). Interestingly, however, not all
aspects of their dental growth and development are modern, with Jebel
Ihroud evincing fast rates of root growth (470) and some of the Qafzeh
teeth showing a more archaic perikymata distribution pattern (474).
These early anatomically modern humans still had rather large teeth.
238 every tooth a diamond

It is only with the origins of agriculture that the rate of dental reduc-
tion accelerated, and with it rates of dental pathology. Of all our
human characteristics that can be traced back in time through fossil
teeth, our myriad dental problems are the most recent.

a taste of what’s next for dental

paleoanthropology
The future of dental paleoanthropology holds new questions, further
research into the genetics and development of dental morphology,
diverse applications of new technologies, and expansion of the com-
parative primate and human database for dental morphology, diet, and
development.
New fossils raise new questions. Homo naledi, a South African
hominin species announced by paleoanthropologist Lee Berger and
colleagues in late 2015 raises many (510). This species, of currently
unknown antiquity, combines a tiny brain (similar to that of austra-
lopiths) with the cranial morphology of Homo erectus and an esti-
mated stature that falls among smaller modern human values.
The molars of Homo naledi are smaller in size than those of Homo
habilis and fall at the smaller end of Homo erectus values. Why this
species had such small molars, smaller than most other hominins of
comparable brain size (Figure 10.1), is one question this species raises.
The molars have a simplified occlusal morphology, and this makes
sense for molars of such small size molars under the Patterning
Cascade Model for tooth formation (see Chapter 6 for discussion).
All kinds of questions will undoubtedly be asked of the Homo naledi
teeth – especially because there are 140 or so of them – aiming to
understand the morphological affinities of this new species, its dietary
proclivities and its rates of dental growth and development.
The use of dental morphology to assess biological relationships
requires a refined understanding of the genetics and developmental
processes that underlie them. Morphological dental features are rou-
tinely treated as independent in phylogenetic analyses, even though
some of these features may share common genetic and developmental
 a taste of what’s next for dental paleoanthropology 239

1400

1200
Middle Pleistocene
Homo (Africa)
Endocranical volume (ml)

Middle Pleistocene
1000 Homo (Europe)
H. erectus

800
H. rudolfensis

H. habilis
600
Homo naledi Au. africanus
Au. garhi
Au. afarensis
400 H. floresiensis Au. sediba

9.0 10.0 11.0 12.0 13.0 14.0 15.0 16.0

Maxillary first molar buccolingual diameter (mn)

figure 10.1: Breadth of upper first molar (buccal-lingual dimension)

related to endocranial volume for a variety of hominins, including
the recently discovered Homo naledi. The image is from Berger
et al., 2015 in eLife, reprinted here under the terms of the Creative
Commons Attribution License, https://creativecommons.org/licen
ses/by/4.0/

underpinnings (360, 361, 511). For example, my colleagues Stephanie

Moormann and John Hunter and I (362) found that there were statis-
tically significant low-level correlations between the presence of the
Carabelli cusp and other accessory cusps on upper molar teeth, sug-
gesting that these cusps do not develop independently, just as the
Patterning Cascade Model of tooth development predicts. It may even-
tually be possible to reconstruct the developmental events that lead to
patterns of dental trait covariation (361) and to use these events, rather
than the traits themselves, in phylogenetic analyses. If that proves too
difficult, then as paleoanthropologist Leslea Hlusko pointed out more
than a decade ago, efforts can be made to identify suites of correlated
240 every tooth a diamond

traits, and use these rather than “atomized characters,” in phyloge-

netic analyses (511).
With respect to new technologies, there are exciting avenues to
further explore. One of the most fascinating of these is laser-ablation
inductively-coupled-plasma mass spectrometry analysis of Strontium-
Calcium (Sr/Ca) and Barium-Calcium (Ba/Ca) ratios in tooth enamel,
which offers a way to reconstruct weaning timelines in fossil teeth (512,
513). Louise Humphrey and colleagues demonstrated that the Sr/Ca
ratios along enamel prisms in children’s deciduous teeth reflected
known dietary shifts from mother’s milk to infant formula or comple-
mentary foods (512). There is greater discrimination in the transfer of Sr
relative to Ca across the mammary gland, such that during the period of
exclusive breastfeeding, the Sr/Ca ratio in infant tissues, including
enamel, is low. When complementary foods are introduced into the
infant’s diet or when the infant transitions to formula, the Sr/Ca ratio of
the infant’s tissues increases. Humphrey et al. used incremental growth
markings in enamel, starting from the neonatal line that marks birth, to
pinpoint when the weaning process began. She and her colleagues then
compared weaning timelines reconstructed from these children’s
deciduous tooth enamel with their actual feeding histories. In three of
the four children, Sr/Ca ratio increases coincided with the ages at which
formula or complementary foods were introduced.
A similar analysis is possible with Ba/Ca ratios, only in this case
values of Ba/Ca are higher during the period of exclusive breastfeeding
and decrease as weaning foods are added to an infant’s diet. Christine
Austin and colleagues (513) showed that the rate of decrease in the Ba/
Ca ratio during weaning closely paralleled the rate at which breast
milk was withdrawn from the infant’s diet. This was true for both
human children and captive macaques. Furthermore, these research-
ers reconstructed dietary transitions in a Neanderthal juvenile. Ba/Ca
ratios in this juvenile’s enamel revealed a seven-month period of
exclusive breastfeeding. This was followed by a seven-month period
of supplementation, after which the Ba/Ca ratio rapidly fell to prenatal
levels. The authors interpreted the rapid fall as an “abrupt”
 a taste of what’s next for dental paleoanthropology 241

termination of breastfeeding at around 1.2 years of age in this

Neanderthal individual. It is not clear to what extent (if at all) this
juvenile reflects the weaning habits of Neanderthals, but the possibi-
lity of similar analyses in other fossil teeth may eventually make it
possible to understand at what ages and in what manner Neanderthals
and other fossil hominins weaned their children.
Inferences made from fossil teeth rest on understanding how the
teeth of nonhuman primates and living humans relate to their diets
and life histories. This is the essence of the comparative method.
Many advances in understanding these relationships have been
made by studying extant species and populations, and many more
are sure to follow. Examples from nonhuman primates include the
findings, based on multiple years of feeding data, that very thick
enamel can be an adaptation to eating hard foods either as fallbacks
or as dietary staples (62, 66). They include the finding that in the wild,
ring-tailed lemurs with significant tooth loss can survive to advanced
ages without the active care of others (387), challenging the notion
that one can infer caregiving directly from the presence of individuals
with severe antemortem tooth loss in the fossil record.
The effort to understand relationships between teeth and the
environment is clearly crucial to our ability to understand the signals
of adaptation, diet, behavior, growth, development, and life history
that are present in fossil teeth. To coalesce research on this topic,
anthropologists Frank Cuozzo, Peter Ungar, and Michelle Sauther
organized a symposium entitled “Primate Dental Ecology: How
Teeth Respond to the Environment.” In their introduction to the
symposium papers published in the American Journal of Physical
Anthropology in 2012, Cuozzo and co-organizers expressed the hope
that this newly defined research field will gain momentum in coming
years (514).
With respect to the comparative database from living humans,
there is much more that can be learned about ranges of variation in
modern humans as well as how modern human teeth respond to their
environments. Christopher Dean and Helen Liversidge’s comparative
242 every tooth a diamond

sample of over 6,000 children of diverse ancestry made it possible to

situate the ages at which dental stages were reached in early Homo
among modern children with advanced dental development (369).
Histological data on modern human variation has been greatly
advanced by the work of Donald Reid (515) and is necessary for direct
comparison to histological data from fossil teeth. Much histological
study of developmental variation remains to be done, with respect to
the ages of initiation of teeth, rates of hard tissue formation, and ages
at crown and root completion in diverse populations. Moreover,
greater understanding of relationships between population variation
in human dental development and the environmental influences that
may have shaped that variation is much needed for interpreting what,
for example, different rates of dental development might mean when
we see them in fossil anatomically modern humans or in
Neanderthals (508).

teeth today
We need to understand teeth today in order to better interpret teeth in
the past. But, it is also true that our understanding of ancient teeth can
inform us about our dental present.
A key lesson emerging from the recent National Evolutionary
Synthesis Center (NESCent) meeting on “Evolutionary Dentistry”
was that dental caries, periodontal diseases and orthodontic condi-
tions are maladies of modernity (Chapter 9). Kevin Boyd, a pediatric
dentist participating in the meeting, suggests in an interview with
“Dentistry iQ” (www.dentistryiq.com) that this evolutionary per-
spective is instructive – it tells us that these dental problems are
entirely preventable. It was suggested at the NESCent meeting that
chewing tougher foods during childhood like our ancestors did might
help to stimulate jaw growth and prevent malocclusions (think beef
jerky) (503). One of the co-organizers of the meeting, John Sorrentino,
came away from the meeting with several evolutionary-inspired
recommendations https://www.jackkruse.com/evolutionary-biology
-meets-dentistry), which include eliminating processed sugar from
 teeth today 243

our diets and reducing our consumption of natural sugars. He also

points out that brushing and flossing your teeth “is not going to
hurt you.”
An evolutionary perspective may also be instructive from the
standpoint of dental esthetics. Evolutionary psychologists view
our facial preferences in terms of sexual selection. The idea is
that over the millenia we have evolved mental preferences for
facial cues of an individuals’ “mate value” (516). As the authors
of one review article put it, “. . . preferences guide us to choose
mates who will provide the best chance of our genes surviving”
(516). On the most basic level, lesions or sores on a person’s face
are not generally considered attractive. Symmetrical faces with
average features tend to be perceived as more attractive, phenom-
ena evolutionary psychologists ascribe to genetic quality and dis-
ease resistance.
In the framework of evolutionary psychology, a recent study
found that human teeth also “signal” mate quality. In their study,
Hendrie and Brewer manipulated the color and spacing of teeth in both
young male and female digital images (517). These authors hypothe-
sized that because smiling is an overture of sexual interest in humans,
teeth would be particularly visible as cues. Tooth loss could signal
a dental problem, such as caries or periodontitis, and dental crowing,
of course is also related to dental disease (Chapter 9). Psychological
preferences for having a full set of straight teeth would have evolved
because these were reliable cues of a mate’s ability to help us get our
genes into the next generation.
The authors also hypothesize that white teeth are also a cue to
mate quality. As we age, additional deposition in our teeth of under-
lying (yellow) dentine and the thinning of the whitish outer enamel
layer contribute to progressive darkening and yellowing of teeth.
Yellower teeth, in the authors’ view are therefore age indicators.
The more limited reproductive lifespans of women relative to men
suggest that age indicators would have been particularly salient cues
of female “mate value.” The authors found what they expected to find:
244 every tooth a diamond

nonnormal spacing of teeth and teeth that were more yellow in color
were rated as less attractive, and for yellowing, this was particularly
true for the female models.
The Hendrie and Brewers results are not so surprising given that
their sample population was from the UK and given that Western
cultures are increasingly influenced by Hollywood ideals of straight
and white teeth. The question is whether such preferences for straight,
white teeth are “cultural universals” that would reflect an underlying
evolved psychology for our species. And the answer to this question is
unclear. Charles Darwin remarked that standards of beauty vary so
greatly among different cultures that such universal standards must
not exist (115).
On the face of it, tooth modification practices, some of which
are done for aesthetic reasons, are so variable across cultures as to
make one question the universal appeal of a full set of white teeth.
In Southeast Asian cultures tooth “blackening” with plant products to
enhance attractiveness can be traced back 4,500 years (518), but the
custom is beginning to wane as people are exposed to the Western
ideal of white teeth. The reasons offered by those who blacken their
teeth include reducing the prominence of canine teeth, which is also
accomplished by filing the canine teeth. Perhaps we have an evolved
preference for small canine teeth that in this society supersedes
a preference for white teeth?
That’s possible but then how does one explain why Mentawi
people of Sumatra, some groups in Kalimantan, and the Kamorans of
Papua New Guinea file their incisors to make them pointy (519)? And,
then there are also many cultures – in Indonesia and especially in sub-
Saharan African peoples – in which the anterior teeth are extracted
and this is considered to be beautiful (520). Thus, while there might be
something to an evolutionary psychology approach to understanding
how we view teeth today, it will be challenging to come up with
testable hypotheses for such diverse cultural practices associated
with dental “beauty” under an evolutionary psychology paradigm.
 teeth today 245

Future dental paleoanthropologists will likely have field day

with modern human teeth, especially with the various ways that
cultures modify them, which include notching teeth, inlaying them
with jewels or gold, lengthening them, filing them down, and remov-
ing them altogether. One thing these future paleoanthropologists may
safely conclude is that these modifications reflect the human ability
to think flexibly, creatively, and not always adaptively.
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 Index

abrasive diets, 37, 39 Au. africanus, 22, 23, 50, 144, 146
Adler, Christina, 227 Australopithecus anamensis, 18, 47, 52, 56,
age at first reproduction, 84, 92 57, 76, 247, 252, 257
agriculture, 220, 222, 227, 228, 231, 238, Au. anamensis, 20, 21, 47, 49, 80, 146
279, 280 Australopithecus bahrelghazali, 21, 47
Aiello, Leslie, 132 Australopithecus deyiremeda, 21, 28
Ala240Pro mutation, 223 Australopithecus garhi, 22, 139, 248
allomother, 172, 174, 207 Au. garhi, 23
Ameloblasts, 93 Australopithecus sediba, 23, 28, 39, 49, 51,
AMHS, 126, 134, 137, 171, 176, 211, 237 57, 248, 249
anatomically modern, 8, 55, 114, 123, 127, Au. sediba, 23
130, 134, 135, 137, 156, 159, 171, 176, aye-aye, 33, 56
178, 181, 185, 186, 200, 203, 208, 209,
211, 212, 213, 214, 215, 216, 217, 218, baboons, 12, 13, 52, 54, 55, 68, 69, 79, 253, 262
219, 220, 230, 236, 237, 242, 275 bacteria, 39, 149, 188, 223, 225, 227, 228, 231
anisotropy, 40, 41, 49, 54, 191 Barium-Calcium, 240
antemortem tooth loss, 226, 229, 241, 279 bark, 33, 36, 51, 58, 71
AMTL, 226, 229, 230 Barrett, Chris, 198
anthropoids, 18, 65, 67, 71, 74, 79, 162, Bar-Yosef, Omar, 190
254, 256 Begun, David, 75
Antón, Susan, 113, 235 Benderlioglu, Zeynep, 196
Ardipithecus kadabba, 16 Berger, Lee, 238
Ardipithecus ramidus, 16, 18, 19, 46, 47, 52, Bermúdez de Castro, José, 170, 212
57, 61, 62, 63, 64, 76, 78, 79, 80, 81, Berrigan, David, 85, 200
82, 234, 247, 252, 254 biological species concept, 116, 262
Ar. ramidus, 18, 47, 234 bipedalism, 15, 16, 61, 63, 77
Ardi, 16, 18, 20, 61 bite force, 43, 72, 129, 142, 145, 146,
Argue, Debbie, 132 151, 156
Armelagos, George, 226 Black, Davidson, 118
Arsuaga, Juan Luis, 125 Blomquist, Greg, 169, 201
Austin, Christine, 240 Bocherens, Hervi, 185, 187
Australians, 135, 213, 214, 215, 230 Bogin, Barry, 157
Australopithecus afarensis, 18, 20, 21, 22, 47, Bond, Sandra, 197
49, 56, 57, 66, 76, 79, 80, 81, 82, 100, bonobos, 14, 32, 66
101, 102, 106, 132, 247, 248, 252, Boule, Marcelin, 177
257, 268 bovids, 38, 48, 56, 185
Au. afarensis, 20, 21, 22, 146 Bower, Bruce, 87
Lucy, 20 Boyd, Kevin, 242
Australopithecus africanus, 18, 22, 23, 28, 30, Brace, Loring, 138, 146, 192, 220, 231
32, 43, 46, 49, 50, 51, 52, 57, 58, 102, Bromage, Timothy, 95, 97
106, 226 Broom, Robert, 24, 259

282
 index 283

brown capuchins, 40 Cuozzo, Frank, 174, 241

browsers, 49, 51 Cuvier, Georges, 4
buccal, 5, 7, 124, 132, 192, 239, 274
Burkart, Judith, 172 Daegling, David, 32, 43
Daoxian, 237
C3 pathway, 44 Dart, Raymond, 14, 18, 22, 31, 63, 87
C4 foods, 45, 46, 52, 53, 56, 79, 82 Darwin, Charles, 14, 59, 60, 61, 63, 67, 77, 82,
C4 pathway, 45 126, 138, 146, 211, 244, 254, 255, 269
calculus. See dental calculus Dawkins, Richard, 11
Callitrichines, 225 De Lumley, Marie-Antoinette, 191
canine reduction, 63, 77, 78, 79, 80, 234, Dean, Christopher, 102, 160, 164, 165, 166,
256, 257 197, 203, 241
Cantius, 74 deciduous teeth, 87, 88, 89, 102, 106, 240
Carabelli, 153, 239, 270 decussating enamel, 47
Carbon-13, 185 Delezene, Lucas, 80
caries, 226, 227, 228, 229, 242, 243, 279, 280, Denisovan, 131, 136
Cartmill, Matt, 218 dental calculus, 3, 35, 39, 44, 51, 58, 187, 188,
Caspari, Rachel, 160, 207 189, 209, 228, 231, 236, 274
Catopithecus, 74 dental development, 87, 88, 89, 91, 98, 100,
cavernous sinus thrombosis, 223 101, 102, 103, 104, 105, 106, 108, 160,
cavities, 119, 226, 227, 229 162, 163, 164, 165, 169, 170, 171, 173,
Charnov, Eric, 85, 200 199, 204, 205, 206, 207, 209, 210, 218,
childhood, 4, 8, 44, 73, 84, 85, 86, 87, 149, 157, 219, 230, 234, 235, 236, 237, 242, 259,
173, 185, 206, 209, 230, 242, 258 261, 270, 271, 276
chimpanzees, 4, 14, 16, 28, 31, 32, 46, 47, 49, dental morphology, 4, 39, 56, 109, 125, 131,
52, 57, 61, 66, 76, 79, 88, 91, 97, 101, 136, 142, 181, 182, 183, 208, 213, 214,
104, 105, 139, 143, 158, 160, 162, 163, 215, 217, 230, 237, 238, 265, 273
167, 170, 171, 172, 175, 188, 205, 230, dental paleoanthropology, 232, 238
232, 233, 234, 235, 246, 251, 259, 274 dental reduction, 138, 146, 147, 150, 151, 152,
Churchill, Steven, 194 156, 211, 212, 220, 221, 222, 223, 224,
cichlid, 36, 250 231, 238, 269, 270, 278
circadian rhythm, 93, 95, 103 dentine, 34, 93, 95, 119, 121, 166, 243
cladistic, 13, 25, 26, 117, 132, 181, 214, derived traits, 13, 24, 125, 214, 217
215, 266 developmental pathways., 65, 158, See also
cladogram, 13, 26, 28, 182 ontogenetic pathways
Clement, Anna, 128 diastema, 16, 22
Coffing, Katie, 144 dietary divergence, 137, 142
Cohen, Mark, 226 Dietary Hypothesis, 30, 43, 58, 137, 234
complexity, 40, 41, 47, 49, 50, 54, 143, 155, distal, 5, 7, 17
186, 189, 235 Dmanisi, 119, 121, 150, 174, 175, 226, 264
Constantino, Paul, 43, 146, 248, 249, 251 DNA, 11, 14, 29, 116, 123, 125, 131, 134, 135,
cooking, 32, 138, 139, 140, 141, 145, 147, 151, 136, 178, 180, 181, 183, 213, 227, 228,
220, 231, 249, 274 231, 237, 258, 267, 272, 277
Cooking Hypothesis, 140 Dobzhanksy, Theodosius, 86
cooperative breeders, 172 Dominy, Nathaniel J., 48
cooperative breeding, 173, 174, 176, 271, 272 dual selection hypothesis, 71, 80
Corruccini, Robert S., 150
cross-striations, 93, 94, 95, East African Rift valley, 24, 36
103, 201 ecological risk aversion hypothesis, 85
Cucina, Andrea, 229 El Sidrón, 194, 275
284 index

El Zaatari, Sireen, 189 Hamilton, WD, 173

enamel matrix, 93, 94, 95, 100 hard foods, 33, 34, 37, 38, 42, 43, 47, 50, 54, 55,
enamel prisms, 47, 93, 164, 240 56, 144, 235, 241
enamel thickness, 36, 37, 145, 164, 195, 247, hard vs. tough foods, 34
250, 269, 276 hard-object feeding, 35, 37, 50
Energetic Budget Effect, 148 Hardy, Karen, 188
Eng, Carolyn, 145 Havers-Halberg, 97
Eriksson, Anders, 178 Hawkes, Kristin, 159, 171, 173
eruption, 73, 87, 88, 89, 90, 91, 92, 98, 100, Hawks, John, 140
102, 104, 105, 106, 108, 160, 162, 163, Henry, Amanda, 51, 187
166, 171, 175, 176, 204, 206, 218, 236, Hillson, Simon, 197
256, 259, 261, 262, 271 histology, 160, 164
Eskimos, 190, 191, 192 Hlusko, Leslea, 239
evolutionary psychology, 243, 244 Homo antecessor, 117, 123, 162, 165, 170,
Expensive Tissue Hypothesis, 31 171, 176, 180, 181, 183, 199
Homo erectus, ix, 24, 26, 63, 113, 115, 117,
fallback foods, 34, 37, 241 118, 119, 120, 121, 124, 128, 133, 137,
female choice, 60, 64, 80 138, 140, 141, 143, 144, 145, 146, 147,
Fernando Ramirez-Rozzi, 203 148, 149, 150, 151, 152, 155, 156, 162,
Fiore, Ivana, 194 165, 166, 167, 169, 170, 171, 173, 174,
Fiorenza, Luca, 189 175, 176, 180, 181, 182, 183, 199, 216,
fire, 3, 118, 137, 138, 141, 151, 152, 156, 230, 234, 235, 238, 261, 263, 264,
235, 263 268, 270
first molar eruption, 91, 92, 93, 101, 104, 105, Homo floresiensis, 109, 126, 132, 133, 266
108, 162 Homo habilis, 53, 113, 114, 115, 116, 117,
fluctuating asymmetry, 195, 196, 198, 275 118, 119, 121, 133, 137, 139, 144, 145,
Frayer, David, 193, 263, 274, 275 146, 148, 149, 150, 151, 155, 162, 163,
Froehl, Andrew, 194 164, 165, 170, 181, 234, 238, 262, 263,
268, 269
gape, 65, 72, 75, 79, 81, 82, 234, 254 Homo heidelbergensis, 123, 124, 125, 133,
gene flow, 135, 179, 181, 182, 213, 222 134, 136, 137, 140, 151, 153, 155, 156,
generalists, 33, 36, 233 179, 180, 183, 212, 264, 275
genetic drift, 152, 156, 180, 181, 212, 222, 272 Homo naledi, 238, 239, 281
Gesher Benot Ya’akov, 141 Homo rudolfensis, 28, 115, 116, 117
gibbons, 64, 69 Homo sapiens, 8, 101, 117, 126, 135, 169, 171,
Gigantopithecus, 75 181, 263, 266, 278
Gilmore, Cassandra, 229 homoplasy, 12, 65, 75, 102
gingival emergence, 105, 106, 166 honing complex, 16, 63, 75, 257
glossopetrae, 1, 246 honing facet, 75
Godfrey, Laurie, 106 howler monkeys, 40
Gómez-Robles, Aida, 182 Hrdy, Sarah, 173
gorillas, 28, 46, 59, 66, 91, 92, 97, Huanglong Cave, 216, 278
106, 246 Hubbard, Amelia, 213
Gran Dolina, 123, 170, 264 Hublin, Jean-Jacques, 131, 217
Grandmother Hypothesis, 159, 207 Humphrey, Louise, 227, 240
grazers, 49, 51 Hunter, John, 153, 239
Green, Richard, 135, 178 Hutchinson, Dale, 197
Greenfield, Leonard, 64, 71, 80 Hylander, William, 64, 72
Grine, Fred, 33, 43, hypocone, 180
50, 54 hypsodont, 37, 38
 index 285

impaction, 149, 150, 223, 229 Lufengpithecus, 74

Industrial Revolution, 228, 229, 231 Lukacs, John, ix, 228
infection, 149, 197, 223, 226 Luna Cave, 216, 278
Inhibitory Cascade Model, 224, 225
Irish, Joel, 28, 213, 215 M1 eruption, 101, 104, 105, 108, 109,
171, 237
Jebel Irhoud, 217, 218, 219 macaques, 69, 240
Macchiarelli, Roberto, 194, 204, 222
Kay, Richard, 68 Macho, Gabrielle, 54, 55, 92
Kenyanthropus platyops, 21, 28, 47, 49, 116 macrowear, 189, 236, 274
Kieser, Jules, 147, 148, 221 Makapansgat, 49, 249
Koobi Fora, 115, 141, 262 Malawi, 115, 262
Krapina Neanderthals, 181, 197, 214, 274 male-male competition, 60, 64, 67, 68, 78, 81,
Kreuger, Kristin, 191 234, 257
Kromdrai, 50 mandrills, 69
Kuhn, Steven, 186 mangabey, 36
Kuzawa, Chris, 85 Manica, Andrea, 178
Mann, Alan, 87, 98
Lacruz, Rodrigo, 95, 101 Manthi, Fredrick, 76
Lahti, David, 147 marmosets, 71, 172
Lambert, Joanna, 36 Martín-González, Jesús, 206
Larsen, Clark Spencer, 197, 228, 277 Martinón-Torres, Maria, 181
lateral enamel, 98, 100, 256 maturation stage, 93
Le Gros Clark, Sir Wilfrid, 117 Mayr, Ernst, 116, 178
Le Moustier, 130, 206 McGraw, Scott, ix, 36
Leakey, Louis, 24, 113, 114, 117 McHenry, Henry, 144
Leakey, Meave, 115 meat-eating, 31, 138, 139,
learning, 84, 86, 87, 158, 159, 173, 207, 235 142, 155, 268
Lee Sang-Hee, 160, 207 mechanically challenging foods, 36, 75, 78,
Lee Thorp, Julia, 48 79, 82, 145, 149, 234
Leigh, Steve, 69, 85, 169, 201 Megadontia Quotient, 144
life history, 8, 84, 85, 86, 88, 89, 90, 91, 92, 93, Melanesians, 135, 215
97, 102, 104, 106, 108, 156, 157, 158, mesial, 5, 7, 17, 80
159, 160, 162, 164, 169, 171, 175, 179, microwear, ix, 37, 40, 41, 42, 43, 45, 47, 49,
199, 200, 201, 204, 207, 209, 219, 232, 50, 51, 54, 55, 142, 143, 152, 155, 191,
236, 237, 241, 259, 260, 261, 272, 233, 235, 236, 248, 250, 251, 252, 253,
276, 278 270, 274
life history mode, 169, 175, 219 microwear texture analysis, 40, 50, 191
life history modes, 176, 200 Miles, AEW, 160
lifespan, 37, 92, 97, 158, 170, 208 mitchondria, 134
linear enamel hypoplasia, 195, 196, 197, 198, mitochondrial DNA, 136
233, 236, 276, 280, 281 mtDNA, 136
linear enamel hypoplasias, 195 modularity, 158
lingual, 5, 7, 119, 120, 153, 239 Molnar, Steven, 190
Liu, Wu, 217 monogamous, 64, 67, 68, 78, 81
Liversidge, Helene, 105, 160, 165, 241 monogamy, 77, 78, 80, 81, 87
longevity, 8, 56, 157, 159, 160, 169, 170 Moormann, Stephanie, 239
long-period increments, 95 multi-male groups, 67, 68
Lovejoy, Owen, 19, 62, 77 Multiregional Continuity, 133
Lucas, Peter, 37, 42, 64, 72, 234 MYH 16, 145
286 index

Narikotome Boy, 169, 173, 174, 175, 235 phylogeny, 8, 14, 23, 133, 136,
Nariokotome Boy, 26, 167, 168 248, 249
National Evolutionary Synthesis Center, physiological stress, 4, 179, 195, 198, 199,
231, 242 209, 210, 236
natural selection, 36, 84, 93, 133, 134, 147, phytoliths, 37, 39, 42, 51, 187
158, 159, 181, 219, 224, 229, 270, 272 Pickering, Travis, 143
Neander Valley, 126 Piperata, Barbara, 172
Neanderthal anterior teeth, 128, 129, 190, placental mammals, 86, 89, 258, 259
191, 237 plaque. See dental calculus
Neanderthal molars, 129 Plavcan, Michael, 60, 66, 69, 78
Neanderthal teeth, 128, 179, 180, 184, 189, polygynous, 67, 81
192, 196, 199, 201, 203, 204, 205, 226 posterior teeth, 56, 115, 124, 137, 138, 144,
neonatal line, 107 165, 190, 235
New World monkeys, 71, 225, 255, 279 Potts, Rick, 144, 233
Nitrogen-15, 184 primitive traits, 12
Nutcracker Man, 24, 25, 32, 53, 114, 253 Probable Mutation Effect, 146, 156, 220,
221, 231
Obama, President Barak, 20 PME, 146, 147, 221, 222
Old World monkeys, 66, 72 prosimians, 60, 65, 106
Oldowan tools, 114, 139 Proteopithecus, 74
Olduvai Gorge, 24, 113, 114, 139, 143, pulp, 119, 226
262, 268
ontogenetic pathway, 73 Qafzeh, 127, 181, 219, 220, 230, 231, 237, 278
orangutans, 43, 59, 66, 91, 92, 105, 106
Orrorin tugenensis, 16 Recent African Origin, 134
Otzi, 227 Regourdou 1194, 275
Ouranopithecus, 74, 75, 254, 257 Reid, Donald, ix, 197, 242
outgroups, 14 relaxed selection, 78, 146, 147, 151, 152, 156,
Oxenham, Marc, 227 212, 220, 221, 235
OY ratio, 169, 170 Rensch’s rule, 66, 74
retromolar space, 127
Paranthropus aethiopicus, 24 Richard Wrangham, 32
Paranthropus boisei, 22, 24, 25, 26, 53, 54, 55, right-handed, 193, 194, 237
56, 57, 58, 100, 115, 143, 234, 248, ring-tailed lemurs, 65, 241, 272
252, 253, 260 Robinson, John T., 30
Paranthropus robustus, 24, 30, 32, 43, 46, 49,
50, 51, 52, 54, 57, 58, 98, 102, 106, Sahelanthropus tchadensis, 16
143, 226, 234, 235, 253, 279 Sauther, Michelle, 174, 241
parsimony, 13, 28 Schultz, Adolph H., 88
pathology, 4, 150, 151, 212, 226, 238, 279 Schultz’s Rule, 88, 160
Patterning Cascade Model, 153, 154, 238, 239 Sciulli, Paul, ix, 198
PAX 9 gene, 223, 225 Scladina, 206
Peking Man, 118 secretory stage, 93
perikymata, 98, 99, 100, 101, 103, 104, 163, sedges, 45, 51, 53, 54, 55, 57, 251
164, 167, 197, 198, 201, 203, 219, 237 septicemia, 150, 223
periodicity, 94, 95, 97, 99, 100, 104, 107, 108, sexual dimorphism, 8, 60, 64, 65, 66, 67, 68,
164, 167, 204, 218, 260, 271 69, 70, 71, 72, 73, 74, 76, 78, 80, 81,
periodontitis, 223, 226, 227, 243 82, 234, 254, 255
periodontium, 223 sexual maturity, 84, 85, 92, 97, 158, 199, 200,
phenetic, 12, 207, 209
 index 287

sexual selection, 59, 65, 67, 69, 71, 77, 78, 82, taurodont, 119, 121, 124, 129, 180
243, 254 Tayles, Nancy, 227
sexually monomorphic, 82 Templeton, Alan, 135
Shackelford, Laura, 205, 237 testosterone, 72, 73, 83, 228
Shipman, Pat, 139 Texture fill volume, 191
shovel-shaped, 119, 120, 128, 133, 180, Theropithecus oswaldi, 53
216, 217 thick enamel, 24, 34, 35, 36, 37, 38, 56,
shovel-shaped incisors, 119, 120, 133, 180, 241, 250
216, 217 third molar agenesis, 119, 217, 223, 224, 225,
Sima de Los Huesos, 125, 126, 136, 151, 152, Tigara, 198, 199, 203, 236
179, 180, 193, 212, 264, 267, 270, 275 tough foods, 3, 34, 42, 49, 54, 56, 72, 138, 143
Sivapithecus, 75 trace elements, 44, 46, 155
Smith, Fred, 218 Trinkaus, Erik, 208
Smith, Holly, 89, 102, 106, 158, 162, 163, 166 tropical grasses, 39, 45, 48, 57
Smith, Patricia, 221 Turkana Basin, 47, 142, 252
Smith, Tanya, 107, 163, 197, 203, 205, 218 Turner, Christy G, 213
Sorrentino, John, 242
sperm competition, 68, 81 underground storage organs, 32, 43, 50,
Sponheimer, Matt, 46, 52, 56, 57 51, 141
stable carbon isotopes, 44, 50, 253 USOs, 32, 43
stable isotopes, 184, 251, 273 Ungar, Peter, 49, 54, 142, 143, 148,
starch grains, 187 235, 241
Starrett, Alyssa, ix, 5, 7, 15, 17, 19, 20, 25, 26, Upper Paleolithic, 179, 186, 189, 198, 203,
33, 38, 48, 62, 70, 76, 101, 121, 122, 207, 208
127, 128, 129, 150, 161, 168, 180
Steinberg, Dan, ix, 196 Variability Selection Hypothesis, 144, 233
Steno, 1, 2, 246 Vega Lizama, Elma, 229
Sterkfontein, 50, 51, 251, 253 Volpato, Virgine, 194
Stewart, Kathlyn, 55, 57
Stiner, Mary, 186 Ward, Carol, 76
Strait, David, 32 weaning, 84, 89, 91, 92, 97, 106, 157, 158, 169,
striae of Retzius, 94, 95, 96, 99, 103, 164, 173, 199, 240, 259
201, 204 White, Peter, 221
Strontium-Calcium, 240 wisdom teeth, 20, 211
stuff and cut, 192 Wonderwerk Cave, 141, 263
suids, 38, 56 woolly spider monkeys, 68, 81, 255
Sundadonty, 213
Swartkrans, 50, 51, 57, 98, 253, 263, 279 Xing, Song, ix, 120, 180
Switek, Brian, 1
synchrotron, 95, 96, 99, 107, 121, 164, 205, ZY chromosome, 72
218, 234 Y’Edynak, Gloria, 222

Tai forest, 50 Zhiren Cave, 216

Taung Child, 15, 18 Zhoukoudian, 118, 119, 120, 125, 180, 181