RSTB_365_1556_Cover.

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Phil. Trans. R. Soc. B | vol. 365 no. 1556 pp. 3263–3410 | 27 Oct 2010
ISSN 0962-8436

volume 365

27 October 2010 number 1556

volume 365 . number 1556 . pages 3263–3410
pages 3263–3410
The first four million years of human
evolution In this Issue

Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer The first four million years of human evolution
Introduction Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer
The first four million years of human evolution 3265
A. Walker & C. Stringer
Articles
In search of the last common ancestor: new findings on wild chimpanzees 3267
W. C. McGrew
More reliable estimates of divergence times in Pan using complete mtDNA sequences
and accounting for population structure 3277
A. C. Stone, F. U. Battistuzzi, L. S. Kubatko, G. H. Perry Jr, E. Trudeau, H. Lin & S. Kumar
Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip–bent-knee gait 3289
C. O. Lovejoy & M. A. McCollum
Arboreality, terrestriality and bipedalism 3301
R. H. Crompton, W. I. Sellers & S. K. S. Thorpe
Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction 3315
M. Brunet

The first four million years of human evolution

Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (central Afar, Ethiopia) 3323
Y. Haile-Selassie
Anterior dental evolution in the Australopithecus anamensis–afarensis lineage 3333
C. V. Ward, J. M. Plavcan & F. K. Manthi
Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis 3345
P. S. Ungar, R. S. Scott, F. E. Grine & M. F. Teaford
An enlarged postcranial sample confirms Australopithecus afarensis dimorphism was similar
to modern humans 3355
P. L. Reno, M. A. McCollum, R. S. Meindl & C. O. Lovejoy
The cranial base of Australopithecus afarensis: new insights from the female skull 3365
W. H. Kimbel & Y. Rak
Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000 3377
F. Spoor, M. G. Leakey & L. N. Leakey
Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene 3389
J. A. Lee-Thorp, M. Sponheimer, B. H. Passey, D. J. de Ruiter & T. E. Cerling
Retrieving chronological age from dental remains of early fossil hominins to reconstruct human
growth in the past 3397
M. C. Dean

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The first four million years of human evolution
Papers of a Discussion Meeting held at the Royal Society on 19 and 20 October 2009.
Organized and edited by Alan Walker and Chris Stringer

Contents

Introduction
The first four million years of human evolution 3265
A. Walker and C. Stringer

Articles
In search of the last common ancestor: new findings on wild chimpanzees 3267
W. C. McGrew

More reliable estimates of divergence times in Pan using complete mtDNA sequences 3277
and accounting for population structure
A. C. Stone, F. U. Battistuzzi, L. S. Kubatko, G. H. Perry Jr, E. Trudeau, H. Lin
and S. Kumar

Spinopelvic pathways to bipedality: why no hominids ever relied on a 3289

bent-hip – bent-knee gait
C. O. Lovejoy and M. A. McCollum

Arboreality, terrestriality and bipedalism 3301

R. H. Crompton, W. I. Sellers and S. K. S. Thorpe

Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction 3315
M. Brunet

Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille 3323
(central Afar, Ethiopia)
Y. Haile-Selassie

Anterior dental evolution in the Australopithecus anamensis – afarensis lineage 3333

C. V. Ward, J. M. Plavcan and F. K. Manthi

Molar microwear textures and the diets of Australopithecus anamensis and 3345
Australopithecus afarensis
P. S. Ungar, R. S. Scott, F. E. Grine and M. F. Teaford

An enlarged postcranial sample confirms Australopithecus afarensis dimorphism 3355

was similar to modern humans
P. L. Reno, M. A. McCollum, R. S. Meindl and C. O. Lovejoy

The cranial base of Australopithecus afarensis: new insights from the female skull 3365
W. H. Kimbel and Y. Rak

Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of 3377
KNM-WT 40000
F. Spoor, M. G. Leakey and L. N. Leakey

3263
3264 Contents

Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary 3389
shift in the Pliocene
J. A. Lee-Thorp, M. Sponheimer, B. H. Passey, D. J. de Ruiter and T. E. Cerling

Retrieving chronological age from dental remains of early fossil hominins to 3397
reconstruct human growth in the past
M. C. Dean
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Introduction
The first four million years of human
evolution
In one of the last paragraphs of The origin of species
(1859), Darwin famously suggested that ‘Much light
will be thrown on the origin of man and his history’.
When he published The descent of man 12 years
later, there was still no fossil evidence of our earliest
evolutionary history, and nothing at all from the
African continent. Yet our close biological relationship
to the great apes, and especially the African apes, the
gorilla (Gorilla gorilla) and chimpanzees, had long
been recognized, even by scientists who were ignorant
of, or unsympathetic to, evolutionary thinking.
Nevertheless, when we remember his cautious nature
and the continuing powerful opposition to his ideas,
it still required fortitude for Darwin to venture ‘It is
therefore probable that Africa was formerly inhabited
by extinct apes closely allied to the gorilla and chim-
panzee; and as these two species are now man’s
nearest allies, it is somewhat more probable that our
early progenitors lived on the African continent than
elsewhere’. In explaining why the fossil evidence of
our origins was slow to appear, he prophetically
stated ‘Nor should it be forgotten that those regions
which are the most likely to afford remains connecting
man with some extinct ape-like creature, have not as
yet been searched by geologists’. In fact it was to
take another 50 years before such fossil evidence
began to emerge in Africa itself, and Darwin would
have been amazed by the remarkable evidence which
has accumulated since then concerning the earliest
stages of human evolution.
Spectacular discoveries of early members of the
human lineage, including nearly complete skeletons
and dozens of other 6 to 2 Ma fossils have been
made in the last 10 – 20 years. Single complete skel-
etons are much more useful analytically than
separate parts of many individuals, yet until recently,
few had been found from the period before 2 Ma.
Even Australopithecus, discovered in South Africa
in 1924, and published and named in 1925, is still
relatively incompletely known. For instance, the
famous ‘Lucy’ skeleton from Ethiopia is only about
20 per cent intact. But new and more complete early
hominin skeletons from different parts of the African
continent now promise to give us a much more
complete picture of the early phases in the history of
the human lineage.
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3265
Phil. Trans. R. Soc. B (2010) 365, 3265–3266
doi:10.1098/rstb.2010.0179
As discussed in one of the first contributions to this
volume, molecular estimates of the divergence time
between humans and chimpanzees presently converge
on approximately 5– 7 Ma, although we two are old
enough to remember the pre-molecular days, when
the supposed uniqueness of humans seemed to require
a time-span 2– 3 times those figures to account for the
evolution of special features like bipedalism and high
encephalization. But now, fossils of putative human
lineage members have been reported from approxi-
mately 6 Ma deposits in Chad and Kenya, and fossils
of the genus Ardipithecus from approximately 4.4 Ma
sediments in Ethiopia include about 40 per cent of a
complete skeleton. Views differ on the relationship
of these forms to each other, and to the succeeding
and better-known genus Australopithecus. Several
skeletons of the latter have been found in the last
few years. These include an adult from Sterkfontein
cave, South Africa, not yet certainly dated, another
adult from 3.8 Ma deposits in Woranso-Mille,
Ethiopia, a 3.3 Ma child’s skeleton from Dikika,
Ethiopia and four partial skeletons from Malapa
Cave, South Africa, dated to about 1.9 Ma. Dozens
of other less complete hominin fossils from approxi-
mately 6 to 2 Ma have been found, as well as these
skeletons.
Our meeting was timed to coincide with the double
celebration of Darwin’s 200th birthday and the 150th
anniversary of the publication of The Origin of Species,
and to take the first opportunity to bring together as
much as possible of the rich, newly published data
concerning the earliest-known members of the
human lineage. Through the generosity of the partici-
pants, our hope that detailed images and casts of the
new material would be brought together for the first
time during the meeting was amply met, although in
the event only one of us could be there to see the
outcome.
The meeting was also planned to showcase the
interdisciplinary nature of palaeoanthropology, by
highlighting the new methods that have been devel-
oped to extract behavioural and life history
information from fossils. These included computer
modelling of locomotor capabilities, finite element
modelling of stresses in bone, laser scanning compari-
sons of joint surfaces, quantification of semicircular
canal morphology and its relationship to head
motion, isotope analysis of teeth for dietary and cli-
mate reconstruction, confocal microscopy and
texture analysis of tooth wear to indicate diet, and
reconstruction of life history parameters from
This journal is # 2010 The Royal Society
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3266 A. Walker & C. Stringer Introduction
incremental lines in tooth enamel and dentine. The
analytical sessions highlighted what could be accom-
plished by the careful reconstruction, study and
analysis of the new fossils.
By concentrating on the early part of the record of
human evolution, the meeting was also able to docu-
ment the essential ecological, behavioural, and
morphological stages that underpinned the subsequent
emergence of the genus Homo. Field workers reported
on studies of the behaviour of wild chimpanzees as
possible models for early hominin behaviour, and on
the geological and environmental setting of the fossils,
as well as their anatomy and preservation. Context for
the discoveries was provided by colleagues who, for
example, used tephrostratigraphy, argon – argon radio-
metric dating, faunal and floral analysis, GIS satellite
imagery and taphonomy.
Our hope was to bring about a new understand-
ing of early hominin evolution by bringing together
the newest fossils and the latest analytical methods,
and we think the meeting at least helped progress
towards that ambitious goal. But the meeting also
provided the first opportunity to present many of
the newest discoveries to scientific and public audi-
ences alike. A memorable conference dinner was
accompanied by a display of replicas of spectacular
Phil. Trans. R. Soc. B (2010)
new material such as the just-published Ardipithecus
skeleton, and the reconstructed Sahelanthropus
cranium.
In the event, we have not been able to publish all of
the contributions made at the meeting, and this unfor-
tunately included a description of the very complete
australopithecine skeleton from Sterkfontein men-
tioned earlier. Nevertheless we feel that The first four
million years of human evolution was an appropriate
measure of how much progress the field of palaeoan-
thropology (a term unknown 150 years ago) has
made in meeting Charles Darwin’s expectations. We
would like to thank all the staff of the Royal Society
who worked on the planning and running of the meet-
ing, and the editorial team who has worked so hard to
bring this volume to fruition.
Alan Walker1
Chris Stringer2,* June 2010
1
Anthropology & Biology, Penn State University,
University Park, PA 16802, USA
2
Dept of Palaeontology, The Natural History Museum,
London SW7 5BD, UK
*Author for correspondence (c.stringer@nhm.ac.uk).
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Phil. Trans. R. Soc. B (2010) 365, 3267–3276

doi:10.1098/rstb.2010.0067

In search of the last common ancestor: new

findings on wild chimpanzees
W. C. McGrew*
Leverhulme Centre for Human Evolutionary Studies, Department of Biological Anthropology,
University of Cambridge, Cambridge CB2 1QH, UK
Modelling the behaviour of extinct hominins is essential in order to devise useful hypotheses of our
species’ evolutionary origins for testing in the palaeontological and archaeological records. One
approach is to model the last common ancestor (LCA) of living apes and humans, based on current
ethological and ecological knowledge of our closest living relations. Such referential modelling is
based on rigorous, ongoing field studies of the chimpanzee (Pan troglodytes) and the bonobo (Pan
paniscus). This paper reviews recent findings from nature, focusing on those with direct implications
for hominin evolution, e.g. apes, using elementary technology to access basic resources such as food
and water, or sheltering in caves or bathing as thermoregulatory adaptations. I give preference to
studies that directly address key issues, such as whether stone artefacts are detectible before the Old-
owan, based on the percussive technology of hammer and anvil use by living apes. Detailed
comparative studies of chimpanzees living in varied habitats, from rainforest to savannah, reveal
that some behavioural patterns are universal (e.g. shelter construction), while others show
marked (e.g. extractive foraging) or nuanced (e.g. courtship) cross-populational variation. These
findings allow us to distinguish between retained, primitive traits of the LCA versus derived ones
in the human lineage.
Keywords: tool use; shelter; diet; ranging; last common ancestor; chimpanzee

1. INTRODUCTION the extinct LCA, based on indirect evidence. Thus,

This paper aims to synthesize and to update recent
(from 2005 onwards) findings from studies of the
ethology and ecology of wild chimpanzees (Pan
troglodytes) that are relevant to modelling human
origins. Given space constraints, this exercise will be
limited to field studies, and therefore mostly to obser-
vational data on the spontaneous behaviour of apes
in situ, cited selectively. It emphasizes primary reports,
usually journal articles, on the assumption that older
secondary reviews (e.g. Mitani et al. 2002; McGrew
2004) provide access to earlier material. It concen-
trates on the eight study sites with fully habituated
subjects, here listed in the order of seniority: Gombe
(Tanzania), Budongo (Uganda), Mahale (Tanzania),
Kanyawara (Uganda), Bossou (Guinea), Taı̈ (Ivory
Coast), Ngogo (Uganda) and Fongoli (Senegal).
However, given the geographical bias to eastern and
western Africa, other sites with partly habituated sub-
jects, especially in central Africa, such as Goualougo
(Republic of Congo), are necessarily invoked too.
Most importantly, it focuses on topics that are relevant
to modelling the behaviour of the last common ances-
tor (LCA) of the divergent lines that led to living
humans and living chimpanzees. These topics are pre-
sented in terms of their ‘directness’ in comparisons
between what primatologists see now in living apes,
and what palaeoanthropologists seek to infer about
*wcm21@cam.ac.uk
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3267
this synthesis covers technology, diet, shelter and
ranging and foraging.
Attempts to use findings from ethological and eco-
logical (as opposed to morphological) research on
chimpanzees to model the behaviour of ancestral
humans are relatively recent, dating from the rise of
primatological field studies in the last 50 years.
Although most early field workers were interested in
apes in their own right, their mentors often had in
mind the potential applicability of the exciting new
findings to human issues (e.g. Goodall & Hamburg
1974). Many of the early attempts now look crude
and simplistic (e.g. McGrew 1981). For example,
most were content to talk about extinct hominids as
a single unspecified class, but as the hominin evol-
utionary record became more and more diverse, with
more and more taxa unearthed, this monolithic exer-
cise was less and less satisfactory. Furthermore, as
data began to emerge on wild bonobos, Pan paniscus
(Kano 1992), who are as equally closely related as
chimpanzees to hominins, and as cross-populational
variation began to emerge in chimpanzees (McGrew
1992), easy generalizations grew harder to make. Eco-
logical studies of chimpanzees in a variety of ecotypes,
from rainforest to savannah, forced more precise mod-
elling (Moore 1996). Finally, debate over the best way
to model human origins and evolution, that is, via
referential versus strategic models, or by homology
versus analogy, muddied the waters (e.g. Tooby &
DeVore 1987). Sayers & Lovejoy (2008) took the
extreme position that chimpanzees may be no more
useful as models than other, more ecologically,
This journal is q 2010 The Royal Society
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3268 W. C. McGrew Chimpanzees and the last common ancestor
zoogeographically and phylogenetically distant taxa,
such as capuchin monkeys (Cebus spp.). More recently,
Lovejoy (2009) has asserted that extant African ape-
based models are no longer appropriate (for a contrary
view, see Whiten et al. 2010). However, for focused
studies, such as of Oldowan lithic industries, apes
may still be the model of choice (Toth & Schick 2009).
This paper takes the conservative line that lacking
a fossil record for apes since the Miocene (cf.
McBrearty & Jablonski 2005), and having only a
shallow archaeological record for apes, all that we
sensibly can hope to model is the LCA. In doing so,
I make several simplifying assumptions, such as that
anything that a chimpanzee can do today, the LCA
could have done 6 – 7 Myr ago. Another pragmatic
assumption is that although the LCA could have
resembled the living chimpanzee, or bonobo, or
neither, or some combination of the two, most of
what we have to work with on grounds of homology
comes from P. troglodytes. Therefore, until comparable
breadth and depth of data are available for P. paniscus,
the chimpanzee must carry the load.
(a) Technology
Most of what behavioural primatologists have to offer
to palaeoanthropology relies on artefacts, as these
objects are comparable to what is found in the archae-
ological record. However, artefacts are the products of
behaviour, and sometimes archaeological data are a
further step removed: butchery cutmarks on bones
are the products of the ephemeral acts that produced
them. Whatever the caveats, primatologists can offer
something that no archaeologist will ever see, that is,
BOTH the product AND the behaviour, directly
recorded. When a glancing blow of a stone hammer
being used to crack a nut hits instead the stone anvil,
producing a conchoidally fractured flake, the observer
can see whether this was an accident. An archaeologist
given only that same single flake could draw no valid
inference about the percussionist’s intentions.
Studies of tool use by apes in nature have come
a long way from piecemeal natural history notes
collected opportunistically and descriptively, to com-
prehensive, systematic, hypothesis-driven empirical
efforts, some of which are experimental. Comparative
analyses of chimpanzee material culture are done at
every level, of individuals, lineages, communities,
populations, subspecies and species (McGrew 2004).
The chimpanzee ethnographic record now spans so
many study sites across equatorial Africa that even
chimpologists have trouble keeping them straight.
Although only eight sites consistently allow all-day,
close-up observation, there are five times as many
other sites with varying degrees of habituation. In the
5 years, long-term sites studying the central (Hicks
et al. 2005; Sanz & Morgan 2007) and Nigerian
(Fowler & Sommer 2007) subspecies have joined the
longer term studies in eastern and western Africa.
Even sites that have yet to habituate their subjects
have yielded new behavioural patterns, e.g. root-
digging at Ugalla, Tanzania (Hernandez-Aguilar
et al. 2007), fruit-cleaving at Nimba, Guinea (Koops
et al. 2010), etc. The only comprehensive study of
Phil. Trans. R. Soc. B (2010)
innovation in wild chimpanzees, at Mahale, shows
inventiveness to be common, but the chance that a
novel behavioural pattern will be propagated and
become established in a population is rare (Nishida
et al. 2009).
No longer is it enough just to list the types of tool
found at a given site, as nominal (presence/absence)
data. Now attention to relative frequency and compe-
tence of performance across age and sex classes is
expected, along with data on context, variation in
form and function of the tools’ manufacture and use
(e.g. Sanz et al. 2009a). Functional (e.g. extractive
foraging), biomechanical (e.g. percussive) and cogni-
tive (e.g. artefact complexity) aspects of technology
are stressed. Anecdotal versus idiosyncratic versus
habitual use of tools is differentiated. Distinction is
drawn between a tool kit (i.e. the whole repertoire of
a community’s collective range of tools) and a tool
set (i.e. the obligate sequence of two or more tools
used to achieve a single goal). Composite tools (i.e.
when two or more objects are used simultaneously
and complementarily to achieve a goal), such as
hammer and anvil (Carvalho et al. 2009), are distin-
guished from compound tools (i.e. when two or
more elements of different types are combined into a
single unit), such as a wedge used to level an anvil’s
working surface (Biro et al. in press). Typology is
now part of chimpanzee technology.
Tool kits show both uniformity and variety across
populations. Sanz & Morgan (2007) presented quanti-
tative and qualitative findings from the Goualougo,
Republic of Congo, chimpanzees, whose tool kit num-
bers 22 types, of which nine are used habitually
(customary). In contrast, Watts (2008b) published
comparable data from Ngogo, Uganda, where the
total tool kit numbers only 10 types, with four of
these being habitual. Such variation suggests the possi-
bility of a normally distributed spectrum, but this is
not the case. As with Goualougo, all habituated popu-
lations show about the same-sized tool kits: Gombe
(22), Bossou (21), Taı̈ (21) and Mahale (16). How-
ever, along with Ngogo, the other Ugandan sites
show small tool kits: Budongo (8) and Kanyawara
(10) (Sanz & Morgan 2007, table 3). Even more strik-
ing is the contrast between Goualougo and Ngogo
with regard to the predominate types of tools: the
top three at Goualougo are used in subsistence, that
is, extractive foraging of termites, honey and water;
the top three at Ngogo are used in hygiene, especially
wiping the penis after copulation, and in courtship.
(The reverse is equally true: Goualougo chimpanzees
very rarely use napkins, and Ngogo chimpanzees
rarely harvest insects.) However, some types of tool
use are chimpanzee universals, being found in all
long-studied populations across Africa, such as leaf
sponge (drinking water), aimed throw (weapon), play
start (toy), branch drag (display), etc.
Of particular importance is percussive technology,
that is, the application of ballistic force via one
object to another to achieve a goal (Ling et al. 2009).
In chimpanzees, this most famously takes the form of
hammer and anvil used to crack nuts, but it also
occurs in smashing hard-shelled objects directly
against anvils, in agonistic clubbing of adversaries or
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Chimpanzees and the last common ancestor W. C. McGrew
in display, or in specialized extractive foraging such as
pestle-pounding (Yamakoshi & Sugiyama 1995). In
the latter case, the pestle is a detached palm frond,
the mortar is the apical growth tip of an oil palm
(Elaeis guineensis) and the result is a cavity full of
mashed-up slurry, which is eaten. Anvil use without
hammers occurs when a hand-held, hard-shelled
fruit is bashed directly against a boulder or root, as
with baobabs (Adansonia digitata). Marchant &
McGrew (2004) hypothesized an evolutionary scen-
ario that led from anvil use to stone-knapping.
Tool sets in apes were first recognized in honey
extraction (Brewer & McGrew 1990). In seeking to
harvest nature’s most calorific food, the minimal tool
set requires a tool to break into the bees’ storage reser-
voir and another tool to extract the liquid. That is,
some kind of percussive tool, such as hammer or
chisel, plus some kind of dip-stick, are needed to
secure the food item (for the most complete treatment
of this resource’s exploitation, see Sanz & Morgan
2009). Tool sets may be more complex: Boesch et al.
(2009) recently described tool sets used by the chim-
panzees of Loango, Gabon, in which up to five tools
were needed, e.g. pounder, perforator, enlarger, col-
lector and swab. Tool sets also are used to exploit
other animal prey, e.g. termites (Deblauwe et al.
2006; Sanz & Morgan 2007), ants (Sanz et al.
2009b) and even when getting honey, the protein-
aceous bonus of bee brood may be important too.
The key point about a tool set is that it is sequential
task: if an A –B – C – D is necessary, then A – C– B – D
will not do; you cannot check the oil level in your
car’s engine via the dip-stick, until you have opened
the car’s bonnet. Although tool sets may suggest
advanced cognitive abilities, many such mandatory
sequences are shown by creatures with modest brains
(Hansell 2004), especially in shelter construction
(see below). What is impressive (and possibly
unique) about chimpanzee tool sets is that alternative
versions may be used flexibly by different apes to
solve the same problem.
In human elementary technology, composite tools
are well known: Mortar and pestle, bow and arrow,
etc. Each element may stand alone, but is almost use-
less without its partner. (Tool composites differ from
tool sets in that they are used simultaneously, rather
than sequentially.) Tool composites are known for
apes (see summary in Sugiyama 1997), and some are
widespread, for example, in all populations where
chimpanzees use long wands to dip for driver ants,
they also use bent-over saplings as a perch while
doing so, to avoid the painful bites of the ants swarm-
ing on the ground below (McGrew 1974). However,
only recently have tool composites been systematically
studied: Carvalho et al. (2009) showed that certain
combinations of stone hammers and anvils were used
over and over again by the chimpanzees of Bossou,
even taking into account the apes’ separate, indepen-
dent preferences for hammer or anvil.
Compound tools are harder to find in living apes in
nature, although their production is readily induced
under contrived captive conditions. Combination of
multiple items of the same type, e.g. leaves compressed
together in leaf-sponging for water, is the simplest kind
Phil. Trans. R. Soc. B (2010)
3269
of compound tool (Sousa et al. 2009), but it barely
qualifies, being iterative. The most obvious example
of compound technology (albeit not tool use) in
non-human primates in nature is the sleeping plat-
forms/nests/beds that are woven daily by great apes
(see below). The best-known example in the extractive
foraging of chimpanzees is the anvil– wedge, known
only from the nut-cracking of the Bossou chimpanzees
(Matsuzawa 2006). Bossou’s stone anvils are movable,
and so their positioning can be adjusted; anvils with
near-horizontal working surfaces are the most efficient,
as the yielded nut-meat is readily picked up. An angu-
lar anvil can be levelled by inserting a smaller stone
as a wedge underneath, to make the working surface
less tilted.
To what extent is the technological repertoire of the
chimpanzee now known? The steepness of the cumu-
lative ethnographic curve may be less than in the last
century, but it has not flattened out. New habitual pat-
terns continue to be described: chimpanzees use spears
to skewer small mammals (Pruetz & Bertolani 2007)
and digging sticks to unearth roots (Hernandez-Aguilar
et al. 2007). Furthermore, new modes of tool use
continue to emerge, such as the chimpanzees of
Nimba, Guinea, using cleavers to break apart large,
fibrous Treculia fruits (Koops et al. 2010).
Much progress has also been made on how individ-
ual apes in nature learn to use elementary technology.
Previous studies were descriptive or qualitative,
whereas modern ones use sophisticated multivariate
analyses (e.g. general linear mixed model) to tease
out the influences of independent variables.
Lonsdorf ’s (2006) study of termite fishing at Gombe
showed that although all chimpanzees in the Kasakela
community show this tool use by 5.5 years of age,
daughters acquire the skills earlier, and this acquisition
is a function of the mother’s overall time spent in the
activity. Humle et al. (2009) showed that chimpanzee
infants at Bossou who had more opportunities to
observe their mothers started ant-dipping sooner and
were more proficient than their low-opportunity
counterparts. However, in neither case were individual
differences in mother’s performance reflected in individ-
ual differences in their offspring, nor was there any
direct teaching by mothers. Youngsters learned to fish
or to dip by passive observational learning of tolerant
models. Matsuzawa et al. (2001) have termed this
dyadic conduit of information from one ape to another
as ‘education by master–apprenticeship’.
Some primatologists now apply archaeological
methods to the study of chimpanzee technology in
nature. Mercader et al. (2002, 2007) have shown that
the past nut-cracking activities of the Taı̈ chimpanzees
leave behind a record of stone artefacts. These can be
distinguished from human artefacts or naturally splin-
tered rocks by ‘blind’ assessors, dated by standard
radiometric techniques (C14), and yield organic resi-
dues (starch grains) that reveal their function. We
can now speak of a chimpanzee ‘stone age’ with time
depth. Carvalho et al. (2008) applied one of the core
concepts of archaeology, the chaine operatoire, to the
nut-cracking of Bossou’s chimpanzees, showing that
from start to finish, this analytical technique is equally
applicable to apes as to humans. Even retrospective
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3270 W. C. McGrew Chimpanzees and the last common ancestor
analyses of chimpanzee artefacts, in this case the
brush-sticks used to fish for termites, as found in a
museum, may explain how they were made (Heaton &
Pickering 2006; cf. Sanz & Morgan 2007). The
extent to which the archaeology of non-humans can
be pushed back in time remains to be seen, but a
new field is now underway (Haslam et al. 2009).
Finally, here is a sobering thought: of all the tools
named so far, only some of the hammers and anvils,
and some of the missiles thrown, will have a chance
of persisting in the archaeological record, taphonomy
willing, because they are made of stone. All of the
others are made of organic raw materials, e.g. plant
or animal matter, and so will perish over time. There
are other lithic objects used, e.g. stones in self-tickle,
pebbles in play start, boulders in splash display, etc.,
but it is unlikely that these will be archaeologically
recognizable.
(b) Diet
The chimpanzee is an omnivore, as all well-studied
populations show a mix of herbivory and faunivory.
The former is dominated by ripe fruit, but also
includes leaves, pith, seeds, flowers, bark, gum, etc.
The latter focuses on social insects (ants, bees,
termites) and small- to medium-sized mammals,
especially monkeys. Invertebrates usually are taken by
tool-assisted extractive foraging, such as ant-dipping,
ant-fishing, honey-dipping and termite-fishing, that
is, by gathering. Until recently, vertebrate prey were
known to be captured and dispatched only by hand,
without technology. Pruetz & Bertolani (2007)
showed that the chimpanzees of Fongoli, Senegal, use
a weapon-assisted hunting technique to disable or kill
bushbabies while they sleep during the day in tree
holes. The weapon is a sharpened stick (spear),
jammed into the prosimian’s sleeping chamber. (Some
sceptics have questioned whether the technique quali-
fies as hunting, or the instrument as a spear. When an
Inuit waits beside a seal’s air-hole in the ice, then thrusts
a sharp-ended linear object into it, skewering the prey,
we are happy to call it hunting, so why not for apes?).
Notably absent from the diets of most chimpanzee
populations are the underground storage organs
(USO) of plants, that is, bulbs, roots, tubers, corms,
rhizomes, etc. This absence was thought to reflect the
generalized, non-digging hands of primates, plus the
apes’ lack of the appropriate technology, that is, the dig-
ging stick. Hernandez-Aguilar et al. (2007) recently
described how the chimpanzees of Ugalla, Tanzania,
dig up roots, using sticks and pieces of bark that show
the abraded wear patterns of repeatedly used digging
tools. Spat-out wadges of fibrous roots show them to
be chewed and sucked, then discarded. A similar pro-
cessing technique is used by the chimpanzees of
Tongo, Democratic Republic of Congo, to get drinking
water from subterranean tubers, but these are dug up
by hand from friable, volcanic soils (Lanjouw 2002).
Across the continent, from Tanzania to Ivory Coast,
chimpanzee hunters take more monkeys as prey than
all other types of vertebrates combined, especially
favouring the red colobus (Piliocolobus badius) (e.g.
Watts & Mitani 2002). Others also hunt ungulates,
Phil. Trans. R. Soc. B (2010)
but one of the keenest hunting populations, the chim-
panzees of Taı̈, does not hunt the small forest
antelopes (Cephalophus spp.) that are plentiful there.
At the same time, several populations of bonobos
avidly hunt antelope, but were said to show no interest
in primate prey; this apparent species difference evap-
orated with Surbeck & Hohmann’s (2008) report that
the bonobos of Lui Kotale, Democratic Republic of
Congo, also hunt guenons (Cercopithecus spp.). What
differs between the two sibling species of chimpanzee
and bonobo is the sexual politics of meat-sharing.
In bonobos, females control the carcass and
distribute the meat, and their collective dominance
over males sometimes leaves the males with none,
even if individually a male can dominate a female
(Hohmann & Fruth 2008). In chimpanzees, males
often control carcasses, and there has been much
debate about how the sharing of the meat functions
in chimpanzee society. Now come solid data to test
Stanford’s (1999) hypothesis of meat-for-sex, that is,
that males selectively give meat to females in exchange
for sexual favours. Gomes & Boesch (2009) report that
females copulate more often with males who share
meat with them in the long term. Thus, the female
need not be in oestrus at the time of the hunt, but
rather forms a relationship that mutually enhances
the lifetime reproductive success of male (insemination
probability) and female (nutritional enhancement).
However, meat-sharing in some chimpanzee
populations, e.g. Gombe in Tanzania (Gilby 2006),
appears to be driven by different mechanisms:
intimidation, harassment, reciprocity, etc. Less likely
is Tennie et al.’s (2009) ‘meat-scrap’ hypothesis that
meat-sharing can be explained by the micro-nutrients
found in even small amounts of meat. Meat-eating is
only one kind of faunivory, and the same nutrients
can be easily obtained from invertebrates, which
chimpanzees eat daily.
Male sharing of prized foodstuffs with females also
occurs with plant foods, which otherwise is rare in
apes, usually occurring only between mother and
infant. However, Hockings et al. (2007) showed that
when males at Bossou raided crops, especially
papaya (Carica papaya), they almost always shared
the proceeds with females of reproductive age, even
when the latter were not in oestrus. These sharing pat-
terns reflected patterns of later sexual consortship.
What about scavenging? Scattered, anecdotal reports
of chimpanzee scavenging mammalian prey have
appeared from time to time, but no systematic study
was done until Watts (2008a) documented all known
scavenging opportunities at Ngogo over 11 years of
observations totalling over 10 000 h. In that period, he
saw only four scavenging events, and opportunities
were rare, occurring on average only every 100 h. This
contrasts mightily with over 650 kills made in over 270
hunts in the same period (Watts & Mitani 2002). Similar
pictures of rarity emerge from Gombe, Mahale and Taı̈.
Chimpanzees are not scavengers, it seems.
(c) Shelter
Shelter can be defined as the use of any material object
to buffer the effects of the elements. A universal
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Chimpanzees and the last common ancestor W. C. McGrew
behavioural pattern among great apes is their daily
construction of arboreal sleeping platforms: every
weaned individual builds an overnight nest and many
also build day nests for napping. These compound
artefacts are scattered over the landscape and may
endure for months, leaving a record of points in
space where chimpanzees spend most of their lives.
(Chimpanzees typically retire at dusk and arise at
dawn, and so spend half of each tropical circadian
cycle in their beds.) Hernandez-Aguilar (2009)
found 5354 nests over a 20 month period at Issa, an
open-country, savannah area in western Tanzania.
These shelters were highly clumped on woodland hill-
sides, in particular sites that were re-used over and
over again. The chimpanzees’ ranging and consequent
nest distribution varied predictably over wet and dry
seasons, reflecting an annual cycle of movement that
reflects availability of surface water and ripe fruit.
However prominent a part these shelters play in their
daily lives, these constructions later will be archaeolo-
gically invisible, being made entirely of woody
vegetation.
At the same time, studies of individual nests and
their making have yielded insights:
Koops et al. (2007) showed that at Nimba, surpris-
ingly many nests were built on the ground. From
the patterning and size of nests, they hypothesized
that this reflected a pattern of male overnight mate-
guarding, that is, when an oestrous female nested in
a tree, a male seemed to nest on the ground at its
base, to sequester her from the nocturnal attention
of other males. Various functions for nests have been
proposed: anti-predator, anti-parasite, anti-disease
vector, thermoregulation, etc., but there has yet
been no comprehensive study of these hypotheses.
Meanwhile, Stewart et al. (2007) studied the proximal
characteristics of nests, in terms of their architecture
and materials. First-hand empirical data showed that
chimpanzees prefer comfortable nests, presumably to
gain restorative sleep for their big brains.
The species’ name for the chimpanzee implies a
cave dweller, yet until recently, there was no record
of chimpanzees using caves as shelter. Pruetz (2007)
reported that the Fongoli chimpanzees, who occupy
one of the hottest and driest areas in the species’ distri-
bution, regularly use a cave during the hottest season
of the year. They retreat to its cooler environment
during the heat of the day for ‘siestas’ and picnics;
overnight, they sleep in arboreal nests, just like other
great ape populations.
Chimpanzees are notoriously hydrophobic, as they
do not swim, which makes watercourses notable bar-
riers to their geographical distribution. However, they
enter surface water in certain circumstances: at Fongoli,
they immerse themselves in temporary rain-filled pools
at the beginning of the rainy season, when it is still hot
and humid; there they rest, groom and play (Pruetz &
Bertolani 2009). Thus, water becomes a thermoregula-
tory device, even when potentially risky.
(d) Ranging
Although some authors (e.g. Lovejoy 2009) stub-
bornly continue to characterize evergreen rainforest
Phil. Trans. R. Soc. B (2010)
3271
as the typical ecotype for wild chimpanzees, and so
contrast their ecological context with that of hominins
who lived in more seasonal, mosaic habitats, this
restrictive picture is less and less tenable. Most of the
study sites at which chimpanzees have been studied,
and at least (depending on definition) three (Fongoli,
Gombe and Mahale) of the eight where the apes
have been fully habituated to close-range observation,
are not evergreen rainforest. More accurately, chim-
panzees subsist in a range of ecotypes, from
woodland savannah (not steppe) to rainforest, with
mean annual rainfall that range from about 800
to more than 2000 mm per year. Many of these
landscapes are vegetationally heterogenous, and chim-
panzee use of this array of habitat types varies greatly.
At the other extreme, chimpanzees (unlike baboons,
Papio spp.) do not survive in places that lack surface
water for drinking or that lack the riverine forests
that follow these watercourses, although only a tiny
fraction of such gallery forest will suffice. Copeland’s
(2007, 2009) detailed comparison of several open
and arid African habitats shows that landscapes with
annual rainfall in the 500 – 750 mm range cannot sup-
port chimpanzees. Early hominins apparently relied on
eating C4 plants and USOs, both of which have yet to
be shown to be important in the diets of chimpanzees,
despite recent prominent findings (Hernandez-Aguilar
et al. 2007). When drinking water runs short, that is,
during the dry season when water table drops below
the surface, chimpanzees turn to digging wells when
riverbeds are sandy enough to allow this (Hunt &
McGrew 2002). Although the wells are dug by hand,
leaf sponges are used to extract water from the wells;
it would not be surprising to find digging tools used
to dig wells in other substrates, e.g. mud, gravel, etc.
On a day-to-day basis, chimpanzees must find
ephemeral food. Frugivores in particular must find
and monitor clumps of food that should be eaten at
peak ripeness and which varies from year to year in
availability. The same grove that yielded a bumper
crop last year may not fruit at all this year. The biodi-
verse array of trees, shrubs and lianas, much less non-
woody plants, may present a potential cornucopia of
food, but the daily challenge is how to be in the right
place at the right time. Various hypotheses have been
put forward as to how chimpanzees achieve this, but
the strategy turns out to be simple:
Normand et al. (2009) showed that chimpanzees in
the Taı̈ Forest memorize the locations of thousands of
individual trees. Modelling of the apes’ powerful
spatial memory allows for their ‘rules’ of foraging to
be inferred, e.g. travel longer distances to resources
that allow longer feeding bouts, revisit more often
sources where you last ate for long periods.
But how to acquire such information? Murray et al.
(2008) showed at Gombe that even in adulthood and
long after their mothers have died, males return to
the core ranges used by their mothers, especially in
lean times. Resource locations learned during depen-
dent infancy are harvested lifelong.
It is all very well to know what resources are in the
home range, but how to know where they are, that is,
how to navigate optimally between them? Again, var-
ious hypotheses have been proposed, e.g. spatial
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3272 W. C. McGrew Chimpanzees and the last common ancestor
orientation by means of landmarks. Normand &
Boesch (2009) show from data on travel directions
and distances that Taı̈ chimpanzees have sophisticated
mental maps, that is, cognitive two-dimensional
representations of the landscape that allow them to
travel from resource to resource in straight lines.
2. DISCUSSION
What can now be said about the LCA, based on what
has been learned over the past 5 years from field
studies of wild chimpanzees?
Technology is the obvious starting point:
— Given the large and varied tool kits of the chimpan-
zee, we can expect that of the LCA to be similar.
That is, tools were made and used not just for
food acquisition and processing, but also in self-
maintenance and shelter, as well as in social and
sexual life (not covered here). However, just as
the size of tool repertoire in chimpanzees is a func-
tion of research effort, so it will be in recovering the
material culture of the LCA.
— Most of the presumed technology of the LCA is
archaeologically unrecoverable, given its perish-
able, organic nature; thus the archaeological
record is biased towards lithics. Short of a time
machine, this problem is insoluble, but aspects of
chimpanzee behaviour that are universal, such as
bed-making or leaf-sponging, are hard to deny to
the LCA.
— As with chimpanzees, the material culture of the
LCA will show inter- and intra-regional differences
(e.g. Schoening et al. 2008). Just as nut-cracking
differs between East and West Africa (Morgan &
Abwe 2006), despite the common presence of
both prey and raw materials (McGrew et al.
1997), so it is for the LCA. Similarly, just as extrac-
tive foraging for social insects is central to
Tanzanian populations of chimpanzees, but is lar-
gely absent in the neighbouring country of
Uganda, so we should not be surprised to find
such differences in e.g. Kenyan and Ethiopian
populations of a species of hominin.
— Subsistence technology in chimpanzees involves
reuse of artefacts, whether these are nut-cracking
hammers or ant-dipping wands. Especially given
that the extent of reuse seems to be a function
of availability of raw materials (and some African
forests afford no surface stones bigger than a
walnut, e.g. Lui Kotale, W. C. McGrew &
L. F. Marchant 2006, unpublished data), the
same is expected of the LCA. Just as at Bossou,
reuse of stone tools may increase the probability
of predictable fracture or amplified use – wear that
would leave archaeological signatures in the result-
ing artefacts. Lack of data on curation of tools by
apes in nature may reflect lack of precise study, as
evidence exists of such premeditated storage in
captivity (Osvath 2009).
— Given tool sets in chimpanzees, we should expect
the same in the LCA. But how to recognize
sequential use from a static assemblage? This is
further complicated by findings that anvils may
Phil. Trans. R. Soc. B (2010)
become hammers, as they are modified by use
(Carvalho et al. 2009). That is, tools may change
functional categories. (Studies of refitting may
help to distinguish reduction products from tool
sets; e.g. Delagnes & Roche 2005). Moreover,
application of knowledge from ape tool sets may
help make sense of patterned heterogeneity in
archaeological assemblages, as revealed by multi-
variate statistical analyses.
— Composite tools probably were used by the LCA,
but the challenge is to recognize such combinations
in recovered lithic assemblages. It is not always
clear what was the goal of reduction sequences in
knapping, such as core or flake. The best candidate
still may be pounding technology, as it seems likely
that flaked stone did not spring de novo with the
Oldowan, but more probably evolved from earlier
lithic percussion for other reasons. Perhaps the
analogues to chimpanzee hammers and anvils are
there to be found in deposits older than 2.6 Ma?
Primatologists should be able to help in seeking
the pre-Oldowan (Haslam et al. 2009), based on
reliably recognized modifications from chimpanzee
hammers and anvils. This may help to clarify per-
sisting confusion and controversy (e.g. Mora & de
la Torre (2005) versus Diez-Martin et al. (2009))
among archaeologists.
— Apart from their nest-building, chimpanzees have
few compound artefacts. In the evolution of
human elementary technology, much is made of
the first evidence of hafted weapons, that is, a com-
pound tool of shaft, point and fixative. However,
arguably, the earliest known compound technology
was necklaces of snail shells, as found in Blombos
Cave, South Africa (Henshilwood et al. 2004).
Whether or not the LCA had compound tools is
unclear, especially as not all components survive
equally well, e.g. the spear’s shaft versus its point,
the necklace’s string versus its shells.
— Studies of the acquisition and development of
chimpanzee technology remind us that some pro-
portion of what is found archaeologically is
probably the immature version of the polished
adult form of material culture. How much debitage
reflects ‘honest’ mistakes by youthful learners
versus clumsy or misguided efforts by adults?
This problem probably applies as well to the
LCA. Actualistic studies of children of various
ages learning to knap stone might be useful.
— Finally, we must repeatedly remind ourselves that
the LCA was almost certainly not a chimpanzee,
and vice versa. Just as living apes continue to
reveal new kinds of technology, so should we
expect the same from the LCA. If chimpanzees
turn out not to use tools to make other tools, or
lack important but basic material cultural items
like the container, or do not transport objects
over long distances, we may have found important
hominin watersheds (cf. Wynn & McGrew 1989).
Regarding diet:
— Chimpanzee opportunistic omnivory is clear, and
so it is probably in the LCA. The same inference
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Chimpanzees and the last common ancestor W. C. McGrew
derives from increasing evidence of dietary overlap
(e.g. monkey-hunting) between chimpanzee and
bonobo, although important differences remain
between these taxa (e.g. extractive foraging for
insects).
— Recent findings of chimpanzee use of USOs para-
doxically show apes to be capable of harvesting
these foodstuffs, yet in no known population are
they a staple (cf. Hockings et al. 2009, for data
on USOs as fallback foods). Experimental studies
need to be done on the limits of chimpanzee-
digging. Similarly, chimpanzees commonly
consume the pith of C4 plants, yet not the seeds
or corms, and so their stable isotope data are con-
fusing (Sponheimer et al. 2006). (It seems likely
that staple exploitation of cereals requires grinding
technology, which seems to be absent in wild chim-
panzees, but apparently has not been tested with
apes in captivity.) Or, it may be that profitable
use of USOs and cereals requires treatment by
fire, that is, cooking, which came much later
in human evolution (Carmody & Wrangham
2009). Here, studies of wild chimpanzees are not
yet helpful in hypothesizing about the LCA.
— Chimpanzees are wide-ranging foragers, and their
patterns of ranging map onto the distribution of
their resources, as in any other organism. What
we now are beginning to know is the extent of
their intelligent foraging, and it exceeds our expec-
tations, e.g. about spatial memory. This upgrades
our estimation of the LCA, but inferring the
timing and spacing of resources in the archaeologi-
cal record is problematic.
— Recent findings on chimpanzee hunting confirm its
seductiveness for evolutionary scenarios. (Conver-
sely, scavenging’s role seems less and less
important, at least until after the LCA, in the
hominin lineage.) However, estimations of the
importance of hunting, based on chimpanzees,
must be tempered: Most chimpanzee hunting is
done arboreally, by ‘four-handed’ hunters who
can leap about in the canopy, pursuing monkeys.
This is not likely to be instructive about hunting
by terrestrial bipeds, even if it applies to the
LCA, who may have practised ambush hunting
on the ground, as well as pursuit hunting in the
treetops. More significantly, the function of carniv-
ory is revealed to be much richer than expected:
sharing meat may drive social and sexual life,
almost as a currency (although many of the same
arguments probably apply also to honey).
On shelter:
— Based on the near-uniformity of arboreal overnight
sleeping off the ground in great apes, it seems likely
that the LCA did the same. It may be that safe ter-
restrial sleeping came much later, with the
domestication of fire (Pruetz & LaDuke 2010).
But we now know that cave use, at least during
the day, did not depend on fire, and that thermore-
gulation needs could have been for diurnal cooling,
rather than nocturnal heat retention. However,
Phil. Trans. R. Soc. B (2010)
3273
most chimpanzee field sites do not offer caves,
although this has never been systematically studied.
— We now know that chimpanzee nests are more
complex structures than hitherto realized, and
this may imply that beyond a certain point of
investment of time and effort, they began to be
reused. This raises the possibility of home bases,
already hinted at in the non-random distribution
of chimpanzee nest sites on the landscape. But
until we know the fitness-enhancing function of
beds, it would be rash to infer the same for the
LCA. Anti-predation is assumed, but equally
attractive alternative hypotheses are there to be
tested. The presence of ground nests is sometimes
presumed to be based on local release from preda-
tion, but no correlative study of sympatric large
carnivores and apes has been done.
On ranging and foraging:
— Chimpanzees are nomadic over areas that can be
large, that is, tens or even hundreds of square kilo-
metres. If the singlemost obvious influence on this
ranging is food availability, the more crucial limit-
ing factors may be drinking water and cover.
Well-digging, especially with the technological
assistance of digging tools and containers, appears
to allow an expanded ecological niche. (Unlike
temperature or humidity, which turn out not to
be so important.) Similarly, no matter how dry
and open the eco-type inhabited, every known
population of great apes seems to require access
to trees for shelter construction. Even savannah-
dwelling chimpanzees need their ribbons of gallery
forest. The same was probably true of the LCA.
In conclusion, even if one-tenth of what has been
learned in the last five years about wild chimpanzees
is applicable to the LCA of living apes and humans,
then the case has been made for preserving them.
Referential modelling requires living proxies upon
which to base the models, and current expectations
are that wild populations of great apes may be gone
by the middle of the current century. Both primatolo-
gists and palaeoanthropologists should work together
to save them.
Most of the author’s data and ideas were supported by the
US National Science Foundation, Researching Hominid
Origins Initiative (Award no. BCS-0321893) grant awarded
to Tim White and to the late Clark Howell. I am grateful
to S. Carvalho, L. F. Marchant, P. Mellars and A. Walker
for comments on the manuscript.
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Phil. Trans. R. Soc. B (2010) 365, 3277–3288

doi:10.1098/rstb.2010.0096

More reliable estimates of divergence times

in Pan using complete mtDNA sequences
and accounting for population structure
Anne C. Stone1,*, Fabia U. Battistuzzi2, Laura S. Kubatko4,
George H. Perry Jr1, Evan Trudeau6, Hsiuman Lin5
and Sudhir Kumar2,3
1
School of Human Evolution and Social Change, 2Center for Evolutionary Medicine and Informatics,
Biodesign Insitute, and 3School of Life Sciences, Arizona State University, Tempe, AZ, USA
4
Department of Mathematics and Statistics, and 5Department of Anthropology, University of New Mexico,
Albuquerque, NM, USA
6
Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, CO, USA
Here, we report the sequencing and analysis of eight complete mitochondrial genomes of chimpan-
zees (Pan troglodytes) from each of the three established subspecies (P. t. troglodytes, P. t. schweinfurthii
and P. t. verus) and the proposed fourth subspecies (P. t. ellioti ). Our population genetic analyses are
consistent with neutral patterns of evolution that have been shaped by demography. The high levels
of mtDNA diversity in western chimpanzees are unlike those seen at nuclear loci, which may reflect
a demographic history of greater female to male effective population sizes possibly owing to the
characteristics of the founding population. By using relaxed-clock methods, we have inferred a time-
tree of chimpanzee species and subspecies. The absolute divergence times vary based on the
methods and calibration used, but relative divergence times show extensive uniformity. Overall,
mtDNA produces consistently older times than those known from nuclear markers, a discrepancy
that is reduced significantly by explicitly accounting for chimpanzee population structures in time
estimation. Assuming the human – chimpanzee split to be between 7 and 5 Ma, chimpanzee time
estimates are 2.1 – 1.5, 1.1 – 0.76 and 0.25– 0.18 Ma for the chimpanzee/bonobo, western/
(eastern þ central) and eastern/central chimpanzee divergences, respectively.
Keywords: mitochondrial genome; Pan troglodytes; Pan paniscus; divergence time

1. INTRODUCTION genetic variation in these species shed light on their

Mitochondrial DNA has long been used to investigate
questions about primate taxonomy and demography
(e.g. Morin et al. 1994; Horai et al. 1995; Gagneux
et al. 1999; Schrago & Russo 2003; Eriksson et al.
2004; Raaum et al. 2005). The ability to sequence
the complete mtDNA genome relatively quickly and
inexpensively has resulted in a number of studies in
humans that investigate population history (Ingman
et al. 2000; Maca-Meyer et al. 2001; Herrnstadt et al.
2002; Ingman & Gyllensten 2003; Macaulay et al.
2005; Thangaraj et al. 2005; Sun et al. 2006) and
selection (Nachman et al. 1996; Mishmar et al. 2003;
Elson et al. 2004). However, the application of com-
plete mtDNA sequence data to questions about
population history and selection within other species
has not been common.
Chimpanzees (Pan troglodytes) and bonobos (Pan
paniscus) are our sister species, and studies of
* Author for correspondence (acstone@asu.edu).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rstb.2010.0096 or via http://rstb.royalsocietypublishing.org.
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
evolutionary histories as well as serve as a comparison
to our own history. Both paleoanthropological
and genetic studies indicate that that the human
and chimpanzee þ bonobo lineages diverged 6.5–
4.2 Ma (Sarich & Wilson 1973; White et al. 1994;
Chen & Li 2001; Glazko & Nei 2003; Kumar et al.
2005), while chimpanzees and bonobos diverged
more recently with estimates ranging from 2.5 to
0.8 Ma (Horai et al. 1992; Kaessmann et al. 1999;
Stone et al. 2002; Yu et al. 2003; Fisher et al. 2004;
Won & Hey 2005; Caswell et al. 2008). Genetic data,
as well as some morphological data, suggest strong
population structuring within chimpanzees that corre-
lates with subspecies boundaries, and this structure
appears to be demarcated by river and habitat bound-
aries and reinforced by dispersal patterns (Gagneux
et al. 2001; Guy et al. 2003; Lockwood et al. 2004;
Gonder et al. 2006; Becquet et al. 2007).
Currently, three subspecies, distributed across the
central part of Africa, are recognized within chimpan-
zees. Pan t. schweinfurthii is the easternmost
subspecies, located in Tanzania, Burundi, Rwanda,
Uganda and the Democratic Republic of Congo. The
central subspecies, P. t. troglodytes, is found in Congo,
Gabon, the Central African Republic, Equatorial

3277 This journal is q 2010 The Royal Society

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3278 A. C. Stone et al. Divergence times in Pan
Guinea and Cameroon, and P. t. verus, the western-
most subspecies, is found in Senegal, Guinea-Bissau,
Guinea, Sierra Leone, Liberia, Mali and Ivory Coast.
MtDNA research has also suggested a potential
fourth subspecies, P. t. ellioti (Oates et al. 2009), for-
merly known as P. t. vellerosus, in Nigeria (Gonder
et al. 1997, 2006; Gagneux et al. 1999), although the
limited Y-chromosome evidence has failed to support
this claim (Stone et al. 2002).
Demographic inferences about chimpanzee subspe-
cies are limited but mostly indicate a larger effective
population size in the central subspecies, and an initial
split between the western and central/eastern subspecies
(Deinard & Kidd 1999; Kaessmann et al. 1999; Stone
et al. 2002; Fisher et al. 2004; Won & Hey 2005; Bec-
quet et al. 2007). There has also been a distinction
between haploid markers (both mtDNA and Y-chromo-
some studies) that have shown high levels of structure
(corresponding to subspecies designations) and autoso-
mal nuclear data that have suggested significant gene
flow, differences in male and female effective population
sizes and/or incomplete sorting of lineages. On the one
hand, this has led to some researchers nominating new
subspecies based on results from haploid markers
(Gonder et al. 1997; Gonder Disotell & Oates 2006),
while others have proposed elimination of subspecies
designations altogether based on the nuclear data
(Fisher et al. 2006). In addition, some experts suggest
that the western and Nigerian chimpanzees should
form one subspecies (P. t. vellerosus), while the central
and eastern chimpanzees should belong to a second
subspecies (P. t. troglodytes; Gonder Disotell & Oates
2006). More recently, a large autosomal microsatellite
dataset has supported substructure within chimpanzees
that corresponds to the subspecies designations (Bec-
quet et al. 2007).
Comparisons of levels of intraspecific variability
have important implications for understanding the
evolution of hominoid genomes and clarifying the
demographic history of contemporary populations of
humans and great apes (Stone & Verrelli 2006).
Because of the different signals regarding population
history as well as the conflicting estimates of diver-
gence times based on different loci, a better sampling
of markers and populations is needed. In this study,
we report complete mtDNA sequences in eight chim-
panzees including individuals from all of the three
currently recognized subspecies as well as an individ-
ual with a P. t. ellioti mtDNA haplotype to assess the
neutrality of evolutionary patterns of the mtDNA
genome and to examine intraspecific diversity. A
major emphasis of our mtDNA analysis is to investi-
gate why the timing of divergence between
chimpanzees and bonobos and among the subspecies
of chimpanzees that have been reported from previous
mtDNA studies are much older than those obtained
using the nuclear DNA (e.g. Horai et al. 1995; Stone
et al. 2002; Fisher et al. 2004; Won & Hey 2005).
2. MATERIAL AND METHODS
(a) Materials
The complete mitochondrial genomes from seven
wild-born chimpanzees (four P. troglodytes verus, two
Phil. Trans. R. Soc. B (2010)
P. t. schweinfurthii and one P. t. ellioti ) and one captive
born chimpanzee (haplotype corresponds to
P. t. troglodytes) were sequenced for this study. When
unknown, subspecies status was determined based on
a comparison of the mtDNA HVI region sequence to
those from chimpanzees of known subspecies (Morin
et al. 1994; Gonder et al. 1997; Stone et al. 2002).
Two P. t. verus samples, Pt115 and Pt120 (ISIS no.
2738 and 2216), and the P. t. ellioti sample, Pt114
(ISIS no. 2412), were from the New Iberia Primate
Center. The remaining two P. t. verus samples, Pt82
and Pt105 (North American regional studbook for
the chimpanzee no. 341 and ISIS no. 2435), were
from the Riverside Zoo in Scottsbluff, NE, and the
Southwest Foundation for Biomedical Research,
respectively. The two P. t. schweinfurthii samples,
Pt96 and Pt161 (ISIS no. 3020 and 925), and the
P. t. troglodytes sample, Pt13 (ISIS no. 4441), were
from the Primate Foundation of Arizona. Whole
blood samples (5 –10 ml) were taken during routine
veterinary examinations, and DNA was isolated
using a standard phenol/chloroform-based extraction
(Sambrook & Russell 2001).
(b) Polymerase chain reaction and nucleotide
sequencing
The complete mtDNA genome was amplified in 28
overlapping segments using the polymerase chain
reaction (PCR) in a PTC-200 thermal cycler
(MJ Research). PCR primers for each segment are
listed in the electronic supplementary material. For
most segments, PCR conditions were: 948C for
5 min (948C, 30 s; annealing temperature specified
in table S1 in the electronic supplementary material,
30 s; 728C, 30 s) for 35 cycles, followed by a single
final extension of 728C for 5 min. A touchdown PCR
protocol was used for segments amplified with primers
L846 and H1620, L4589 and H5276 and L14110 and
H14900. For these segments, PCR conditions were:
948C for 5 min (948C, 30 s; 108C above annealing
temperature specified in table S1 in the electronic sup-
plementary material minus 0.58C per cycle, 30 s;
728C, 30 s) for 20 cycles, (948C, 30 sec; annealing
temperature specified in table S1 in the electronic sup-
plementary material, 30 s; 728C, 30 s) for another 20
cycles, then 728C for 5 min. PCR products were pur-
ified with the QIAquick Purification Kit (Qiagen) and
sequenced in two directions, using the BigDye termin-
ator cycle sequencing kit v. 3.1 (Applied Biosystems)
and an Applied Biosystems 3730 capillary sequencer.
Sequence trace files were assembled using the
SEQMAN program (DNAStar), and then manually
checked and aligned.
MtDNA insertions into the nuclear genome
(numts) can complicate analyses and invalidate con-
clusions if they are mistakenly amplified in the place
of authentic mtDNA sequence (Bensasson et al.
2001; Thalmann et al. 2004). Although there was no
direct evidence that numts had been amplified here
(i.e. there were no ‘heterozygous’ positions and no
nucleotide mismatches between overlapping frag-
ments), we checked the authenticity of our sequences
with the long-range PCR method described by
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Thalmann et al. (2004) using Platinum Taq HiFi
(Invitrogen). Briefly, for each chimpanzee individual,
we amplified two large fragments, A (approx. 9 kb)
and B (approx. 10 kb), which overlap each other at
both ends to cover the entire mtDNA genome using
primers listed in table S1 in the electronic supplemen-
tary material. Five microlitres of the PCR product was
electrophoresed through a 2 per cent NuSieve GTG
low-melting agarose (Cambrex) gel. Bands were
excised and melted in 100 ml Molecular Biology
Reagent Water (Sigma) at 558C for 1 h, and then
vortexed thoroughly. Four microlitres of this mixture
was then used to amplify and sequence three of our
original segments, using the methods specified above.
One of these segments (primers L15255 and H107,
1214 bp) was amplified from both fragments A and
B. Additionally, we amplified a 687 bp segment
(L4589 and H5276) from fragment A and an 862 bp
segment (L8333 and H9195) from fragment B. The
resulting sequences were compared with each other
and with the original sequence for each individual.
There were no observed discrepancies, supporting
the authenticity of the complete mtDNA genome
sequences generated for these eight individuals.
These data were submitted to GenBank and
are listed under accession numbers GU112738 –
GU112745.
(c) Data analysis
We compared our sequences with those from previous
studies, including two P. t. verus (Jenny, GenBank
accession number X93335 and the chimpanzee
mtDNA reference sequence no. NC 001643), one
P. paniscus (no. NC 001644), one gorilla (Gorilla
gorilla, no. NC 001645), one orangutan from each of
the two subspecies (Pongo pygmaeus, no. NC 001646
and Pongo pygmaeus abelii, no. NC002083), one
gibbon (Hylobates lar, no. NC 002082), the Cambridge
human reference sequence (Homo sapiens, no.
AC000021) and 53 additional humans (Anderson
et al. 1981; Horai et al. 1992, 1995; Arnason et al.
1996; Xu & Arnason 1996; Andrews et al. 1999;
Ingman et al. 2000). The hypervariable region or
D-loop is non-coding and was excluded from most
analyses because it is known to have a very different
mutational pattern.
Two estimates of diversity were calculated for each
locus: p is based on the average number of nucleotide
differences per site between two sequences randomly
drawn from a sample and us is based on the
sample size-corrected proportion of segregating sites
(Watterson 1975; Nei 1987). The Jukes & Cantor
(1969) correction was applied to all sequence
comparisons involving interspecific variation and
divergence (Lynch & Crease 1990). Under equili-
brium conditions with respect to mutation and drift,
both p and us estimate the neutral parameters: 2Nem
for mtDNA, where Ne is the effective population size
and m is the neutral mutation rate. Tajima’s D-statistic
was calculated to test for deviations from neutral fre-
quency distribution (Tajima 1989). The measures of
diversity and tests of neutrality were performed with
the program DNASP 4.0 (Rozas et al. 2003).
Phil. Trans. R. Soc. B (2010)
Divergence times in Pan A. C. Stone et al. 3279
The mutation rate for the complete genome,
excluding the D-loop region, was calculated from
the data as follows: mutation rate per site per year ¼
(k/2Tsplit)  l, where k is the mean genetic distance,
l the length of the sequence and Tsplit the time in
years since the human and chimpanzee divergence.
Tsplit is assumed to be 6 Ma. The mean genetic dis-
tance was estimated between the 10 chimpanzees
examined in this study and the 53 humans from
Ingman et al. (2000) using the Tamura– Nei distance
(Tamura & Nei 1993) with the evolutionary rates
among sites modelled using the gamma distribution
in MEGA 4 (Tamura et al. 2007). The shape par-
ameter for the gamma distribution was calculated
using MODELTEST as noted below.
MODELTEST (Posada & Crandall 1998) was used to
select the most appropriate evolutionary model
for each dataset. For the 13 protein-coding genes,
the general time-reversible (GTR) model with a
proportion of the sites invariable (I) and gamma-
distributed rates among sites (G ) was selected by the
AIC criterion. For the complete genome without
the D-loop, the GTR þ G model was selected by the
AIC. Phylogenetic analyses were then performed
using PAUP* (Swofford 2003) using the model and
parameters estimated by MODELTEST. Ten random
addition sequences with TBR branch swapping were
used to obtain the maximum-likelihood estimates of
the phylogenies. Bootstrap analyses were subsequently
performed using 100 bootstrap replicates and TBR
searches for each replicate for each dataset.
We calculated divergence times between species and
subspecies using two relaxed-clock methods: MULTI-
DIVTIME (MDT) and BEAST (Thorne & Kishino
2002; Drummond & Rambaut 2007). In these
methods, a Markov Chain Monte Carlo (MCMC)
procedure is used within a Bayesian analysis frame-
work to estimate the posterior distributions of
evolutionary rates and divergence times, given priors
on phylogenetic relationships and calibration nodes.
These analyses were performed using DNA sequence
alignment of the complete mitochondrial genome,
except the D-loop region, and for 13 protein-coding
genes separately. The protein-coding genes were ana-
lysed at amino acid and DNA sequence level as a
super-alignment. We also analysed the fourfold (4F)
degenerate sites by themselves, as their evolutionary
patterns are expected to be the closest to the strict
neutrality (Kumar et al. 2005).
In MDT, branch lengths of the amino acid dataset
(16 taxa, 3772 sites) were estimated with the mito-
chondrial mammal (mtmam.dat) model of
substitution, while for nucleotides (genome and 4F
sites) the F84 þ gamma model was used within the
PAML program package (Yang 2007). Initial number
of sites analysed for whole genome and 4F degenerate
sites were 15 514 and 1843, respectively. All sites con-
taining gaps and ambiguous nucleotides were excluded
from the analyses. Other parameters used in MDT
were: 10 000 sampling of the Markov chain, with
sampling frequency every 100, burn-in of 100 000,
and bigtime was set to 50 Ma. The root to tip distance
(rttm) was set at 25 Ma with identical standard
deviation (rttmsd).
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3280 A. C. Stone et al. Divergence times in Pan

Table 1. Diversity statistics for mtDNA. Length is excluding gaps. *Significance: p , 0.05.

taxa n length s p (%) u (%) Tajima’s D

complete genome
P. troglodytes 10 16 543 695 1.48 1. 49 20.16
P. t. schweinfurthii 2 16 556 38 0.23 0.23
P. t. s. and P. t. t. 3 16 556 134 0.54 0.54
P. t. verus (w/Nigeria) 7 16 548 413 0.95 1.02 20.49
P. t. verus 6 16 548 320 0.84 0.85 20.1
H. sapiens a 53 16 553 657 0.37 0.87 22.12*
without D-loop
P. troglodytes 10 15 441 544 1.23 1.25 20.16
P. t. schweinfurthii 2 15 443 26 0.17 0.17
P. t. s. and P. t. t. 3 15 443 95 0.41 0.41
P. t. verus (w/Nigeria) 7 15 441 298 0.72 0.79 20.59
P. t. verus 6 15 441 224 0.62 0.64 20.17
H. sapiens a 53 15 430 516 0.29 0.74 22.23*
a
Ingman et al. (2000).

The same data sets were analyzed also in BEAST 3. RESULTS

with an uncorrelated lognormal relaxed clock.
Substitution model used were the mtREV þ
gamma þ invariant sites model for amino acids and
the GTR þ gamma þ invariant sites for nucleotides.
We also separated models for population and species
divergences by using two populations based on the
geographical distribution of the western and eastern þ
central chimpanzee subspecies (two populations plus
one species model). The remaining divergences were
estimated under a Yule speciation process. The
length of the chain for each analysis was adjusted to
the dataset in order to obtain effective sample sizes
above 200 for all parameters.
The same prior information on times (lower and
upper bounds) was used for the two molecular clock
methods. These included the times of the following
species divergences: gorilla versus chimpanzee þ
human divergence (10 – 6.5 Ma) and the chimpanzee
and human divergence (6.5 – 4.2 Ma) times defined
as uniform distributions. These calibrations were
used together or separately depending on the dataset
and the hypothesis to test. MDT and BEAST yielded
divergence times and their 95% credibility intervals
(CrIs).
In addition to species and subspecies divergences,
BEAST also produces the age of the most recent
common ancestor (TMRCA) based on the population
sample included. We compared these estimates with
those obtained using the GENETREE program, which
simulates a coalescent process including time infor-
mation conditional on a specific haplotype tree with
a given value of u (Griffiths & Tavaré 1994; Bahlo &
Griffiths 2000). We estimated u for each dataset by
GENETREE using the maximum-likelihood method.
Indels and the D-loop were not included in the ana-
lyses, and constant population sizes and panmixia
were assumed. Simulation results are based on 10
million replicate runs. To calculate the TMRCA in
years, a chimpanzee generation time of 15 years was
used and the divergence between chimpanzees and
humans was set at 6 Ma.
Phil. Trans. R. Soc. B (2010)
The complete mtDNA genomes (16 541 bp) of 10
chimpanzees contain 695 segregating sites (table 1).
We also observe insertion/deletion (indel) polymorph-
isms in both the 12S rRNA gene and the D-loop. In
the 12S rRNA gene, an insertion of a guanine (G)
after nucleotide position 138 was present in all
sequences except the chimpanzee reference sequence.
This G is also present in humans (Anderson et al.
1981; Ingman et al. 2000) where it is found in stem
7 of the secondary structure model of Neefs et al.
(1993). In addition, a length polymorphism was
found in the 12S rRNA gene in the loop between
stems 23 and 24. Here, at nucleotide positions 378 –
384, an unstable run of cytocines resulted in signifi-
cant variation with at least 6 –15 cytocines present.
This region was difficult to PCR and produced a het-
eroplasmic sequence. In the D-loop, a total of 12
indels was found. Because it is difficult to properly
incorporate indels into models of sequence evolution
for estimating divergence times, these were removed
from further analyses.
Non-synonymous polymorphisms were found in all
13 protein-coding genes. On average, chimpanzee
sequences contained 28.8 non-synonymous differ-
ences when compared with 8.91 observed in
humans. The estimates of synonymous and non-
synonymous substitution diversities for each
mitochondrial gene as well as comparative data from
humans are shown in table 2. When examining silent
and replacement sites separately (table 2), Tajima’s
test rejected strict neutrality at a 5 per cent significance
level in chimpanzees only for non-synonymous sites at
CO3 and ND4L. Humans show many significantly
negative Tajima’s D-statistic for both synonymous
and non-synonymous sites. When data from only
P. t. verus (without Pt114) was examined, three genes
(ND1, CO2 and ND6) showed significantly negative
Tajima’s D-values at replacement sites. When Pt114
was included in P. t. verus, only replacement sites at
CO3 produced a significantly negative value (data
not shown).
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Divergence times in Pan A. C. Stone et al. 3281

Table 2. Population diversity estimates and tests of neutrality at mtDNA protein-coding genes in humans (n ¼ 53, Ingman
et al. 2000) and chimpanzees (n ¼ 10). *p , 0.05.

replacement silent

taxa and genes lengtha S pb TDc S p TD

Pan troglodytes
ND1 954 3 0.0016 0.13 41 0.0539 20.27
ND2 1041 16 0.0066 20.46 33 0.046 0.18
CO1 1539 4 0.0016 1.32 42 0.042 0.51
CO2 681 2 0.0013 20.03 14 0.026 20.46
ATP8 204 4 0.0097 0.23 4 0.025 20.45
ATP6 678 7 0.0054 0.39 25 0.051 0.11
CO3 783 6 0.0021 21.8* 28 0.058 0.68
ND3 345 5 0.0055 20.83 10 0.045 0.41
ND4L 294 2 0.0019 21.4* 9 0.048 0.81
ND4 1377 12 0.0032 21 46 0.045 20.05
ND5 1809 17 0.0046 0.23 63 0.05 0.07
ND6 522 3 0.0022 0.54 16 0.045 0.33
CYTB 1140 8 0.0035 0.11 54 0.069 0.18
all genes 11 316 88 0.0034 20.34 385 0.049 0.14
Homo sapiens
ND1 954 8 0.0007 21.93* 19 0.0087 21.49*
ND2 1041 13 0.0012 22.04* 29 0.0071 22.31*
CO1 1539 8 0.0008 21.32 40 0.0083 22.15*
CO2 681 3 0.0007 21.11 19 0.0067 22.32*
ATP8 204 2 0.0014 20.96 6 0.0158 21.18
ATP6 678 8 0.002 21.17 22 0.0096 22.08*
CO3 783 4 0.0003 21.73* 25 0.0105 22.01*
ND3 345 3 0.0028 0.12 10 0.0108 21.67*
ND4L 294 1 0.0002 21.32* 9 0.015 21.09
ND4 1377 12 0.0007 22.15* 43 0.0116 21.89*
ND5 1809 23 0.0015 21.95 51 0.0095 22.12*
ND6 522 5 0.0013 21.31 20 0.0118 22.01*
CYTB 1140 16 0.0011 22.2* 26 0.0099 21.66*
all genes 11 316 106 0.0011 22.19* 318 0.0096 22.17*
a
Length does not include the stop codon, for ‘all genes’, ATP8 and ND4L were truncated so that overlapping regions with other genes
were not counted twice.
b
Nucleotide diversity.
c
Tajima’s D-test.

Our analysis shows that chimpanzees harbour
approximately four times more nucleotide diversity
( p) than humans (table 1), while us is 1.7 times
greater. Within chimpanzees, P. t. verus exhibited the
most variation; however, multiple samples of the cen-
tral subspecies were not included in this study and
only two P. t. schweinfurthii were sampled. Despite
the population structure within chimpanzees, Tajima’s
test of the complete genome and also of only the
protein-coding genes did not show a significant depar-
ture from neutrality, while it is significantly negative
in humans (tables 1 and 2). These results support
the assumption of constant population size in
chimpanzees used in the GENETREE analysis.
For a reduced dataset including only the chimpan-
zees, the best evolutionary model selected by
MODELTEST using both likelihood ratio tests and the
AIC was the GTR þ G model with the shape par-
ameter in the gamma distribution, a, estimated to be
0.066. PAUP* was then used to estimate the ML
tree and bootstrap support. Using the entire dataset,
the phylogenetic analyses of both the complete
genome without the D-loop and using only the
protein-coding genes produced similar results
Phil. Trans. R. Soc. B (2010)
(figure 1). Bootstrap support was high (greater than
97%) for all nodes. The western chimpanzee
sequences, Pt82, Pt105, Pt115 and Pt120, the chim-
panzee mtDNA reference sequence and the sequence
for the chimpanzee Jenny cluster together with the
Nigerian sequence, Pt114, as their most closely related
taxon. The eastern chimpanzees, Pt96 and Pt161,
cluster with the central chimpanzee sequence, Pt13.
We first inferred a time tree of chimpanzee and
bonobo evolution by using the MDT software. In
this case, we used two primary time constrains:
10.0 –6.5 Ma for gorilla/(human þ chimpanzee) diver-
gence and 6.5 – 4.2 for human/chimpanzee divergence.
Using this calibration for full mitochondrial genome
(excluding the D-loop), only amino acid alignments
of 13 protein-coding genes and only 4F degenerate
sites produced similar estimates (table 3).
The chimpanzee/bonobo split was estimated to be
3.2 – 2.3 Ma. The time estimates for western/
(eastern þ central) and eastern/central splits were
dated to 1.68– 1.13 and 0.46 – 0.34 Ma, respectively
(table 3). Interestingly, MDT analysis yielded a
human/chimpanzee divergence date of approximately
5.7 Ma, which would be considered young by some
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3282 A. C. Stone et al. Divergence times in Pan

Pt161
100 eastern
Pt96 +
100 central
Pt13

100 Pt114
Pt115
100
Pt82
100
Pt105 western
97
100 Pt120
100
100 Jenny
100 Pt reference
100
P. paniscus
H. sapiens
G. gorilla
0.01
Figure 1. Maximum-likelihood phylogeny of chimpanzees, human and gorilla. Full mitochondrial genome (excluding the
D-loop) and 13 mitochondrial protein-coding genes gave similar results. The geographical location of the chimpanzee
populations is shown. Bootstrap values are shown near each node.

Table 3. Time estimates and 95% CrIs (in million years) for major divergences in the phylogeny obtained using MDT and
BEAST for three datasets (mitochondrial genome, amino acids, and 4F degenerate sites). MDT and BEAST coalescent
model do not model population structure within chimpanzees, which, instead, is accounted for in BEAST 2 þ 1 model.
MDT divergence times in parenthesis for the 4F degenerate sites are obtained with the human/chimpanzee calibration
fixed at 6.5 Ma. All other times are estimated using gorilla/human þ chimpanzee (10.0–6.5 Ma) and human/chimpanzee
(6.5 –4.2 Ma).

Mt genomea amino acidsb 4Fc

time 95% CrI time 95% CrI time 95% CrI

MDT
human/chimpanzee 5.69 4.76– 6.46 5.73 4.72 –6.46 5.65 (6.5) 4.49 –6.46
chimpanzee/bonobo 2.33 1.75– 3.14 3.17 2.23 –4.24 2.81 (3.35) 1.68 –4.19
western/eastern þ central 1.13 0.80– 1.70 1.5 0.86 –2.47 1.68 (2.04) 0.84 –3
Nigerian/western 0.55 0.37– 0.86 0.78 0.4–1.48 0.811 (1) 0.35 –1.66
eastern/central 0.34 0.22– 0.58 0.43 0.16 –0.93 0.458 (0.57) 0.7–1.11
BEAST (coalescent model)
human/chimpanzee 5.48 4.63– 6.5 5.43 4.46 –6.5 5.28 4.24 –6.35
chimpanzee/bonobo 2.02 1.53– 2.57 2.79 1.88 –3.72 1.79 1.23 –2.42
western/eastern þ central 0.96 0.70– 1.22 1.13 0.84 –1.85 0.92 0.62 –1.27
Nigerian/western 0.48 0.35– 0.61 0.72 0.45 –1.03 0.42 0.27 –0.60
eastern/central 0.27 0.18– 0.37 0.35 0.15 –0.58 0.21 0.11 –0.33
BEAST (2 þ 1 model)d
human/chimpanzee 4.94 4.2–5.68 4.87 4.2–5.73 4.7 4.2–5.43
chimpanzee/bonobo 1.76 1.35– 2.19 2.28 1.5–3.16 1.49 1.05 –1.99
western/eastern þ central 0.83 0.64– 1.04 1.05 0.67 –1.45 0.76 0.51 –1.01
Nigerian/western 0.41 0.32– 0.52 0.57 0.36 –0.80 0.35 0.23 –0.47
eastern/central 0.23 0.16– 0.31 0.27 0.1–0.44 0.18 0.095–0.27
a
Mitochondrial genome excluding the D-loop.
b
Thirteen mitochondrial protein-coding genes.
c
4F degenerate sites of the 13 protein-coding genes.
d
Two populations (western and eastern þ central) and one speciation model (Yule).

experts. Therefore, we re-estimated divergence times
in MDT by assuming the human/chimpanzee diver-
gence to be 6.5 and found that all the resulting time
estimates increased proportionally (table 3).
Because MDT assumes that evolutionary rates
among lineages are autocorrelated, we also estimated
Phil. Trans. R. Soc. B (2010)
divergence times using the BEAST software, which
allows rates among lineages to vary independently.
For genomic DNA and amino acid sequence analysis,
BEAST analyses produced estimates very similar to
those from MDT for the same sequences (table 3).
However, the BEAST analysis of 4F degenerate sites
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3.5
3.0
time estimates (Ma)
2.5
2.0
1.5
1.0
0.5
0 in the western subspecies ( p ¼ 0.94% for all or
chimpanzee/ western/
bonobo eastern + central
Figure 2. Compilation of estimated divergence times
between chimpanzees and bonobos and within chimpanzees
from literature (autosomal loci only, filled circle) and this
study (MDT, cross; BEAST (2 þ 1), square).
yielded much younger estimates (table 3). The above
analyses, however, did not take into account the popu-
lation structure of chimpanzees. In order to
incorporate this biological reality, we conducted
BEAST analysis by assuming that each P. t. subspecies
constitutes a population (western subspecies and
eastern þ central subspecies). This leads to a two
populations plus one speciation model (2 þ 1
model), which yields younger divergence times than
those obtained from MDT or from other BEAST
analyses (table 3).
Although the use of 2 þ 1 model in BEAST makes
results younger compared with the estimates obtained
without considering population structure within chim-
panzees, the time estimates based on amino acid
sequences are 50 per cent older than those from the
analysis of DNA sequences (genome as well as 4F
degenerate sites). Kumar et al. (2005) have previously
shown that amino acid time estimates are often older
and not preferred for relatively recent divergences.
Overall, the 2 þ 1 model produces time estimates
that are more similar to those reported from nuclear
autosomal loci (figure 2). Based on the 2 þ 1
BEAST analysis, the average divergence times within
the chimpanzees across three datasets are 2.28 – 1.49,
1.05– 0.76 and 0.27– 0.18 Ma for the chimpanzee/
bonobo, western/(eastern þ central) and the eastern/
central divergences, respectively (table 3). These
results highlight the need for modelling populations
correctly while estimating times of closely related
species and subspecies divergences when using
relaxed-clock methods.
The time to the MRCA (TMRCA) for each chim-
panzee population in the BEAST analysis was 0.35
and 0.18 (table 3). We compared these estimates of
TMRCA with those obtained from GENETREE, which
employs a coalescence process and estimates of diver-
sity to generate time estimates. The estimate of
sequence diversity for the complete genome, excluding
the D-loop, was 1.38  1028 substitutions per site per
year assuming a chimpanzee – human divergence
time of 6 Ma. Using this estimate and applying
GENETREE separately to each subspecies (western
and eastern þ central), we obtained TMRCA of
202 000 (+14 000) and 180 000 (+19 000) years,
Phil. Trans. R. Soc. B (2010)
Divergence times in Pan A. C. Stone et al. 3283
respectively. These results were similar to those
found by BEAST in the 4F dataset.
4. DISCUSSION
Studies of diversity and divergence times in chimpan-
zees, and primates in general, have frequently used
mtDNA. Similar to some previous studies (Morin
et al. 1994; Gagneux et al. 1999), our new data
indicate that diversity within chimpanzees is greatest
eastern 0.84% without the Nigerian individual), although
/central the sample size for the eastern/central subspecies
( p ¼ 0.54%) is rather small (n ¼ 3). This pattern of
diversity is contrary to those found at nuclear loci
where diversity estimates are higher in the central sub-
species. For example, analyses of NRY data showed
that central chimpanzees had higher levels of diversity,
because five different haplotypes were observed when
compared with only one observed in a much larger
sample of western chimpanzees (Stone et al. 2002).
In a survey of approximately 10 kb at Xq13.3 from
30 chimpanzees (17 P. t. verus, 12 P. t. troglodytes and
1 P. t. schweinfurthii), Kaessmann et al. (1999) found
that P. t. troglodytes were the most diverse. The mean
pairwise sequence diversity at this locus among
chimpanzees was 0.13 per cent, which is about four
times greater than that in humans (0.037%). We also
found a similar difference.
Kaessmann et al. (1999) also noted that the subspe-
cies were not monophyletic for X-chromosome
haplotypes (one western and one central chimpanzee
shared the same haplotype). However, Verrelli et al.
(2006) found that haplotypes were not shared between
subspecies for the X-chromosome locus G6PD. At this
locus, diversity was also greatest among central
chimpanzees in a survey of 56 chimpanzees
(6 P. t. troglodytes and 48 P. t. verus). Because the
X-chromosome has three times the effective popu-
lation size (Ne) of mtDNA, it should take three times
as long as mtDNA to achieve monophyly. So it is not
surprising that some of the X-chromosome lineages
are not completely sorted among the subspecies
given their likely divergence times.
Autosomal sequences also indicate higher diversity
in central chimpanzees followed by eastern and wes-
tern chimpanzees (Deinard & Kidd 1999; Yu et al.
2003; Fisher et al. 2004, 2006). Fisher et al. (2004)
found that central chimpanzees are 2.0 – 2.5 times
more diverse than western chimps and worldwide
samples of humans. Central chimpanzees also show a
relatively high proportion of rare alleles that could be
the result of an old bottleneck or fine-scale population
structure. Won & Hey (2005) found evidence for one-
way gene flow from P. t. verus to P. t. troglodytes and
suggest that this may be the result of interactions
between the Nigerian chimpanzees and the central
subspecies.
The distinct pattern of higher mtDNA diversity and
lower diversity at other loci found in western chimpan-
zees suggests that the founding population of this
subspecies may have been skewed with a larger
number of females and a smaller group of closely
related males. This pattern is perhaps not surprising
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3284 A. C. Stone et al. Divergence times in Pan
Table 4. Divergence times (in million years) and ratios among major divergences for 4F degenerate sites from BEAST 2 þ 1
model. The human/chimpanzee (H/C) time is used as the reference in calculating the time ratios. The gorilla/human þ
chimpanzee divergence was used as calibration (10.0–6.5 Ma) in all the estimations. The human/chimpanzee calibration was
used either as a range (6.5–4.2 Ma) or fixed (6.5 Ma). Absolute times with H/C at 5 or at 7 Ma were scaled according to the
ratios calculated.
BEAST (2 þ 1)a
absolute times (4F)
H/C ¼ (4.2 –6.5)
human/chimpanzee 4.70
chimpanzee/bonobo 1.49
western/(eastern þ central) 0.76
eastern/central 0.18
a
Two populations (western and eastern þ central) and one speciation model (Yule).
given the philopatric mating patterns of chimpanzees
where females disperse at adolescence, and males
remain within their natal group (Nishida 1979;
Pusey 1979; Wrangham 1979; Goodall 1986;
Pusey & Packer 1986; Langergraber et al. 2007;
Inoue et al. 2008). However, the pattern of higher
mtDNA diversity/lower nuclear diversity in western
chimpanzees compared with central þ eastern chim-
panzees indicate that the finding and/or subsequent
demography of the western subspecies was somehow
different from that found in the other subspecies. Gen-
etic studies confirm that the males within many
chimpanzee groups are typically more closely related
than females; however, this is not true in all groups,
particularly those where habitat fragmentation, disease
or poaching affect group demography (Morin et al.
1994; Vigilant et al. 2001; Lukas et al. 2005; Inoue
et al. 2008). The mtDNA data generated in this
study indicate that chimpanzee female effective popu-
lation size has been large (Ne ¼ approx. 36 000 for all
chimpanzees and approx. 20 000 for P. t. verus) with
no evidence of population bottleneck or expansion.
MtDNA data may also be affected by selection, and
several studies suggest that many mtDNA protein
polymorphisms are slightly deleterious in humans
(e.g. Nachman et al. 1996; Rand & Kann 1996;
Kivisild et al. 2006). In this study, we also found
evidence for a significantly negative value of Tajima’s
D for most mitochondrial protein-coding genes in
humans (and for the genome as a whole) which can
be indicative of population expansion and/or selection.
However, in these chimpanzee data, a significant
departure from neutrality was only found for CO3
and ND4L at replacement sites and there was no evi-
dence for a departure from neutrality for the genome
as a whole (table 2).
In molecular phylogenetics analysis of the complete
mtDNA of chimpanzees, bonobos, humans and other
great apes, human lineages are the most recent closest
relative of Pan, in agreement with the scores of pre-
vious studies. A more controversial issue in
chimpanzee evolutionary genomics has been the
timing of divergence between chimpanzees and bono-
bos and among the subspecies of chimpanzees owing
to the discrepancy between nuclear and mitochondrial
results. The results from our mtDNA analysis provide
Phil. Trans. R. Soc. B (2010)
time ratios (4F) absolute times
H/C ¼ 6.5 H/C ¼ (4.2–6.5) H/C ¼ 6.5 H/C ¼ 5 H/C ¼ 7
6.50 — — 5.00 7.00
1.94 32% 30% 1.49 2.09
0.98 16% 15% 0.76 1.06
0.23 4% 4% 0.18 0.25
partial resolution for this discrepancy. We find that the
lack of consideration of population substructure of the
chimpanzee subspecies when using mtDNA is a major
cause of this difference. Therefore, we consider the
time estimates from the use of two populations þ one
speciation model for analysing 4F degenerate sites
data in BEAST to be the least biased and most appro-
priate for estimating chimpanzee divergence times.
However, the absolute divergence times are strongly
influenced by the calibration points used. For
example, when using two calibration ranges (10.0–6.5
and 6.5 – 4.2 for gorilla/(human þ chimpanzee) and
human/chimpanzee splits, respectively), we obtain
chimpanzee/bonobo divergence of 1.49 Ma. However,
the human/chimpanzee divergence predicted by
BEAST in this case is only 4.70 Ma, which is
significantly lower than the current expectation.
By constraining the human/chimpanzee divergence
to be 6.5, the chimpanzee/bonobo time increases to
1.94 Ma. Interestingly, the ratio of the estimates of
human/chimpanzee and chimpanzee/bonobo diver-
gences is very similar (0.30–0.32) in different BEAST
analyses under 2 þ 1 model (table 4). Therefore, the
estimate of chimpanzee/bonobo divergence times
scales proportionally with the human/chimpanzee
calibration. In this case, mtDNA analyses suggest a
range of 2.09–1.49 Ma for chimpanzee/bonobo
divergence, because the best estimates of human/
chimpanzee divergence are in the range of 7–5 Ma
(Kumar et al. 2005; Hedges et al. 2006; figure 3).
These mtDNA estimates for chimpanzee/bonobo
are consistent with the range of 1.8 – 0.93 Ma based
on the earlier analysis of Y-chromosomes, non-
coding and non-repetitive genomic segments and
X-chromosomes (Xq13.3; Kaessmann et al. 1999;
Stone et al. 2002; Yu et al. 2003). However, more
recent nuclear genome analyses have typically yielded
a much younger date for this divergence (0.93 –
0.79 Ma). For example, Fisher et al. (2004) estimated
a divergence time of 0.80 Ma for this divergence using
a moment estimator method that examines the num-
bers of segregating sites at particular frequencies
(Wakeley & Hey 1997). Won & Hey (2005) obtained
an estimate of 0.89– 0.86 Ma from multiple datasets
(Deinard & Kidd 1999; Kaessmann et al. 1999;
Stone et al. 2002; Yu et al. 2003) using an isolation
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Divergence times in Pan A. C. Stone et al. 3285

Jenny
H/C: 6.5 – 4.2 Ma Pt reference
Pt120
Pt105 western
Pt82
Pt115
Pt114
Pt13 central
Pt96 +
Pt161 eastern
P. paniscus
H. sapiens
G. gorilla
Pongo pygmaues pygmaeus
Pongo pygmaeus abelii
Hylobates lar

H/C: 6.5 Ma Jenny

Pt reference
Pt120
Pt105 western
Pt82
Pt115
Pt114
Pt13 central
Pt96 +
Pt161 eastern
P. Paniscus
H. sapiens
G. gorilla
Pongo pygmaeus pygmaeus
Pongo pygmaeus abelii
Hylobates lar

25 20 15 10 5 0 Ma
Figure 3. Timetrees obtained from BEAST (2 þ 1 model) from 4F degenerate sites. The time scale is in million years (Ma).
Both trees used the gorilla/human þ chimpanzee calibration (10.0–6.5 Ma). Additionally, the upper tree used the human/
chimpanzee (H/C) calibration range of 6.5 –4.2 Ma while the lower tree fixed it at 6.5 Ma.

with migration (IM) model, as did Becquet &
Przeworski (2007) who estimated a split of 0.92–
0.79 Ma from two datasets using an MCMC method
to estimate the parameters of an IM
model. Recently, Hey (2010) estimated a split of
0.68– 1.54 Ma using a multi-population IM model,
while Wegmann & Excoffier (2010) used an approxi-
mate Bayesian computation approach to estimate a
divergence time of 1.6 Ma. These previous studies
and our analysis show how the time estimates are sen-
sitive not only to the choice of dataset, but also to the
models used to describe the chimpanzee’s population
structure.
Within chimpanzees, the western and central þ
eastern clades diverged between 1.06 –0.76 Ma
according to our mtDNA analyses. This is younger
than previous estimates from mtDNA (1.6 – 1.3 Ma;
Morin et al. 1994), but older than other estimates
based on nuclear loci. Fisher et al. (2004) examined
5.4 kb of autosomal sequence in 14 central and 16
western chimpanzees, and they propose a time of
0.65– 0.43 Ma for the divergence of western and
central þ eastern groups. Won & Hey (2005) also cal-
culated a divergence time estimate of 0.43 Ma for
the central and western subspecies, while Becquet &
Przeworski (2007) obtained much younger time
Phil. Trans. R. Soc. B (2010)
estimates (0.28 Ma for western/eastern split and
0.44 Ma western/central divergence). More recent
estimates range from 0.34 – 0.91 Ma (Caswell et al.
2008; Wegmann & Excoffier 2010). Therefore,
nuclear DNA time estimates are again much younger
than those indicated by mtDNA.
The eastern and central subspecies of chimpanzee
are estimated to have diverged recently. Although
these two subspecies do not appear to share either
mtDNA or NRY haplotypes, these haplotypes are
not monophyletic (Gagneux et al. 2001; Stone et al.
2002). From the limited number of sequences in this
study, we estimate the divergence of eastern and cen-
tral subspecies to be approximately 0.25– 0.18 Ma.
The Nigerian lineage appears to have diverged signifi-
cantly earlier (approx. 0.4 Ma). Even though the single
Nigerian lineage potentially diverged much earlier
than its closest relatives, there is yet no evidence
from Y-chromosome and autosomal STR markers
to elevate the Nigerian chimpanzees to a separate
subspecies (Stone et al. 2002; Becquet et al. 2007).
The consistent discrepancy among the different
divergence estimates, both within chimpanzees and
between chimpanzees and bonobos, are probably due
to the different population histories reflected by differ-
ent parts of the genome. The older divergence times
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3286 A. C. Stone et al. Divergence times in Pan
based on mtDNA data may reflect a demographic his-
tory of greater female effective population size in Pan
compared with the male effective population size
(Stone et al. 2002; Eriksson et al. 2006).
Despite the wealth of information gleaned from
complete mtDNA genome sequences to provide
insight into the maternal history and patterning of
humans (e.g. Ingman et al. 2000; Macaulay et al.
2005), such population genetic data have not been
available for other primates. In chimpanzees, complete
mitochondrial DNA sequences have previously been
published for only one of the three subspecies (Horai
et al. 1995; Arnason et al. 1996). Analysis of these
sequences along with eight additional sequences repre-
senting all of the recognized subspecies, including one
individual from the proposed subspecies P. t. ellioti,
add to the picture of diversity and population history
in this species; however, these data also illustrate the
need for additional sampling of chimpanzees through-
out their range. In addition, mtDNA data may be
affected by certain demographic scenarios (sex-
biased dispersal and bottlenecks), as suggested in
this study, as well as selection, and thus may not pro-
vide an accurate time scale of evolutionary or
population events unless population structure is con-
sidered (Nachman et al. 1996; Ballard & Rand
2005). Much of the primate diversity and taxonomic
data published to date relies solely on mtDNA data.
These studies should be eyed with caution until
additional data are available.
We thank Cecil Lewis, Vinod Swarna and Brian Verrelli for
helpful discussions and comments pertaining to this study
and/or manuscript. This study would not have been
possible without the samples generously provided by the
New Iberia Primate Center (supported by an NCRR grant
no. U42 RR015087 to the University of Louisiana at
Lafayette, New Iberia Research Center), the Primate
Foundation of Arizona, the Southwest Foundation for
Biomedical Research and Riverside Zoo, Scottsbluff,
Nebraska. This research was supported by the National
Science Foundation to A.S. (BCS-0073871), the National
Institutes of Health to S.K. (HG002096) and the Arizona
State University.
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Phil. Trans. R. Soc. B (2010) 365, 3289–3299

doi:10.1098/rstb.2010.0112

Spinopelvic pathways to bipedality:

why no hominids ever relied on a
bent-hip – bent-knee gait
C. Owen Lovejoy1,* and Melanie A. McCollum2
1
Department of Anthropology, School of Biomedical Sciences, Kent State University, OH, USA
2
Department of Cell Biology, University of Virginia, VA, USA
Until recently, the last common ancestor of African apes and humans was presumed to resemble
living chimpanzees and bonobos. This was frequently extended to their locomotor pattern leading
to the presumption that knuckle-walking was a likely ancestral pattern, requiring bipedality to have
emerged as a modification of their bent-hip-bent-knee gait used during erect walking. Research on
the development and anatomy of the vertebral column, coupled with new revelations from the fossil
record (in particular, Ardipithecus ramidus), now demonstrate that these presumptions have been in
error. Reassessment of the potential pathway to early hominid bipedality now reveals an entirely
novel sequence of likely morphological events leading to the emergence of upright walking.
Keywords: Australopithecus; bipedality; bent-hip – bent-knee; Ardipithecus; human evolution

1. INTRODUCTION now considerable evidence indicating that they have

For several decades, largely subsequent to the recovery
of A.L.288-1 (‘Lucy’) ( Johanson et al. 1982), upright
walking in early hominids was argued to have relied on
a bent-hip – bent-knee (BHBK) gait (see, e.g. Stern &
Susman 1983; Susman et al. 1984; Stern 2000). This
argument rested on observations of locomotion in
chimpanzees and gorillas, coupled with the presump-
tion that the post-cranium of our last common
ancestor (LCA) of Pan and Homo was fundamentally
similar to those of extant African apes (but see Filler
1981). Despite the fact that early hominids such as
A.L.288-1 (and other members of Australopithecus
afarensis and Australopithecus anamensis) exhibit
pelves, knees and feet with highly advanced adap-
tations to a striding, bipedal gait (Latimer & Lovejoy
1989; Lovejoy 2005a,b, 2007), the BHBK hypothesis
has remained largely unchallenged save arguments
based on energy consumption (e.g. Crompton et al.
1998; Carey & Crompton 2005; Sellers et al. 2005).
The BHBK gait of Pan and Gorilla, however, is not a
function of limitations imposed by hip or knee anatomy,
but is instead a direct consequence of an absence of
lumbar spine mobility. African apes are unable to lor-
dose their lumbar spines, and therefore must flex both
the hip and knee joints in order to position their
centre of mass over the point of ground contact
(Lovejoy 2005a). Lumbar immobility in Pan and
Gorilla is a consequence of their possession of only
three to four lumbar vertebrae and the ‘entrapment’
of the most caudal lumbar vertebra(e) between cranially
extended ilia (Stevens 2004; Stevens & Lovejoy 2004;
Lovejoy 2005a; McCollum et al. 2009). Although all
three African ape species share these features, there is
* Author for correspondence (olovejoy@aol.com).
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3289
not been retained from the common ancestor shared
with the human clade. Instead, a more detailed study
of the vertebral formulae and the lumbar column of
African apes and early hominids indicates that the
LCA of Pan and Homo most probably possessed a
long (six to seven segments) mobile lumbar spine simi-
lar in number to those of Old World monkeys (OWMs),
Proconsul and Nacholapithecus (McCollum et al. 2009).
Because such columns would have been capable of
near-full lordosis, these new findings in and of them-
selves contraindicate pronounced African ape-like
BHBK bipedality in early hominids. New revelations
about LCA structure provided by Ardipithecus ramidus
(especially ARA-VP-6/500; Lovejoy et al. 2009a–d;
White et al. 2009) further establish that hominids
never displayed any of the numerous African ape-like
specializations that have reduced lumbar mobility and
thus required an unusually restricted BHBK gait.
Here we review this new evidence.
2. THE AXIAL PATTERN OF THE LCA
As is discussed more fully in McCollum et al. (2009), it
is reasonable to assume that the modal vertebral for-
mula of basal hominoids and the LCA of Pan and
Homo to have been 7-13-6/7-4–one that differs from
those of OWMs merely by the addition of a fourth
sacral vertebra, and replacement of the external tail by
a short coccyx. Two lines of evidence support this view.
First is evidence provided by the vertebral formulae
of Australopithecus and early Homo (Sanders 1995).
Although complete axial data are unavailable for any
single early hominid specimen, a number of partial
specimens, including A.L. 288-1 (complete sacrum)
and KNM-WT 15000 (interpretable lumbar
column), indicate a pre-coccygeal vertebral formula
of 7-12/13-6-4 (Pilbeam 2004; McCollum et al. 2009).
This journal is q 2010 The Royal Society
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3290 C. O. Lovejoy & M. A. McCollum Spinopelvic pathways to bipedality

Gorilla P. troglodytes P. paniscus H. sapiens

7-13-4-5 7-13-4-6 7-13-4-7 7-12-5-5
7-13-4-6 7-13-4-5 7-13-4-6 7-12-5-6
7-13-3-6 7-13-3-6 7-14-4-6
T11 T11 T11 T10
T12 T12 T12 T11
T13 T13 T13 T12
L1 L1 T14/L1 L1
L2 L2 L2 L2
L3 L3 L3 Australopithecus L3
L4 L4 L4 7-12-6-4 L4
S1 S1 S1 7-12-6-5 L5
S2 S2 S2 7-13-6-4 S1
S3 S3 S3 T11 S2
S4 S4 S4 S3
S5 S5 S5 T12 S4
S6 LCA L1 S5
7-12-6-5 L2
7-13-6-4 L3
7-13-6-5 L4
L5
T11 L6
T12 S1
T13 S2
L1 S3
L2 S4
L3
L4
L5
L6
S1
S2
S3
S4
Figure 1. Probable pathways of lumbar reduction in African apes and hominids as deduced from extant vertebral formulae for
each taxon. All axial formulae that exceed 10% of the total sample for each taxon are shown here, along with presumed modal
formulae (those of highest probable frequencies) for the LCA and early hominids. A horizontal arrow indicates loss of a body
segment (i.e. a reduction in the number of somites contributing to the pre-coccygeal vertebral column). A vertical arrow sig-
nifies changes in the positions of the anterior boundaries of Hox gene expression domains underlying the indicated
transformations of vertebral identities. Note the differences in extant Pan species. For details, see McCollum et al. (2009).
Axial formula data from Pilbeam (2004) and McCollum et al. (2009). (q M.A. McCollum).

The second source of evidence is the axial
morphology of bonobos (Pan paniscus). Unlike chim-
panzees (Pan troglodytes) and modern humans, whose
modal number of pre-coccygeal vertebrae is 29/30,
bonobos possess an axial column typically composed
of 30/31 vertebrae, identical to that inferred for the
basal hominoid. Although it is certainly possible that
the long axial column of bonobos re-evolved from an
ancestor with an abbreviated column similar to that
of chimpanzees and modern humans, such modifi-
cation has no obvious selective advantage and runs
counter to the trend towards axial length reduction
observed in all suspensory anthropoids (Benton
1967; McCollum et al. 2009). Rather, the long axial
column of bonobos, along with the significantly differ-
ent combinations of sacral, lumbar and thoracic
vertebrae that are characteristic of common chimpan-
zees (seven cervical, 13 thoracic, three to four lumbar,
five to six sacral) and bonobos (seven cervical, 13– 14
thoracic, four lumbar, six to seven sacral), suggest
instead that the two species of Pan evolved their
short lumbar spines from an ancestor with a long
axial column (n ¼ 30/31 pre-coccygeal vertebrae)
and a long lumbar spine after division from their
own LCA. This receives support from data which
suggest that lumbar spine reduction in chimpanzees
apparently occurred through sacralization of the
Phil. Trans. R. Soc. B (2010)
caudal-most lumbar vertebrae plus reduction in the
number of somites (figure 1). Bonobos, conversely,
appear to have reduced their lumbar column purely
through transformations of segment identity, i.e. by
transforming lumbar vertebrae into sacral and thoracic
vertebrae (McCollum et al. 2009).
3. THE LOCOMOTOR SKELETON OF
ARDIPTHECUS RAMIDUS
The Ar. ramidus limb skeleton indicates that much of
extant African ape locomotor anatomy has been inde-
pendently derived for vertical climbing, suspension
and a feeding habitus that probably included high
canopy access in relatively large-bodied hominoids
(Lovejoy et al. 2009a). While OWMs also frequently
climb vertically, they nevertheless retain adaptations
that are primarily for more active, above-branch pro-
nograde running and leaping. Such acrobatics appear
to have become much more limited in hominoids, pre-
sumably inter alia, because of their significantly larger
body mass (Cartmill 1985).
The locomotor skeleton of Ar. ramidus establishes
that the LCA, unlike modern apes, retained many
OWM-like features sufficiently primitive to assure a
primary gait pattern of above-branch pronograde
palmigrady (Lovejoy et al. 2009a– c). To be sure,
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Spinopelvic pathways to bipedality
numerous modifications of OWM-like anatomy had
become more like that of extant hominoids in the
LCA (Lovejoy et al. 2009c)—alterations known to
have been initiated in likely exemplars of its remote
ancestors, especially various species of Proconsul
(Ward 1991, 1993; Ward et al. 1991, 1993;
Nakatsukasa et al. 2003). However, the Ar. ramidus
foot still retained a relatively elongated mid-tarsus, a
robust os peroneum complex and presumably numerous
soft tissue features associable with an inherently stiff
plantar structure more typical of the above-branch
propulsion seen in OWMs. These latter features can
be reliably extended to the LCA by parsimony, since
they are still present in the feet of modern humans
(quadratus plantae, plantaris, os peroneum, elongated
cuboid, etc.), but have been largely eclipsed by special-
izations in the feet and ankles of more highly
specialized, extant African apes (Desilva 2009;
Lovejoy et al. 2009a).
Similar observations of the Ar. ramidus forelimb
suggest that it also shares a number of primitive
features with humans. These include a very primitive
and unreinforced central joint complex (CJC)
(capitate, trapezoid, metacarpals 2 and 3), a relatively
substantial pollex, a short metacarpus, a lack of
significant Mc4/Mc5 – hamulus contact, a narrow tra-
pezoid, a palmarly displaced capitate head and an
unmodified, markedly rugose, deltopectoral crest.
Each of these has since been modified in extant
large-bodied African apes in favour of ones associable
with knuckle-walking, suspension and/or vertical
climbing (Lovejoy et al. 2009c).
4. THORACOABDOMINAL STRUCTURE
AND FORELIMB MOBILITY IN THE LCA
At the same time, it is equally clear that the LCA dif-
fered fundamentally from its likely ancestors
(including Proconsul) in several major ways, none
more important than the structure of its vertebral
column and its position within the thorax (Lovejoy
et al. 2009c). In comparison with Proconsul and
OWMs, in which the pectoral girdle is positioned
more anteriorly on the thoracic cage, the hominoid
pectoral girdle is located more dorsolaterally, in a
manner that causes its glenoid fossa to face more
laterally than is typical of more primitive taxa
(Waterman 1929; Schultz 1961; Erikson 1963; Ward
2007). Such ‘posterolateralization’ places the girdle
into a more favourable position for circumduction,
which in turn permits relatively large-bodied primates
to successfully negotiate the canopy via clambering,
bridging and suspension. What has gone almost
entirely unrecognized until the recovery of Ar. ramidus,
however, is that repositioning of the scapula (so as to
make the glenoid face more laterally and less ante-
riorly) in hominoids was achieved by thoracic
reorganization which relied on invagination of the
post-cervical spine ventrally into the thorax. This
resulted in dorsal repositioning of the lumbar trans-
verse processes (LTPs), a change in bauplan that
apparently occurred independently and repeatedly
even in some early Miocene hominoid taxa (e.g. in
Morotopithecus by 17 Ma; MacLatchy et al. 2000;
Phil. Trans. R. Soc. B (2010)
C. O. Lovejoy & M. A. McCollum 3291
Filler 2007a,b), and was significantly progressing in a
number of forms by the Mid-Miocene (e.g. in Pierola-
pithecus by at least 10 Ma; Moya-Sola et al. 2004;
Almecija et al. 2009). This shift appears to have
accompanied other forelimb modifications, especially
ulnar withdrawal and olecranon abbreviation. These
modifications increased potential wrist adduction,
enhanced stability during complete elbow extension
and greatly increased the forelimb’s range of motion
at the shoulder girdle (Rose 1988; Lewis 1989). How-
ever, as this change in bauplan also resulted in the
sacrifice of substantial erector spinae mass (Benton
1967; Lovejoy 2005a), increasing the range of
motion of the shoulder came at the expense of
dynamic stabilization of the lower back. Consequently,
African ape suspension and vertical climbing required
compensatory lumbar column reduction—virtually to
the point of inherent (i.e. osteological) rather than
dynamic (i.e. muscular) rigidity. Thus, LTP position,
rather than being the primary target of selection
during lumbar column shortening, as has long been
argued (e.g. Benton 1967), was instead a product of
the fundamental change in the hominoid
bauplan that centred about a general restructuring of
the thorax.
5. LOCOMOTION IN THE LCA
Features assignable to the LCA, therefore, now point
to a pattern of cautious climbing that combined
above-branch palmigrady with occasional below-
branch suspension, enhanced by a highly mobile, later-
alized shoulder girdle in combination with marked
wrist adduction (Cartmill & Milton 1977; Lewis
1989) and elbow extension (Rose 1988). Below-
branch suspension, however, must not have been so
frequently employed (and/or so vigorously performed)
as to require emergence of the considerably more
advanced metacarpal, carpal, elbow and shoulder
modifications seen only extant African apes. This
suggests that much of the LCA’s activities may have
been largely low-canopy, and might have been com-
bined, possibly extensively, with terrestrial travel
between food patches (White et al. 2009). The latter
supposition receives support from the fact that the
adaptations to terrestrial travel present in extant Afri-
can apes (knuckle-walking) and fossil hominids
(bipedality) are extensive, fundamentally divergent,
and therefore likely to be of substantial antiquity. It
is also likely that reliance on terrestrial travel between
food patches was driven by increasing competition
with radiating OWMs in the Mid-Miocene (Andrews
1981). That the post-crania of Pongo and the lesser
apes (Hylobates, Symphalangus) differ substantially
from those of the African apes is probably largely
due to the absence of a significant terrestrial com-
ponent in their respective adaptive strategies, and
their entirely independent evolution from much more
primitive ancestors.
If the above hypothesis is correct, what was the
LCA’s terrestrial locomotor habitus prior to the emer-
gence of either knuckle-walking in apes or bipedality in
hominids? One possible pattern ‘of choice’ might have
been a simple extension of its primary arboreal pattern
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3292 C. O. Lovejoy & M. A. McCollum Spinopelvic pathways to bipedality
to ground travel, i.e. palmigrade quadrupedality. In
fact, some of the more unusual characters present in
Ar. ramidus are strongly suggestive that hominids
once exhibited such an ancestral gait pattern. These
include its primitive intermembral index, relatively
short metacarpus, allowance of substantial metacar-
pal – phalangeal dorsiflexion and especially the
strongly palmar positioning of the head of its capitate
(Lovejoy et al. 2009b). Indeed, the latter can be
viewed as being particularly advantageous to palmi-
grade terrestrial quadrupedality, and this would now
seem to be a possible explanation for this unusual
peculiarity in Ar. ramidus, i.e. it inherited it from a
habitually terrestrial palmigrade LCA.
Unlike OWMs, quadrupedal terrestrial gait in
large-bodied hominoids (including the LCA) may
have required a much more compliant wrist, i.e. pal-
migrady that included more extreme dorsiflexion.
Absence of such extreme adaptations in OWMs is
likely explicable by their retention of primary
above-branch adaptations at the radiocarpal, elbow
and shoulder joints. Palmar disposition of the capi-
tate head as seen in Ar. ramidus (Lovejoy et al.
2009b) may even now serve, given further fossil evi-
dence, as an indicator of palmigrade/plantigrade
terrestrial quadrupedality in yet undiscovered, large-
bodied, Miocene forms. In combination with the
retention of a long mid-tarsus, a robust os peroneal
complex and other primitive aspects of its foot
(retained M. quadratus plantae, retained M. plantaris
and associated dense palmar fascial aponeurosis
(see earlier)), palmigrade/plantigrade quadrupedality
seems to have been, at the least, a likely terrestrial
locomotor habitus in the African ape/hominid LCA
(Lovejoy et al. 2009c).
6. LOCOMOTOR SPECIALIZATIONS
IN EXTANT HOMINOIDS
If so, from whence came the relatively highly special-
ized gait patterns of the LCA’s descendants:
bipedality in hominids and knuckle-walking in the
African apes? The latter is reasonably explicable in
these taxa as a relatively facile means of modifying pal-
migrade/plantigrade terrestrial travel into a form that
could be successfully combined with their highly
specialized modifications of the pelvis, thorax and
limb skeletons for suspension and vertical climbing.
Such changes included (independently in each
taxon) elongation of the forelimb, abbreviation of the
hindlimb, elongation of the metacarpus, stabilization
of several major carpal joints either by ligamentous
reinforcement or joint enlargement or both (especially
in the CJC), major revisions of overall scapular mor-
phology (predominantly in Pan as opposed to
Gorilla), cranial retroflexion of the ulnar trochlear
notch, modification of the deltopectoral enthesis and
especially, virtual fusion of the thorax and pelvis via
abbreviation and iliac fixation of the lumbar column
(see earlier) (Lovejoy et al. 2009c,d ). All of the modi-
fications to the forelimb would have reduced its
inherent stability and increasingly restricted its
energy-dissipating capacity during prolonged terres-
trial travel. These difficulties appear to have been
Phil. Trans. R. Soc. B (2010)
resolved by adoption of knuckle-walking, which per-
mits reliance on substrate-forced dorsiflexion of the
wrist that can be eccentrically resisted by powerful
wrist flexors as well as both the connective tissue envel-
opes and contractile components of the long digital
flexors. The uniqueness of these long flexors is evi-
denced by development of a distinctive flexor
tubercle on the proximal ulna in both Pan and Gorilla
(Lovejoy et al. 2009b).
The most salient question remaining, of course, is
the issue of the eventual adoption of bipedality in
hominids. Why did hominids exchange palmigrade/
plantigrade quadrupedality for upright walking?
While there have been many theories advanced for
this locomotor shift, most have been made untenable
by evidence now provided by Ar. ramidus (White
et al. 2009). The recent suggestion that bipedality is
a sequel to an arboreal upright stance stabilized by
overhead forelimb grasping (Thorpe et al. 2007a,b,
2009) is untenable because the practice has emerged
in Pongo as a consequence of that taxon’s extreme
adaptations to suspension, none of which were ever
present in hominids or their ancestors (Lovejoy et al.
2009c). The most likely explanation for the adoption
of terrestrial bipedality, in our view, continues to
involve novel adaptations in hominid social structure
that required upright locomotion for carrying. These
have been discussed extensively elsewhere (Lovejoy
1981, 1993, 2009).
7. SOME ADDITIONAL ANATOMICAL
CORRELATES OF BIPEDALITY IN HOMINIDS AND
ADVANCED ARBOREALITY IN EXTANT APES
As noted above, still equipped with a mobile lumbar
spine, the LCA was probably capable of at least facul-
tative lordosis, sufficient to place its hip and knee
either directly below its centre of mass or sufficiently
close to that centre so as not to generate excessive
ground-reactive torques so large as to require debilitat-
ing muscle recruitment during terrestrial travel. While
the earliest hominid gait pattern probably required
some degree of hip and knee flexion, research on
bipedality in OWMs now suggests that it would not
have been nearly as excessive as it is in extant apes,
so long as the lumbar column remained long and
mobile (as it is in OWMs). Studies of OWMs have
now greatly illuminated our understanding of its ori-
gins in hominids (Nakatsukasa et al. 1995, 2004,
2006; Hirasaki et al. 2004). Macaques trained to
walk bipedally expend less energy than do those in
which the behaviour is novel, so much so that the ani-
mal’s long flexible spine is permissive for convergence
with ‘human-style’ walking in the former. While those
using bipedality ‘in the wild’ exhibit upright gaits that
differ kinesiologically from human walking, those
exposed to long-term training for bipedality walk
‘with longer, less-frequent strides, more extended
hindlimb joints, double-phase joint motion at the
knee joint, and most importantly, efficient energy
transformation by using inverted pendulum mech-
anics’ (Hirasaki et al. 2004: 748).
While lordosis was certainly facilitated by the pres-
ence of six to seven lumbar vertebrae in the LCA
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Spinopelvic pathways to bipedality
4.25
4.00
log alar breadth
3.75
3.50 Homo
Pan
Gorilla
A.L. 288-1
3.25
BSN49/P27
KSD-VP-1/1
STS-14
3.00 human mean
4.20 4.50 4.80
log total sacral breadth
Figure 2. Components of sacral breadth in African apes
and early hominids. Scatter plot of log total sacral breadth
versus log alar breadth. The findings of a strong correlation
(r ¼ 0.901) between sacral breadth and alar breadth, and
an absence of any significant correlation between alar
breadth and centrum area (figure 3) indicate that total
sacral breadth in African apes and early hominids is largely
a consequence of alar breadth. Note especially the exceed-
ingly broad alae in the early hominid specimens. This is
consistent with their having mediolaterally expanded the
sacrum as an adaptation to free the most caudal lumbar
from contact with the iliac crest, and fully accounts for the
unusual platypelloidy in A.L.288-1 and Sts-14. Later, a
caudally directed gradient of increasing centrum size and
interfacet distance (see text) appears in Homo, and probably
accounts for the unusually large human centrum. Note the
much narrower alae in the two African apes compared with
those of all hominids.
(most probably six; figure 1), even in most OWMs
lordosis is not as complete as it is in five-lumbared
humans (Nakatsukasa et al. 1995; Hirasaki et al.
2004). One probable and very important reason is
that complementary motion in the most caudal
lumbar vertebra in OWMs is usually restricted by its
proximity to the posterosuperior portion of each iliac
blade. Such iliac– lumbar propinquity is usually suffi-
cient to probably assure at least some degree of
ligamentous restriction of potential motion.
Two characters that are uniquely associated with
hominid pelvic adaptations to bipedality are therefore
of particular interest: (i) an exceptionally short super-
oinferior iliac height (coupled with both anterior
extension of the anterior inferior iliac spine (AIIS)
and development of the greater sciatic notch) and (ii)
an extremely wide sacrum generated largely by excep-
tionally broad sacral alae (figures 2 and 3). Both of
these characters eliminate contact between the pos-
teromost iliac crest and the most caudal lumbar
vertebra, and are therefore likely to have appeared
early in hominids as a means of increasing the lordotic
capacity of the lumbar spine during terrestrial bipedal-
ity. Indeed, these changes are likely to have been the
earliest in the evolution of bipedality in hominids,
Phil. Trans. R. Soc. B (2010)
C. O. Lovejoy & M. A. McCollum 3293
4.25
4.00
log alar breadth
3.75
3.50
Homo
Pan
Gorilla
A.L. 288-1
3.25
BSN49/P27
KSD-VP-1/1
STS-14
3.00 human mean
6.00 6.25 6.50 6.75 7.00 7.25 7.50 7.75
log centrum area
Figure 3. Components of sacral breadth in African apes and
early hominids. Scatter plot of log centrum area (length 
breadth) versus log alar breadth. For discussion, see legend
of figure 2.
and largely exaptive for increased abductor capacity
during the single-support phase of upright walking
(Lovejoy et al. 2009c).
Moreover, three features of ape sacra appear to have
directly opposite polarity compared with those of
hominids (figures 2– 4): (i) their strongly abbreviated
sacral alae, (ii) their reduced lumbar number, and
(iii) their greater number of fused sacral elements,
the latter almost certainly achieved by progressive
sacralization of the most caudal lumbar element(s)
(McCollum et al. 2009). Alar reduction reduces the
space between the two ilia so as to promote contact
with the most caudal lumbar vertebra(e). In combi-
nation with the additional extension of the ilia
superiorly (especially by elongation of the iliac isthmus
at least in Pan; Lovejoy et al. 2009c), the African apes
achieved stabilization of the entire lower spine by its
fixation to the thorax—creating a rigid pelvothoracic
‘block’ in which the pelvis and thorax are separated
by a distance of only a single intercostal space (Schultz
1961). Both mechanisms compensate for the loss of
erector spinae mass (see earlier). Thus, both sacral
structure and superoinferior iliac length directly reflect
hominoid post-cranial natural history. Panids and
gorillids independently elongated their ilia, narrowed
their bi-iliac spaces and reduced the number of
lumbar vertebrae (often by sequestration as additional
sacral segments), all mechanisms that stiffened the
lower back and eliminated any possibility of lordosis.
Hominids, per contra, remained almost entirely plesio-
morphic, retaining both the primitive number of
lumbar (mode ¼ six) and sacral vertebrae (mode ¼
four), and in addition, expanded the sacral alae so as
to assure the full independence of the most caudal
lumbar, assuring its freedom to participate in lordosis
as well.
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3294 C. O. Lovejoy & M. A. McCollum Spinopelvic pathways to bipedality
2 misinterpretation from crushing defects. Not all of
2 3
3 of Oreopithecus. There is general agreement, based on
1 had five lumbar vertebrae (Harrison 1986, 1991;
1
Figure 4. Hominid and pongid mechanisms of emancipation
or fixation of the most caudal lumbar(s). A human pelvis
(left) compared with that of a chimpanzee (right). Note the
following numbered characters in each. The iliac isthmus
(1) and the ilium itself (3) have both been greatly shortened
in the human, so much so that a greater sciatic notch has
been created (entirely absent in the chimpanzee), and there
is no potential contact between the iliac crest and the most
caudal lumbar. In the chimpanzee, the opposite change has
occurred, i.e. the iliac isthmus (1) and the iliac blade (3)
have both been superoinferiorly elongated, encouraging
such contact. In addition, the sacral alae have been greatly
broadened in the human and narrowed in the chimpanzee
(cf. figure 2). As a consequence, there is now a very substan-
tial horizontal distance between the iliac crest and the most
caudal vertebra in the human (2), but a greatly narrowed
bi-iliac gulf in the chimpanzee. In combination with (1)
and (3), such narrowing in the chimpanzee (via reduced
alar breadth; cf. figure 2) results in full restrictive contact
between the iliac crest and the most caudal lumbar ver-
tebra(e). In the earliest phases of this morphological shift
in hominids, the pelvis became decidedly platypelloid, and
the enhanced iliac breadth encouraged a more effective use
of the anterior gluteal muscles as abductors during upright
gait (Lovejoy 2005a; Lovejoy et al. 2009d ). The latter was
thus an exaptation, rather than the primary adaptation.
8. THE QUESTION OF OREOPITHECUS
Delineation of the vertebral evolutionary pattern of
African apes and hominids throws considerable new
light on the troublesome issue of both the locomotor
pattern and phylogeny of perhaps the most enigmatic
hominoid of the later Miocene, Oreopithecus.
Arguments as to its potential phylogenetic relation-
ships and locomotor patterns have been many
(reviewed in Harrison 1986, 1991; Kohler & Moya-
Sola 1997; Rook et al. 1999). However, all have been
hampered by its extremely poor condition, largely
the consequence of its extreme compression during
fossilization. This has frequently led to excessively
liberal interpretations of its badly compromised
structure.
A case in point is the attribution of a lordotic spine
to this taxon based on a sagittal section of specimen
BA72, a crushed and compressed amalgam of three
lumbar vertebrae (Kohler & Moya-Sola 1997). It
seems inconceivable to us that such sectioning can
reliably indicate the presence/absence of wedging in
centra after they have been compressed to less than
one half of their dorsoventral diameter. A far more
conservative approach is to rely on more
Phil. Trans. R. Soc. B (2010)
straightforward morphological characters of greater
inherent reliability, and which are more resistant to
these appear to have been considered.
One of the most important is the vertebral formula
the ‘1958 specimen’ (IGF 11 778), that Oreopithecus
Kohler & Moya-Sola 1997; Rook et al. 1999). A lar-
gely overlooked vital statistic, however, is that it also
had six sacral vertebrae (Straus 1963; method of
Schultz 1961; for details, see McCollum et al. 2009).
This can be safely concluded from specimen BA-50,
which preserves five sacral foramina on the left side,
and at least four on the right. Moreover, the masses
of the right and left halves of the sixth sacral vertebra
appear to be fully symmetrical (therefore the right
side presumably had five full foramina as well). We
have demonstrated elsewhere that the basal hominoid
column almost certainly exhibited 13 thoracics
(among living taxa, only Homo and Pongo have any
significant incidences of fewer). Thus, the minimum
pre-coccygeal vertebral number in Oreopithecus was
31, which, as noted above, is the likely pre-coccygeal
vertebral number for basal hominoids and was prob-
ably modal for Early and Mid-Miocene apes as well.
Except for P. paniscus, a modal vertebral number as
high as 31 is extremely rare in extant species, occurring
in only 2.8 per cent of P. troglodytes and 0.06 per cent of
Homo (McCollum et al. 2009).
Much has been made of the putative ‘short,
broad, ilium’ of Oreopithecus and of its relatively
broad retroauricular segment (Hürzeler 1958). How-
ever, a substantial reduction in the size of the post-
auricular region of the pelvis appears to have
accompanied the spinal invagination underlying
scapular relocation in all hominoids (see earlier).
That reduction was in turn accompanied by a broad-
ening of the pre-auricular portion of the pelvis and
is therefore expected in any clade in which shoulder
reorganization occurred (Lovejoy et al. 2009c). This
same developmental process is likely to have re-
occurred a number of times in hominoid evolution,
and is almost certainly universally responsible for
the dorsal migration of the LTPs. Broadening of
the ilium well beyond comparable dimensions in
Proconsul is therefore fully expected in virtually any
large-bodied Miocene hominoid that exhibits
posterolateralization of the shoulder.
The fifth lumbar vertebra of the ‘1958 specimen’
lies (in situ) directly within its bi-iliac space, sharing
the same functional position as the trapped (immobi-
lized) L7 of a typical Presbytis and the L3 or L4 of
Pan (see Straus 1963; figure 5). Therefore, Oreopithe-
cus exhibits a maximum of only four potentially
mobile lumbar vertebrae. This is fully consistent with
its ‘classic’ adaptive regimen for suspension as also
seen in Gorilla, Pan and Pongo, and with directly oppo-
site polarity compared with their homologues in
bipedal hominids in a host of major adaptive charac-
ters (table 1). These included transformation of
lumbars via their sacralization, direct reduction in
lumbar number from the primitive condition and
entrapment (immobilization) of at least one lumbar
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Spinopelvic pathways to bipedality C. O. Lovejoy & M. A. McCollum 3295

(a) (b) (c)

Figure 5. (a) Sacra of a chimpanzee, (b) A.L. 288-1 and (c) a modern human. Note the extremely narrow sacrum of the
chimpanzee compared with the two hominids. Note also the much broader alae in A.L. 288-1 compared with its centrum.
Compare this with the similar dimensions in the human specimen (figure 2).

(a) (b)

1
2
(c) (d)

Figure 6. Comparison of interfacet distances in the third lumbars and sacra of African apes and hominids. The drawing on the
left demonstrates the comparison being made. In this drawing, the third lumbar has been rotated 1808 from its normal ana-
tomical position (its superior zygapophyses now point inferiorly) for comparison with those of the sacrum. Double-headed
arrows indicate the interfacet distance in each specimen. (a) chimpanzee; (b) gorilla; (c) A.L. 288-1 and (d ) human. Note
that in (a) and (b) the interfacet distance is greater in the lumbar vertebra than it is in the sacrum, whereas the opposite is
true of the two hominids. The increasing gradient of centrum size and interfacet distance in Homo may be an adaptation
that facilitated increased lordosis and thereby enabled lumbar column reduction. The opposite gradient in chimpanzees is
the likely source of reduction of the bi-iliac space. For discussion, see text. Redrawn from Lovejoy (2005a).

by contact with a posterodorsally extended iliac crest.
Given its primitive vertebral number, and a series of
others, such as its retention of an anterior keel on its
lumbar vertebrae (Straus 1963), Oreopithecus appears
to have acquired extensive adaptations to suspension
entirely independently of other Miocene clades (as
did Nacholapithecus; Nakatsukasa et al. 2007). It is
thereby unrelated to hominids, its similarities (which
are few; table 1) being largely minor convergences.
Any bipedality would have been largely driven by the
same context that does so in hylobatids—excessively
long forelimbs combined with highly abbreviated
hindlimbs (table 1).
Phil. Trans. R. Soc. B (2010)
One additional supposedly hominid character in
Oreopithecus is worthy of brief note. The degree of pro-
tuberance of its AIIS is not unusual for a non-hominid.
What distinguishes the AIIS in hominids from those in
apes is not its protuberance (those of Gorilla are often
very prominent), but rather its emergence from a
novel, separate physis, a hominid adaptation that is
almost certainly associated with dramatic expansion
of iliac isthmus breadth (Lovejoy et al. 2009b). There
is no evidence of a similar degree of broadening in
Oreopithecus (note its relative pelvic breadth in
table 1) and certainly none suggesting its origin by
means of a separate physis.
 3296

Phil. Trans. R. Soc. B (2010)

Table 1. Principal characters of Oreopithecus compared with those of other hominoids.

no. of no. of iliac width/length radius/ medial

no. of sacral lumbar functional forelimb length/ intermembral index (relative iliac tibia humerus/ cuboid third Mc length/
taxon vertebraa vertebra lumbars body mass(0.33)b indexb breadth)c indexb femur indexb lengthb body mass(0.33)b,d

Oreopithecus 6e 5e 4e 170e 119 80 120 117 very shortf 20.5

C. O. Lovejoy & M. A. McCollum

P. troglodytes 5 –6 3 –4 2 –3 160 106 66 111 101 short 24.7

P. paniscus 6–7 4 2–3 159g 101g 107g 108g short
Gorilla 5 –6 3 –4 2 –3 152 114 92 113 116 short 18.9
LCAh [4] [6] [6] [131– 143] [87–91] ? [88 –95] [77 –87] [long] ?
Ar. ramidus [4] [6] [6] 143 89–91 113 95 87 long ?
Au. 4 6 6 145 84 137 93 84 ? ?
afarensis
H. sapiens 5 5 –6 5 135 65–79 125 65 71 very long 15.8
Pongo 5 –6 3 –4 2 –3 192 138 74 147 130 very short 27.6
Hylobates 4 –5 5 4 278 130 49 145 116 short 34.1
Proconsul [4] 6 –7 6 (131 –134) 87 50 88 77 [long] ?
a
Method of Schultz (1961).
b
Data from sample described in Lovejoy et al. (2009c) or additional sources therein unless otherwise noted.
c
Data from Straus (1963), except for Proconsul, Ar. ramidus and Au. afarensis, which were obtained from casts.
Spinopelvic pathways to bipedality

d
Data for Oreopithecus from Susman (2004).
e
Oreopithecus data from Straus (1963) and examination of BA-50; other data from Pilbeam (2004) and McCollum et al. (2009).
f
See Kohler & Moya-Sola (1997).
g
Data from Morbeck & Zihlman (1989).
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h
Data in brackets hypothesized for LCA of African apes and humans and/or Proconsul based on Ar. ramidus and living hominoids.
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Spinopelvic pathways to bipedality
9. A NOTE ON POTENTIAL MECHANISMS IN
LUMBAR COLUMN MODIFICATION
In considering the anatomy of the lumbosacral spine, it
is of some interest that whereas in humans both the
overall size of the centrum and the distances separating
the articular facets (zygapophyses) increase in each
successively more caudal lumbar vertebrae, centrum
size and interfacet distances in extant African apes
instead decrease caudally (Latimer & Ward 1993;
figure 6). Lumbar centrum dimensions do not
appear to differ substantially in the only column that
permits their observation in Australopithecus (Sts-14;
Robinson 1972). There is, however, an increase in
the interfacet distance between the putative L3 and
sacrum of A.L. 288-1 (Lovejoy 2005a). The latter
findings suggest that the progressive caudal expansion
of both the interfacet distances and centrum dimen-
sions evident in Homo, but only partially adumbrated
in Australopithecus (i.e. no increase in lumbar centrum
dimensions, a retention of six lumbar vertebrae, but a
partial increase in interfacet distance), may be an
adaptation that permits a more intense lordosis in
humans, ultimately enhancing lumbar column stability
by allowing a reduction in total lumbar number. If so,
emergence of this gradient must have postdated Homo
erectus at 1.6 ma, since the lumbar column in
KNM-WT-15000 still numbers six with four sacral
vertebrae (Latimer & Ward 1993; Pilbeam 2004;
McCollum et al. 2009).
10. SUMMARY AND CONCLUSIONS
New evidence from the fossil record and from obser-
vations of extant hominoid skeletal anatomy leads to
several conclusions. Among the most important is
that hominids never acquired the numerous specializ-
ations seen in extant apes for vertical climbing,
suspension or knuckle-walking. This demonstrable
divergence between the natural histories of hominids
and those of all living apes renders most observations
of locomotor behaviour in the latter, whether con-
ducted in the laboratory or observed in the wild, no
longer directly relevant to the reconstruction of the
earliest locomotion of hominids. Bipedality in homi-
nids can instead now be seen to have emerged from
a predominantly primitive locomotor skeleton with a
long lumbar spine capable of at least partial lordosis,
and one never restrictively modified for suspension,
vertical climbing or knuckle-walking.
Suspension (e.g. Pongo, Hylobates) and vertical
climbing (e.g. extant African apes) have repeatedly
induced a rigid lower spine, especially as body mass
increased. This has been accomplished in a variety of
taxa in several ways, but always by a combination of
reduction in lumbar number (by reduction in somite
vertebral number and/or transformation of lumbar
identity) via modification of hox regulation and further
entrapment of a portion of the remaining lumbar ver-
tebrae by narrowing of the bi-iliac space. The latter has
been accomplished either by sacral narrowing or
dorsal extension of the iliac crest (e.g. Pan and
Gorilla), or both. The failure of hylobatids (but not
symphalangids (i.e. modal lumbar number ¼ 4) to
achieve the extreme lumbar column reductions seen
Phil. Trans. R. Soc. B (2010)
C. O. Lovejoy & M. A. McCollum 3297
in African apes is probably a product of their modest
body size and the unique nature of suspension in
these lesser apes.
The earliest hominids were able to functionally
achieve bipedality because they had never rigidified
their lumbar spines. Instead, they evolved an opposite
morphology—a reduction in iliac height and a broaden-
ing of the sacrum, both of which assured sufficient
lordosis to reduce and eventually eliminate what were
probably only moderate vertical moments about the
knee and hip. Were hominids to have first engaged in
African ape-like behaviours, the ‘Rubicon’ to
bipedality may have become too great to cross. Our
decades-long assumption that the abducent capacity
of the early hominid pelvis was its primary selective
agent (e.g. Lovejoy et al. 1973) was, in retrospect,
entirely misdirected. The favourable position of the
anterior gluteal muscles in hominids that allows them
to control pelvic tilt during single support can now
be seen to have been largely a refinement that followed
the initial primary adoption of a lordotic spine with an
emancipated caudal-most lumbar vertebra. The gener-
alized structure of earliest hominids that permitted this
sequence of events is almost certainly extendable to
the LCA. At least initially in pre-divergence homi-
noids, it now suggests a combination of cautious,
palmigrade, plantigrade climbing with a long flexible
back during arboreal travel, and possibly, palmigrade
quadrupedality during terrestrial travel as well.
We thank Alan Walker and Chris Stringer for organizing the
discussion meeting and the staff of the Royal Society for
ensuring its success. We thank David Pilbeam for extensive
help in constructing the bonobo sample used in this paper.
We thank Wim Wendelen and the staff and administration
of the Royal Museum for Central Africa, Tervuren,
Belgium for access to the primate collections in their care
and for the valuable assistance during our examination of
their specimens, and Yohannes Haile-Selassie and Lyman
Jellema for aid with examination of specimens housed at
the Cleveland Museum of Natural History.
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Phil. Trans. R. Soc. B (2010) 365, 3301–3314

doi:10.1098/rstb.2010.0035

Review

Arboreality, terrestriality and bipedalism

Robin Huw Crompton1,*,†, William I. Sellers2,†
and Susannah K. S. Thorpe3,†
1
Primate Evolution and Morphology Research Group, School of Biomedical Sciences, The University
of Liverpool, Sherrington Buildings, Ashton Street, Liverpool L69 3GE, UK
2
Faculty of Life Sciences, The University of Manchester, 3.614 Stopford Building, Oxford Road,
Manchester M13 9PT, UK
3
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK
The full publication of Ardipithecus ramidus has particular importance for the origins of hominin
bipedality, and strengthens the growing case for an arboreal origin. Palaeontological techniques
however inevitably concentrate on details of fragmentary postcranial bones and can benefit from
a whole-animal perspective. This can be provided by field studies of locomotor behaviour, which
provide a real-world perspective of adaptive context, against which conclusions drawn from
palaeontology and comparative osteology may be assessed and honed. Increasingly sophisticated
dynamic modelling techniques, validated against experimental data for living animals, offer a differ-
ent perspective where evolutionary and virtual ablation experiments, impossible for living
mammals, may be run in silico, and these can analyse not only the interactions and behaviour of
rigid segments but increasingly the effects of compliance, which are of crucial importance in guiding
the evolution of an arboreally derived lineage.
Keywords: bipedalism; biomechanics; evolution; field studies

1. INTRODUCTION and the panins (bonobos and common chimpanzees),

Darwin’s (1871) argument on human origins has
never appeared stronger than now, when molecular
evidence suggests a divergence time of only 5– 8 Ma
for humans and their extinct relatives (the tribe Homi-
nini), from the chimpanzees and bonobos (tribe
Panini; Bradley 2008). But as pointed out by Tuttle
et al. (1974) in their excellent review, Darwin, while
he did not present a detailed model of the last
common ancestor of humans and other African apes,
made an important point that is too often ignored:
that we should not expect the last common ancestor
to resemble either living humans or other living apes
particularly closely.
2. BIPEDALISM: AN ARBOREAL OR
TERRESTRIAL ORIGIN?
In the first four decades of the twentieth century, it was
generally accepted that bipedalism had an arboreal
origin (e.g. Keith 1903, 1923; Morton 1922; Schultz
1936). But for the last 60 years, since the first field
study of mountain gorillas by Schaller (1963), the
field studies of chimpanzees by Goodall (1998), and
the ensuing recognition (e.g. Zihlman et al. 1978) of
a special and genetically very close relationship
between the hominins (humans and their ancestors)
* Author for correspondence (rhcromp@liv.ac.uk).
†
All authors contributed equally to this manuscript.
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3301
the prevailing paradigm for the origins of human
bipedalism has been the knucklewalking quadrupedal-
ism model (first proposed by Washburn (1967) and
reviewed by Tuttle et al. (1974)). This model holds
that the common ancestor of hominins and panins
would have looked much like chimpanzees do today,
and so bipedalism would have arisen in an ancestor
which was a terrestrial, quadrupedal knucklewalker,
like the panins, and the remaining African apes, the
gorillines.
This paradigm was developed in some detail by
Gebo (1992, 1996), who identified heel-strike planti-
grady as a common, shared-acquired character of
African apes linked closely to knucklewalking quadru-
pedalism, and to the hominin acquisition of a
terrestrially adapted foot. However, heel-strike planti-
grady is not limited to the African apes (Meldrum
1993; Crompton et al. 2003); also, heel-strike is actu-
ally particularly clearly expressed in an Asian ape, the
most arboreal of great apes, the orangutan, subfamily
Ponginae (Crompton et al. 2003, 2008).
All great apes can and do walk bipedally, and most
do so in an arboreal context. Again, it is the most
arboreal, the orangutan, which uses bipedal locomotion
most often (Thorpe & Crompton 2005, 2006). While
bipedal locomotion supported by the hindlimbs alone
makes up only about 2 per cent of arboreal locomotion
of orangutans, a further 6 per cent consists of bipedal-
ism where one or both forelimbs are used for balance.
But this small percentage of locomotor bipedalism (or
compressive orthogrady, if preferred) plays an
This journal is # 2010 The Royal Society
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3302 R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism
ecologically crucial role in movement on the fine per-
ipheral branches, where fruits are located. It further
allows orangutans to bridge from tree to tree at
canopy level, avoiding the very high costs (Thorpe
et al. 2007a) and predation risk associated with cross-
ing on the ground. It is again the orangutan which of
all living apes approaches closest to us in one of the
most important of the biomechanical features ident-
ified by Alexander (1991) as characteristic of human
walking: namely stiff-legged, upright gait. As a conse-
quence of its stiff-legged gait, the orangutan
produces, in a fifth of its bipedalism, double-humped
vertical ground reaction force curves (vGRF) which,
alone among apes, overlap with those produced by
human walking (Crompton et al. 2003), and which
allow a high degree of pendular energy conversion.
Our calculations indicate that while in untrained
common chimpanzees energy conversion in bipedal-
ism reaches little more than 8 per cent, it approaches
some 50 per cent in untrained orangutans, still well
short, of course, of the 70 per cent possible in
humans (Wang et al. 2003). But while it has recently
been argued that the elongated, inverted foot of the
orangutan does not at all closely resemble our own
(Sayers & Lovejoy 2008), orangutan foot function in
bipedal walking, expressed in the pattern of foot
pressure, is actually very similar (Crompton et al.
2008) to that of the bonobo (Vereecke et al. 2003),
often suggested by others as a model for the
common panin –hominin ancestor (e.g. Zihlman
et al. 1978 and reviewed in Vereecke et al. 2003).
It has been apparent for the last few years that a
growing number of scientists have found cause to
doubt whether firm evidence exists in the fossil
record for a knucklewalking origin: see, e.g. Stern &
Susman (1983) for Australopithecus afarensis; Ward
et al. (1999) for the South Turkwel handbones and
Clarke (1999, 2002) for the StW-573 hand. A range
of purported ‘knucklewalking features’, dorsal ridges
on the distal aspect of the metacarpals, os centrale
– scaphoid fusion or extension of the proximal articu-
lar surface of the capitulum onto its dorsum, have
been sought in the hominin fossil record, but have
either not been found or found only inconsistently.
Dainton & Macho (1999) raised doubts about whether
knucklewalking was a homologous phenomenon even
in chimpanzees and gorillas. However, Richmond &
Strait (2000) argued that the distal radial morphology
of Au. afarensis was evidence for a knucklewalking
phase in evolution some time between 3.6 Ma and
the commonly accepted 5 – 8 Ma limits for genetic
separation of hominins and panins. It is therefore note-
worthy that the morphology plotted by Richmond &
Strait (2000) lies well within the orangutan range of
variation. Only large male Bornean orangutan make
much use of the ground, the Sumatran tiger being a
major discouragement to terrestriality on that island,
the clouded leopard posing a threat to small or juvenile
orangutan on Borneo. Large Bornean males have too
much unstable mass above the hip to sustain unas-
sisted bipedalism, and so tend to cross the ground
quadrupedally. But when crossing the ground they
do not walk on the middle phalanx, as chimpanzees
or gorillas do, but on their proximal phalanges or on
Phil. Trans. R. Soc. B (2010)
the side of their hand. Richmond et al. (2001), however,
stoutly defended a knucklewalking origin in an exten-
sive review, and Richmond & Jungers (2008) claimed
that similarities in curvature of a single phalanx of the
late Miocene protohominin Orrorin to that in chimpan-
zees represented evidence of knucklewalking, although
Orrorin is regarded by its discoverers as arboreally
adapted, orthograde and bipedal when moving on the
ground (Senut et al. 2001). Kivell & Begun (2007)
however found no clear functional link between os cen-
trale–scaphoid fusion and knucklewalking and Kivell &
Schmitt (2009) argue that there are two functionally
distinct modes of knucklewalking in African apes: that
in chimpanzees being associated with extended wrist
postures in an arboreal environment (directly addressing
Richmond & Jungers 2008), and that in gorillas with a
neutral wrist posture in a terrestrial environment.
Kivell & Schmitt (2009) go on to argue that the pur-
ported knucklewalking features of hominins are
instead adaptations to arboreality, and thus that
bipedalism indeed arose in the arboreal ecological
niche common to living apes.
While the absence of purported knucklewalking fea-
tures in the hand of Au. afarensis (e.g. Stern & Susman
1983) leaves little time for hominins to lose any such
features after the separation of hominins and panins
5– 8 Ma, the publication of a full description of
Ardipithecus ramidus shows that knucklewalking
features, including dorsal distal metacarpal ridges are
also absent in Ar. ramidus (Lovejoy et al. 2009a),
with the exception of os centrale– scaphoid fusion.
However, recall that Kivell & Begun (2007) found
no functional link to knucklewalking for this feature.
This extends the lack of evidence for a terrestrial
knucklewalking phase in the evolution of human
bipedalism to 4.4 Ma. Equally, in linking terrestrial
bipedalism to arboreality (Lovejoy et al. 2009a,b),
publication of Ar. ramidus has greatly strengthened
the positive case for an arboreal origin for the core
hominin adaptation. In doing so, it challenges us to
develop a convincing arboreal alternative to a terres-
trial knucklewalking model of the origins of human
bipedalism.
While still based on the concept that we should look
for the origins of human bipedalism among activities
of living African apes, the most supported arboreal
challenger for the terrestrial knucklewalking model is
the ‘vertical climbing’ hypothesis of Fleagle et al.
(1981). This was derived primarily from electromyo-
graphic similarities between hip, buttock and thigh
musculature activity of African apes during climbing
on large, vertical supports, and that of humans walking
bipedally. However, the kinematics of vertical climbing
(Isler 2002, 2003; Isler & Thorpe 2003) and knuckle-
walking (Watson et al. 2009) are rather similar,
involving highly flexed postures of the hip and knee
(Crompton et al. 2003), which are quite unlike the
extended postures seen in human walking and which
underlie its efficiency (Alexander 1991). Running
does involve more flexed limb postures, but this is
linked to the use of elastic recoil, as the spring-mass
mechanism requires substantial elastic energy stores.
The most well known of these elastic energy stores, a
marked Achilles tendon, is absent in both the African
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Review. Arboreal origins of hominin bipedalism
apes and the orangutan, which all have large distal
muscle masses (Thorpe et al. 1999; Payne et al.
2006a,b), which help the more powerful forelimbs
(Thorpe et al. 1999; Oishi et al. 2009) in climbing
but probably also act to tune the limbs to deal with
variations in support compliance in an arboreal
context. Interestingly, the gibbons and siamangs do
have a large Achilles tendon: its mechanical role
is currently under investigation in our laboratory
(Channon et al. 2009).
The absence of a medial longitudinal arch (MLA)
in the non-human great apes and its reported absence
in Ar. ramidus (Lovejoy et al. 2009a) appears to rule
out that possible location of the required mass of elas-
tic tissue. So the existence of one or both of the most
likely possible elastic energy stores, a large mass of
plantar soft tissue housed within a MLA (Ker et al.
1987) or a large Achilles tendon, is required to be
demonstrated before a mechanically effective com-
pliant, rather than stiff-legged, gait can reasonably be
posited for early hominins.
While energetic efficiency and mechanical perform-
ance are by no means the only parameters subject to
natural selection (as fieldworkers know better than
most), they are very often directly or indirectly impor-
tant, and can be assessed and predicted relatively
readily. Several laboratories, including our own, have
therefore used computer simulation to assess the effec-
tiveness of alternative gaits in Au. afarensis and other
hominins. Independent studies by at least three separ-
ate laboratories (Crompton et al. 1998; Kramer 1999;
Kramer & Eck 2000; Sellers et al. 2003, 2004, 2005;
Nagano et al. 2005) demonstrate that Au. afarensis
could have been an effective stiff-legged upright
biped, particularly over relatively short distances and
walking unloaded (Wang & Crompton 2004; Wang
et al. 2004). Using forwards dynamic modelling, meta-
bolic cost can be predicted. Predicted costs for human
models have been verified against experimental values
for human adults and come within 10– 15% of these
values. Predicted values for upright walking by
Au. afarensis in independent studies by Sellers et al.
(2004, 2005) and Nagano et al. (2005) are in good
accord and come quite close to the experimental
values for human children of equivalent size. If
Au. afarensis could thus have been an effective stiff-
legged, upright biped, and if moving in a compliant
gait would have incurred both substantial increases
in the mechanical cost of locomotion (Crompton
et al. 1998) and physiological costs including increased
heat load (Carey & Crompton 2005), an origin for
bipedalism in locomotor modes associated with
highly flexed limb postures, such as vertical climbing,
seems unlikely.
A different objection to the vertical climbing model
has recently been raised by DeSilva (2009). He argues
that early hominin ankle joint morphology is distinct
from that of vertical-climbing African apes, and
incompatible with the kinematics required for vertical
climbing. Lovejoy et al. (2009b) argue that anatomical
features of the hand associated with vertical climbing,
such as elongated metacarpals, are absent in
Ar. ramidus, and they follow Thorpe et al. (2007b) in
proposing that both knucklewalking and a strong
Phil. Trans. R. Soc. B (2010)
R. H. Crompton et al. 3303
adaptive commitment to vertical climbing were
acquired independently in panins, after the divergence
from hominins, although Lovejoy et al. (2009b) do not
appear to make a functional link between the two.
Lovejoy et al. (2009a,b,c) identify a number of fea-
tures in which the hands and feet of Ardipithecus
resemble those of the root hominoid Proconsul and
some living arboreal monkeys, rather than living great
apes. These include evidence for short hands with an
extensive dorsiflexion range in the metacarpophalangeal
joints that is absent in living great apes apart from
humans (individuals in some human populations,
such as the Han Chinese can often dorsiflex to more
than 908 when young; personal observation, R. H.
Crompton 1982). Following earlier arguments (Moyà-
Solà et al. 2004) that the presence of the same feature
in the Miocene hominoid Pierolapithecus catalaunicus
suggested that it was an arboreal quadruped, they
suggest, although acknowledging that it is a curious
combination, that while bipedal on the ground (Lovejoy
et al. 2009c), Ar. ramidus was primarily quadrupedal in
the trees (Lovejoy et al. 2009b), while using some ‘care-
ful climbing and bridging’, presumably at the periphery
of trees (Lovejoy et al. 2009b).
The feet of Ar. ramidus, like those of monkeys,
apparently retained a thick plantar layer of fibrous
tissue, and were thus rather stiff when compared
with those of the panins, gorillines and pongines
(Lovejoy et al. 2009a). This implies lesser ability to
conform to branch diameter, and thus relatively poor
grip for what was apparently a large-bodied (50 kg,
Lovejoy et al. 2009c) hominin, nearly twice the mass
of the largest cercopithecine monkey, the mandrill,
and more than 10 kg greater than the largest individ-
uals of the largest monkey, the Sichuan snub-nosed
monkey Rhinopithecus roxellana (Rowe 1996). It is
argued that panins, gorillines and pongines also
acquired their compliant feet independently (Lovejoy
et al. 2009a). With no tail, but equally little pedal
gripping power, as well as short hands, there can
have been little or no capability to exert balancing
counter-torques on the support. Then how did
Ar. ramidus balance their body mass above branches
during pronograde quadrupedalism? Quadrupedal
monkeys, lacking the wide and powerful grasp of the
living non-human great apes, improve stability by
deep flexion of the limbs. Stability in flexion is very
often aided by anteflexion of the olecranon process
in arboreal monkeys (Fleagle 1998), but there is
apparently no evidence of anteflexion of the olecranon
in the Ardipithecus proximal ulnae (Lovejoy et al.
2009b). Further, habitual deep flexion of the limbs
as an arboreal quadruped would increase mismatch
(in the power capacity of muscles at different joint
angles) between the requirements of terrestrial
bipedalism and those of arboreal quadrupedalism.
3. THE ARBOREAL ORIGINS OF BIPEDALISM:
COMPRESSIVE ORTHOGRADY?
A more parsimonious explanation of the metacarpo-
phalangeal dorsiflexion seen in Ar. ramidus is surely
desirable. It exists, in part, in consideration of
elements of arboreal behaviour of all the great apes,
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3304 R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism
namely in the use of arboreal hand-assisted bipedal-
ism, or if preferred, compressive orthogrady, both
postural and locomotor, to move around the forest
canopy. Again, in part, the explanation is to be
found in consideration of the similarity, in shared
lack of digital elongation and in morphological con-
servatism, between the human hand and that of
Ar. ramidus, demonstrated by Lovejoy et al. (2009a).
Together with the suggestion of Thorpe et al.
(2007b) that vertical climbing and knucklewalking
were both acquired independently in panins (after the
separation from hominins) and in gorillins, and its con-
firmation by the description of Ar. ramidus (Lovejoy
et al. 2009b,c), there is increasing evidence (e.g.
Larson 1998) that suspensory adaptations did not
evolve at the same time as other features of orthogrady,
but rather homoplastically. While it is difficult to obtain
definitive figures from all studies and for all species,
table 1 shows that, together, terrestrial knucklewalking
quadrupedalism, vertical climbing and forelimb suspen-
sion make up some 67 per cent of bonobo locomotion,
93 per cent of common chimpanzee locomotion and 97
per cent of mountain gorilla locomotion, but only 39
per cent of orangutan locomotion. A figure for lowland
gorilla knucklewalking versus non-knucklewalking
quadrupedalism is more difficult to determine, but
based on proportions of arboreal and terrestrial activity,
we have assigned a tentative figure which allows a total
proportion of novel locomotor modes in the repertoire
to be set pro tempore at 62 per cent. Thus, from the
reported evidence of Ardipithecus, the great majority of
the panin and gorilline locomotor repertoire employs
novel adaptations since the divergence from hominins.
This observation has significance for both palaeontolo-
gists and fieldworkers, and underlines Darwin’s (1871)
warning, with which we began this paper, that we
should not expect the common ancestor to resemble
either humans or living apes particularly closely.
This suggests that what is now the relatively small
compressive component of great ape orthograde loco-
motion may be the oldest, and human locomotion thus
relatively conservative. (Whether compressive ortho-
grady is as old as orthogrady itself, or whether
orthograde body posture arose earlier from a random
homeotic event (Filler 2007), we currently have no
way of knowing). Importantly however, this behaviour
offers a reasonable alternative for locomotion in a
species not yet in possession of vertical climbing and
suspensory adaptations. We suggest that in an arboreal
context, hominin species such as Ar. ramidus (as well
as ourselves) which do not have elongated hands,
powerful in suspension, may tend more often to
climb upwards (which they must have done relatively
frequently if they were exploiting both terrestrial and
arboreal niches) by pushing themselves up by pressure
of the hands below shoulder level, so that the ulnar
four metacarpophalangeal joints pass into deep dorsi-
flexion. This adds much of the length of the
metacarpals to the potential lift. This is of course
exactly how humans usually climb large-trunked
trees when they lack climbing equipment to help
them move on the main trunk, with the human lack
of ‘vertical climbing’ adaptations (primarily very
powerful arms; see Thorpe et al. 1999; Payne et al.
Phil. Trans. R. Soc. B (2010)
2006a,b; Oishi et al. 2009): we climb up bough by
bough, further out in the tree. In the absence of climb-
ing aids, humans find it difficult and of course
dangerous (Pontzer & Wrangham 2004) to climb up
trees where long, naked trunks occur before any side
branches. Gorillas and chimpanzees are readily able
to do so, using the vertical climbing adaptations,
which Ardipithecus suggests (Lovejoy et al. 2009a,b,c)
arose independently and in parallel in the two lineages.
Similarly, hand-assisted compressive orthogrady has
been shown to allow orangutans to move on very flex-
ible branches at the periphery of tree crowns where the
most abundant supply of fruit is generally situated
(Thorpe et al. 2007b) and it may play a similar role
in the behaviour of lowland gorillas (see table 11 in
Remis 1994). Analogy with the largest cercopithecine,
the mandrill (Lahm 1986), less than 27 kg, and con-
sideration of the behaviour of the largest of all
monkeys, Sichuan snub-nosed monkeys Rhinopithecus
roxellana (Kirkpatrick et al. 1999; Li 2001; Li et al.
2002), less than 37 kg, suggests that the 50 kg body
weight claimed for Ar. ramidus (Lovejoy et al. 2009c)
may exceed mass limits of effective monkey-like
arboreal plantigrade quadrupedalism. However, com-
pressive orthogrady is exhibited by similar-sized apes
and could facilitate both access into trees and move-
ment within them. Further, Miocene crown-
hominoid body weight begins above that of mandrills,
and equals or exceeds that of R. roxellana: 30 – 54 kg
for Morotopithecus (MacLatchy et al. 2000), 30 kg for
Pierolapithecus (Culotta 2004; Moyà-Solà et al. 2004),
30– 37 kg for Hispanopithecus (Moyà-Solà & Köhler
1996) and 32 kg for Oreopithecus (Köhler & Moyà-
Solà 1997). We suggest that it is unlikely that the
consistently larger size of Miocene crown hominoids
was not accompanied by a shift from monkey-like
arboreal locomotion.
Thus, we argue that a hominin which had not
acquired suspensory/vertical climbing features in the
forelimb would have accessed the trees and moved
within them primarily by palmigrade compressive
orthogrady. In the absence of vertical climbing capa-
bilities and a powerful hand grip, access to trees
would of course favour use of more stable supports,
which can be loaded under compression without
excessive deflection. In the absence of suspensory fea-
tures, hand-assisted bipedalism could have facilitated
movement among the finer supports at the periphery
of trees, employing strategies similar to those we
have reported in the orangutan (Thorpe et al. 2007b,
2009). Quadrupedalism would be used when absol-
utely necessary—as of course it is by ourselves when
we no longer trust our balance or stability—but palmi-
grade hand postures would be inappropriate among
finer supports. Many anthropoids are able to employ
some degree of suspension, vertical climbing and
quadrupedalism regardless of their primary adap-
tation, although perhaps rarely, and at some
additional cost, so suspension is also likely to have
been used under certain conditions. It may be
argued that this is referential modelling (Sayers &
Lovejoy 2008): but at least we are using multiple refer-
ents, and we are able to test the predictions of our
models by simulation. We predict, for example, that
Phil. Trans. R. Soc. B (2010)
Table 1. Frequencies of locomotor behaviour in the great apes and ‘ballpark estimates’ of the per cent of their locomotion that has evolved since divergence from their last common ape
ancestora.

knucklewalk/run other quadrupedal vertical orthograde pronograde % loco evolved

(terrestrial and arboreal) (terrestrial and arboreal) climb/descent brachiate clamber/transfer bipedal leap scramble otherb since separationc

mountain 95 ,1 ,1 0.1 0 0.8 0 .0 0 97

gorilla d,e
lowland 38.5 26.7 19.7 3.6 3.3 6.1 0 0 1.3 62
gorillad,f
chimpanzeed,g 86.1 4.5 6.5 0.8 0.5 0.7 0.2 0.3 0.1 93
bonobod,h 7.8 27.5 50.4 8.9 0 1.5 3.1 0 0 67
orangutani 0 8 26 13 22 7 ,1 9 11 39
a
Note that all values are ballpark figures as differences in methodology and subject profiles preclude detailed comparison.
b
For example, tree sway, pronograde suspension.
c
This value assumes that the common ancestor at all levels was a monkey-like above branch quadruped. The value includes knucklewalking, vertical climb/descent, brachiation and orthograde clamber/
transfer.
d
Modified after Hunt (2004) and based on data from Tuttle & Watts (1985), Doran (1996), Hunt (1992) and Remis (1995).
e
Adapted from Tuttle & Watts (1985).
f
Knucklewalking/non-knucklewalking values are not available for lowland gorillas at present. However, 59% of their time is spent terrestrially and 41% arboreally (adapted from Hunt 1996). Consequently, as
a rough estimate, we have allocated 51% of quadrupedalism to be terrestrial knucklewalking and the remainder to be arboreal non-knucklewalking quadrupedalism.
g
Adapted from Hunt (1992) following personal communication (K. D. Hunt, 2009).
h
Bonobos are more arboreal than chimpanzees but no conclusive data exist, neither for the per cent of time they are arboreal nor for how much of their quadrupedalism is knucklewalking. However, Susman
Review. Arboreal origins of hominin bipedalism

(1984) observed that of 532 bouts of arboreal quadrupedalism, only 20 (3.8%) were knucklewalking and of Susman’s (1984) 89 first sightings of bonobos, 17 (19%) were terrestrial. Thus, we have weighted
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Doran’s (1996) frequency data with these values to calculate proportions for knucklewalking and non-knucklewalking quadrupedalism.
i
Modified from Thorpe & Crompton (2006).
R. H. Crompton et al.
3305
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3306 R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism
a dynamic model of quadrupedalism in Ardipithecus
would show that quadrupedalism would be possible,
if unstable, and very expensive, if perhaps less so
than it would be for longer-legged humans.
A parallel case has very recently been discussed in
the literature. Pierolapithecus is described by Almécija
et al. (2009) as orthograde, but as lacking the obvious
suspensory adaptations seen in the rather later Iberian
crown hominoid, Hispanopithecus (D.) laietanus. The
metacarpophalangeal joints are described as adapted
for use in dorsiflexion in palmigrade postures
(Almécija et al. 2009). Reference to monkeys would
suggest that it was an arboreal quadruped (Moyà-
Solà et al. 2004), but these authors now regard it as
orthograde in body plan (Almécija et al. 2009) but
moving by palmigrade quadrupedalism. The authors
also suggest that the description of the Miocene pon-
gine Sivapithecus by Madar et al. (2002) may suggest
similar behaviour. It is very difficult to reconcile an
orthograde body plan with quadrupedal locomotion,
even when there are no claims that Pierolapithecus
was a terrestrial biped. The obvious, simple solution
is again the one we propose here, that it (and perhaps
even Sivapithecus) was an orthograde clamberer which,
in the absence of marked suspensory adaptations, used
hand-compressive climbing techniques below shoulder
level, in other words, hand-assisted bipedalism and
other components of the compressive-orthogrady
continuum best exemplified today in orangutans.
4. THE LEGACY OF ARBOREAL ORIGINS FOR
HUMAN BIPEDALITY
The arboreal habitat differs markedly in one major
mechanical respect from the terrestrial: it is compliant
(Alexander 2003) and thus unstable, as it can be set
vibrating by imposed forces. Arboreal mammals need
to have strategies for dealing with this compliance.
Schmitt (1999) has shown that limb flexion (limb
compliance) is one such response, but limb flexion
requires muscle power to maintain stable flexed pos-
tures. For this reason, most probably, muscle masses
tend to be higher in arboreal animals (Degabriele &
Dawson 1979), while terrestrial cursor limbs have
short muscle bellies and long tendons (Alexander
2003). To what extent has this legacy of compliance
influenced early hominin evolution?
(a) A compliant foot?
Lovejoy et al. (2009a) argue that whereas the living
non-human great apes have acquired compliant feet,
to enable them to grip branches more effectively, and
humans have of course acquired a MLA, Ardipithecus
is again conservative in the plantar foot, lacking a
MLA, but retaining a thick and fibrous layer on the
plantar aspect of the foot, like that of cercopithecines,
contrasting with the loss of such a thick aponeurotic
layer in the non-human apes, which gain thereby in
foot adaptability to irregular substrates.
Following Bojsen-Møller (1979), it is common in
the hominin palaeontology literature (e.g. Lewis
1980; Berillon 2000; Harcourt-Smith & Aiello 2004;
Jungers et al. 2009) to assess the presence or absence
of a MLA by the degree of development and
Phil. Trans. R. Soc. B (2010)
asymmetry of the cuboid peg for the calcaneus
(figure 1a), and Lovejoy et al. (2009a) appear to
follow this practice. The asymmetry and size of the
cuboid peg is not, however, entirely a reliable guide
to the existence or absence of a functional MLA: as
can be seen in figure 1a, the peg is not overlapped ven-
trally by the calcaneus. While it is usual to associate
this development with loss of the mid-tarsal break
(axis of plantarflexion), which is present in other
living apes (Lewis 1980), the absence of a mid-tarsal
break is not universal in humans. Setting aside con-
ditions such as Charcot foot, where soft-tissue failure
arising from diabetes or directly from neurological
conditions results in collapse of the lateral midfoot
and in some cases a midfoot pressure peak under, or
near, the calcaneocuboid joint, figure 1b (unfortu-
nately from uncalibrated pressure plate data, but
qualitatively reliable) shows that clinically normal indi-
viduals may also show a lateral midfoot pressure peak.
It is interesting that this individual also shows absence
of a lateral-to-medial path of the centre of pressure
and, in figure 1c, a single-peaked vGRF, with a non-
human-ape-like slow tailing-off of vGRF at ‘toe-off ’.
While the absence of the mid-tarsal break does seem
functionally linked with an extended toe-off, neither
are therefore universal features of hominins. Neverthe-
less, if Ardipithecus lacked a human-like cuboid peg,
lateral-foot stability would be limited. In both cases,
a certain degree of rigidity provided by retention of a
thick plantar fibrous layer would improve the capacity
of the lateral metatarsals to deliver accelerative force
from a more effective, relatively anterior, position.
We (Pataky et al. 2008) recently demonstrated a
negative correlation of plantar pressure with walking
speed in humans, which implies reduced collapse of
the MLA, and thus increased stiffness. This may be
directly beneficial to force transmission to the ground.
It is also important in enabling control of gear ratios,
and thus in tuning muscles to enhance performance
during constant-speed running by applying pre-tension
during landing, while optimizing them also for effi-
ciency or power at toe-off (Carrier et al. 1994).
Perhaps most importantly, we can optimize muscle
properties during rapid changes in speed and changes
in incline in both running and walking (Lichtwark &
Wilson 2006, 2007, 2008). We have suggested that
increased stiffness results from pre-tension applied to
the plantar aponeurosis (PA) by heel-strike or early-
stance muscle activity (in triceps, tibialis anterior and
the digital dorsiflexors; Pataky et al. 2008; Caravaggi
et al. 2009). The windlass mechanism created as the
PA wraps round the heads of the metatarsals
(figure 1a) is known to contribute to stiffen the foot
in late stance (Hicks 1954) by pulling on the calcaneus,
causing inversion of the subtalar joint and hence ‘lock-
ing’ the midtarsal joint (Tansey & Briggs 2001). A
dynamic model of the plantar foot constructed in our
laboratory (Caravaggi et al. 2009) however shows that
the PA is also pre-tensioned in early stance, from
heel-strike onwards, as proposed by Pataky et al.
(2008), and the tension appears to increase with walk-
ing speed. The predicted tension (verified against
cadaveric data from Gefen (2003)) increases from lat-
eral to medial, and ranges from 0.47 body weight at
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Review. Arboreal origins of hominin bipedalism R. H. Crompton et al. 3307

(a) (b)

metatarsal heads

spring
ligament
talonavicular
joint, with cuboid peg
calcaneocuboid
joint forms calcaneocuboid
‘midtarsal’ or joint
transverse tarsal
joint the 5 slips of the
head of the plantar
talus aponeurosis

(c) 1600
1400
1200
1000
force (N)

800
600
400
200
0
0 50 100 150 200 250 300
time (ms)

Figure 1. (a) Diagram of the plantar aspect of the human foot, showing the position of the cuboid peg and illustrating the
‘windlass mechanism’, whereby the five slips of the PA are tensed by the curvature of the metatarsal heads as the metatarso-
phalangeal joint dorsiflexes. Similarly, the spring ligament is tensed by plantad motion of the head of the talus. Both
mechanisms act to stiffen the median longitudinal arch during stance. (Figure modified from image from Primal’s ‘Anatomy
TV’). (b) Peak pressures, in false greyscale, where lighter tone indicates higher pressure, during bipedalism of a clinically
normal subject recorded by Nike Inc., courtesy of J.-P. Wilssens of RSscan International. Dots indicate the path of the
centre of pressure under the foot. (c) vGRF curve calculated from the same data for the individual featured in (a).

heel-strike to a peak 1.5 BW, generating vertical forces
which sustain the MLA and metatarsals. Thus, the
MLA is supported through much of stance by soft
tissue: stiffening of the PA, as well as bone shape, con-
tributes directly and very substantially to the existence
of the MLA. An assumption that lack of a human-like
cuboid peg (figure 1a) implies lack of a MLA is
unsafe without extensive investigation of the possibility
of soft-tissue stiffening. The case of human individuals
with a mid-tarsal break suggests that sustained vGRFs
and a substantial hallucal toe-off depend on stiffening
of both the medial and lateral foot by soft-tissue ten-
sioning throughout stance.
It is notable that Vereecke et al. (2003) have shown
that foot pressure records of human bipedalism are
much less variable between strides and between indi-
viduals than those of the bipedalism of other
hominoids. In humans, forces are applied in a more
consistent manner, particularly by the hallux, which
plays a limited propulsive role in most non-human
apes, and may act more as a balancing structure
during bipedalism. If the hallux of Ardipithecus is as
Phil. Trans. R. Soc. B (2010)
abducted as Lovejoy et al. (2009a) report, the degree
of abduction is comparable to that in living gibbons
(e.g. Vereecke et al. 2005; Crompton et al. 2008)
and perhaps Oreopithecus. While Moyà-Solà et al.
(1999) suggested that the extent of hallucal abduction
in Oreopithecus would not have been compatible with
other than postural bipedalism, Vereecke et al.
(2006a,b) have shown that gibbons, despite compliant
feet with widely abducted halluces, can sustain run-
ning on the ground for some hundred yards and
attain absolute speeds equalling the human walk–run
transition. Neither do compliant feet prevent the
non-human great apes from walking bipedally, terrest-
rially or arboreally. High robusticity of metatarsals two
and three is also a feature of Ar. ramidus (Lovejoy et al.
2009a) and suggests that these digits may have been
more important in applying accelerative parasagittal
force than the hallux, while the abducted hallux pro-
vided grip on branches. However, even in human
bipedal walking, plantar pressure tends to be lower
under the hallux, and greater under metatarsal heads
two and three, in flat-footed humans or humans who
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3308 R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

(a) 1.4 (b)

1.2

1.0

hindlimb length (m)

forelimb length (m)

0.8

0.6

0.4

0.2

(c) 1.5 (d)

hindlimb moment of inertia (kg m2)

forelimb moment of inertia (kg m2)

1.0

0.5

0
Gorilla Pan Pongo Hylobates Homo Equus Gorilla Pan Pongo Hylobates Homo Equus
Figure 2. (a,b) Chart showing the limb lengths and (c,d) moments of inertia for hominoids and horse. Forelimb moments of
inertia are about the shoulder joint and hindlimb moments of inertia are about the hip joint. Great ape data are from Isler et al.
(2006), human data are from Winter (1990) using a median male height and weight from the GEBOD database (Cheng et al.
1994), horse data from Buchner et al. (1997).

have been brought up as barefoot walkers (D’Août dedicated terrestrial cursor (horse). All dimensions
et al. 2009). have been geometrically scaled to the estimated mass
Thus, the human foot is less distinct than is often of Ar. ramidus, 50 kg, using mass1/3 for lengths and
thought from that of other great apes. It has built on mass5/3 for moments of inertia. All the arboreal species
the compliant arboreal legacy (whether prior to or have longer than expected forelimbs, but, except for
after the separation from panins we submit is not yet humans and gibbons, hindlimb length is not greatly
clear, given the mixed message of Ardipithecus; Lovejoy different from that of the specialist cursor. However,
et al. 2009a) by becoming a variable-gear organ, able when looking at the moments of inertia it can clearly
to change its stiffness to accommodate to speed, as be seen how elongated limbs with heavy autopodia
well as to support compliance and irregularity. lead to extremely large moments of inertia when
compared with the values seen in horses. This has
inevitable but complex effects in terms of top speed
(b) Limb mass proportions and efficiency. Long, high-inertia legs are perfectly
Another likely legacy from a recently arboreal past is efficient for the pendular mechanics of slow walking,
the partial retention of arboreal limb mass pro- but the high-speed spring mechanics of running require
portions. A cursorial animal needs to accelerate its low moments of inertia to minimize the internal energy
limbs rapidly. Rapid acceleration can be achieved lost per step. Hylobates seems to some extent to have
with less energy if the moments of inertia are reduced, dealt with the inertial problem of very long legs by redu-
and this is commonly achieved by a reduction in distal cing distal muscle mass. We suggest, following
limb elements (Hildebrand 1995). Figure 2 shows Channon et al. (2009), that several aspects of gibbon
a comparison of the inertial properties and limb anatomy may relate to an unrecognized importance of
dimensions of hominoids in comparison with a leaping in the gibbon locomotor repertoire.
Phil. Trans. R. Soc. B (2010)
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Review. Arboreal origins of hominin bipedalism R. H. Crompton et al. 3309

However, upper limb – lower limb proportions and 10

the distribution of lengths and mass within limbs
also affect their swing frequency. Part of the efficiency
of long distance human walking at least depends on a
forward swing of the contralateral arm to counteract
the horizontal torque applied to the body by the

tendon mass fraction (%)

swing leg (e.g. Li et al. 2001) which, among other 1
effects, interferes with lateral stability. These swings
occur even in short-distance walking of young children
of similar stature/mass to Au. afarensis, and increase in
magnitude with walking speed (Li et al. 2001), so they
are of relevance to any consideration of early hominin
locomotion. Match between the natural pendular 10−1
period (NPP), and hence swing-time of upper and
lower limbs, affects efficiency of all gaits, bipedal and
quadrupedal; and distribution of mass within the
limb affects the NPP (Isler et al. 2006). The distal pos-
ition of the centre of mass of the forelimb of most great
apes, with the exception of the chimpanzee, means 10−2
that there is a considerable mismatch with forelimb

ee

la

on

an

er

re

d
ta

un
ril

de

ha
nz

m
bb
NPP, and segment proportions are thus not well opti-

gu

ho
go

hu

in
pa

gi
an

re

ey
im
mized for quadrupedal gaits (Isler et al. 2006).

or

Chimpanzees may have modified their limb mass dis-
tribution for more efficient quadrupedalism,
suggesting that the last common African ape ancestor
was not a proficient quadruped (Isler et al. 2006).
However, experimental work on the oxygen consump-
tion of both bipedal and quadrupedal locomotion in
chimpanzees confirms that they are relatively ineffi-
cient in both modalities (Sockol et al. 2007),
compared with both modern humans and quadrupeds
of equivalent body size. This may indicate that maxi-
mum terrestrial speed, rather than minimal terrestrial
energy cost, may be the target of selective pressure
for chimpanzees. (By contrast, preliminary data from
the same research group suggest that metabolic costs
of bipedalism in the orangutan are some of the
lowest recorded locomotor costs for the body size;
personal communication from H. Pontzer (2009)).
(c) Proportion of mass as tendon
Another area where there is still a considerable legacy
from the recent arboreal past is in the amount of
tendon in the hindlimbs of hominoids compared
with cursorial animals. Figure 3 shows the mass of
hindlimb tendon in both hindlimbs as a proportion
of body mass. This parameter is informative since its
biomechanical interpretation is independent of
moment arm data, of which there is very little available
for comparison in non-primates. Tendon acts as a
simple damped spring during locomotion, so the
amount of energy that can be stored depends on the
mass. The strain energy storage of tendon is
2500 J kg21 at 8 per cent strain (Vogel 2003), which
is therefore the limit of the amount of elastic strain
energy that is potentially available per gait cycle—
whether for power amplification or energy saving.
For the hominoids, tendon mass was estimated using
published tendon length and muscle physiological
cross-section area data. Tendon cross-section area
was estimated by assuming 6 per cent strain at maxi-
mal isometric contractile force and muscle
contraction stress of 300 kN m22 (Sellers & Manning
Phil. Trans. R. Soc. B (2010)
gr
ch
Figure 3. Total tendon in both hind limbs as a fraction of body
mass. Data are based on information from Pierrynowski
(1995), Payne et al. (2006), Williams et al. (2007, 2008) and
Wareing et al. (submitted).
2007). Resulting volumes were converted to tendon
mass using a density of 1100 kg m23 (Watson &
Wilson 2007). It is clear that tendon mass is highly
variable and more often related to high speed and
high acceleration than to efficiency. It is also clear
that while humans have appreciably increased their
hindlimb tendon proportion when compared with
the other apes, they are still a long way from the
much higher proportions in more specialized cursorial
quadrupeds—particularly those specializing in explo-
sive acceleration rather than long-distance efficiency.
This is emphasized if we multiply through by
2500 J kg21 to express elastic storage capacity in
terms of energy. Most hominoids have about 1 J kg21
of elastic energy storage, humans nearly three times
that, reindeer 10 J kg21 but greyhounds fully
100 J kg21. Thus, while humans have adjusted
tendon mass somewhat to enhance terrestrial running,
perhaps retaining a relatively large muscle mass to
allow for adjustments to optimize the hindlimb for ter-
rain, speed and support characteristics, the African
apes have not. Bonobos and lowland gorillas may not
require to do so because of limited terrestriality;
mountain gorillas may be protected by size, but chim-
panzees may simply have modified mass proportions to
match hindlimb – forelimb swing frequencies better,
suggesting that the selective pressures associated with
movement in an unstable arboreal milieu remain
strong.
We can further investigate the role of elasticity in
human locomotion by simulation. In recent simulation
work (Sellers et al. 2010), the role of tendon elasticity
was quantified by ‘virtual ablation’. In this paradigm,
simulations are repeated with identical anatomical
models except for the structure of interest, which is
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

3310 R. H. Crompton et al. Review. Arboreal origins of hominin bipedalism

(a) 6 expectations from body size but also to Ar. ramidus’

velocity (m s−1) 5 clear adaptations for one form of compressive ortho-
4 grady, terrestrial bipedal walking.
3 Secondly, we argue that from our arboreal ancestors
2 humans have inherited feet and legs that can adapt to a
1
large variety of terrains, support compliances and
0
speeds. However, at some stage in our evolution we
(b) have departed some way from other hominoids in
4.0
net cost of locomotion

3.5 adaptation for energy-efficient running. This combi-

3.0 nation probably has a lot to do with our ability to
(J kg−1m−1)

2.5
2.0 outrun horses in trials such as those over 22 miles of
1.5 hilly mid-Wales or 50 miles of sand-dunes in the
1.0
0.5 United Arab Emirates. But we are not fast runners
0 (see Bramble & Lieberman 2004), and in terms of
energy storage have a very long way to go to catch
s

T
s
on

on

A
nd

nd

up with dogs bred for hunting. Early human ancestors

ff

al
sti

rm
te

te

would clearly have been no match for a cursorial

al

ff

no
nd
sti
rm

sa

nd

predator, so that it is perhaps fortunate that along

no

on

sa
nd

on

with late retention of long forearms (Dunsworth

te

nd
al

et al. 2003), which would improve throwing distance

te
rm

ff
no

sti

if not accuracy, part of our arboreal inheritance was

Figure 4. (a) Chart showing the maximum velocity and (b)
the cost of locomotion of human running simulations
where the elastic properties of the hindlimb tendons are
manipulated. AT, Achilles tendon. (Sellers et al. 2010).
removed or altered in some versions of the model. This
allows the effect of a specific structure to be isolated in
much the same way as classical ablation experiments
but without the danger of side effects (let alone ethical
difficulties) associated with performing such exper-
iments surgically. In this case, the elastic effect of
tendons was removed by making them 100 times
their normal stiffness, so that the simulated tendons
were unable to store appreciable amounts of energy
in the simulation. Four experimental conditions were
compared: normal hindlimb tendons; all hindlimb ten-
dons stiff; all normal hindlimb tendons except for a
stiff Achilles tendon; all tendons stiff except for a
normal Achilles tendon. Figure 4 shows that for
humans, the presence of tendon has only a moderate
effect on the maximum running speed of the simu-
lation but a very marked effect on the net cost of
locomotion, and that this effect was mostly produced
by the Achilles tendon. This confirms the critical
role in efficient, high-performance running of a sub-
stantial Achilles tendon, which is missing from all
hominoids except humans, gibbons and siamangs.
Whether such a structure is present in fossil hominins
(and which) is currently unknown but evidence of its
presence, perhaps by analysis of calcaneal microstruc-
ture, would probably be diagnostic of running ability.
5. CONCLUSIONS
We argue that, given the large body mass of Ar. rami-
dus, typical of both living and extinct hominoids, it is
more likely that when it moved in the trees it made
use of compressive orthogrady, which we suggest
may be the oldest crown-hominoid locomotor adap-
tation, than that it adopted a monkey-like
quadrupedalism. This would run counter not only to
powerful leg muscles, which remain very helpful for
climbing trees!
R.H.C. thanks Alan Walker and Chris Stringer for the
invitation to participate in this meeting. We thank the
Royal Society, the Leverhulme Trust and the Natural
Environment Research Council, the Biotechnology and
Biological Sciences Research Council and the Engineering
and Physical Sciences Research Council for supporting our
research, and Chester and Twycross Zoos for permission to
study the hominoids under their care. R.H.C. and W.I.S.
also thank the NorthWest Grid and the Science and
Technology Facilities Council Daresbury Laboratory for
access to high-performance computing facilities.
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Phil. Trans. R. Soc. B (2010) 365, 3315–3321

doi:10.1098/rstb.2010.0069

Two new Mio-Pliocene Chadian hominids

enlighten Charles Darwin’s 1871 prediction
Michel Brunet1,2, *
1
Collège de France, Chaire de Paléontologie Humaine, F75231 Paris Cedex 05, France
2
Institut International de Paléoprimatologie et Paléontologie Humaine, IPHEP UMR 6046
CNRS/Université de Poitiers, F86022 Poitiers Cedex, France
The idea of an evolutionary sequence for humans is quite recent. Over the last 150 years, we have
discovered unexpected ancestors, numerous close relatives and our deep evolutionary roots
in Africa. In the last decade, three Late Miocene hominids have been described, two about 6 Ma
(Ardipithecus and Orrorin) in East Africa and the third dated to about 7 Ma (Sahelanthropus) in
Central Africa. The specimens are too few to propose definite relationship to other species, but
clearly these belong to a new evolutive grade distinct from Australopithecus and Homo. Moreover,
all of them were probably habitual bipeds and lived in woodlands, thus falsifying the savannah
hypothesis of human origins. In light of all this recent knowledge, Charles Darwin predicted
correctly in 1871 that Africa is the birthplace of humans, chimpanzees and our close relatives.
Keywords: earliest hominids; central Africa; evolutionary grade; woodland origin

1. INTRODUCTION temporally close to the last common ancestor of chim-

Who our ancestors were, and when and how they
arose, are questions that are always topical.
The notion of fossil humans is quite recent: the first
Neanderthal specimen from the Neander Valley of
Germany was first described only in 1856 (Fuhlrott
1859, 1865) and Darwin’s masterpiece ‘On the
Origin of Species’ only published in the middle of the
nineteenth century (Darwin 1859).
By the 1980s early hominids were known just from
south and east Africa (figure 1).
But from 1994 in the Djurab desert of Northern
Chad the M.P.F.T.1 unearthed successively a new aus-
tralopithecine dated to 3.5 Ma (Brunet et al. 1995;
Lebatard et al. 2008), Australopithecus bahrelghazali
(Brunet et al. 1996; figure 2), the first ever found
west of the Rift Valley; and a new hominid, Sahelan-
thropus tchadensis (Brunet et al. 2002a,b), from the
Late Miocene (figures 3 – 6), dated to 7 Ma (Vignaud
et al. 2002; Lebatard et al. 2008). This earliest
known hominid is a new milestone suggesting that an
exclusively southern or eastern African distribution
of the early hominids is unlikely to be correct.
And so in the last 15 years our roots have been
shown to be deeper, from the Lower Pliocene
(4.4 Ma) to the Late Miocene (7 Ma), with three new
species: Ardipithecus kadabba (Haile-Selassie 2001;
Haile-Selassie & Woldegabriel 2009; 5.2–5.8 Ma,
Middle Awash, Ethiopia), Orrorin tugenensis (Senut
et al. 2001; ca 6 Ma, Lukeino, Kenya) and, the earliest
one, S. tchadensis (Brunet et al. 2002a,b; 7 Ma, Chad).
Sahelanthropus tchadensis (figures 3– 6) displays a
unique combination of plesiomorphic and apomorphic
characters that clearly illustrate its hominid affinities
*michel.brunet@college-de-france.fr, michel.brunet@univ-poitiers.fr
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3315
panzees and humans, and also that it cannot be related
to chimpanzees or gorillas (Brunet et al. 2002a,b,
2004, 2005; Vignaud et al. 2002; Guy et al. 2005;
Zollikofer et al. 2005; Brunet 2006, 2009a,b; Lebatard
et al. 2008). In Chad, the Late Miocene sedimentolo-
gical and palaeobiological data are consistent with
mosaic landscapes probably very similar to the present
Okavango Delta (Central Kalahari, Bostwana; Brunet
et al. 2005). As with the other Late Miocene hominids,
S. tchadensis represents a new evolutionary grade
(Brunet 2009b), surely a habitual biped with its
usual habitat probably a wooded one.
So, now, it is completely clear that the earliest homi-
nids are not dependent on savannah and were not
living just in south and east Africa.
Accordingly, this early hominid history enlightens the
Charles Darwin prediction of 1871 (Darwin 1871) and
must be reconsidered from a completely new viewpoint.
2. A NEW STORY . . . WEST OF THE RIFT VALLEY
In the 1980s, the distribution of hominid remains in
Africa, with the earliest being in east Africa (Ethiopia
and Tanzania) (figure 1), led Coppens (1983) to pro-
pose an ‘East Side Story’ scenario in which early
hominids appeared and evolved in the Pliocene pri-
mary savannah east of the Rift Valley, while the
tropical forest, west of the Rift Valley, was thought to
represent the early African ape habitat.
In 1994, I received a research permit from the
Chadian authorities to conduct geological and
palaeontological survey in the Djurab desert of north-
ern Chad. With the M.P.F.T., one year later ( January
1995), at a site east of Koro-Toro, we found a
Lower Pliocene vertebrate fauna with a partial lower
jaw belonging to a new australopithecine that we
nicknamed ‘Abel’, the first ever found west of the
This journal is q 2010 The Royal Society
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3316 M. Brunet Chadian hominids and Darwin’s prediction

LIBYA

NIGER Toumaï 25 Abel

24

CHAD SUDAN
Lucy 23
NIGERIA ETHIOPIA 22
21
CENTRAL 20
19 18
CAMEROON AFRICAN REPUBLIC
16 17
14 15
13 12
11 KENYA
10
89
TANZANIA
7

45 6
SOUTH 32
AFRICA 1

Figure 1. Map of Africa showing the main Mio-Pliocene hominid localities. 1, Taung; 2, Drimolen; 3, Sterkfontein; 4, Swartk-
rans, 5, Kromdraai; 6, Makapansgat; 7, Malema; 8, Laetoli; 9, Olduvai; 10, Peninj; 11, Lukeino; 12, Chesowanja;
13, Lothagam; 14, Kanapoi; 15, Chemeron; 16, W. Turkana; 17, Koobi Fora; 18, Allia Bay; 19, Omo; 20, Konso; 21, Maka;
22, Aramis; 23, Hadar; 24, Koro-Toro; 25, Toros-Menalla.

Rift Valley (Brunet et al. 1995). We named it

A. bahrelghazali (Brunet et al. 1996; figure 2).
Other australopithecine sites have been discovered
in the Koro-Toro area since 1995 (Brunet et al.
1997), all having the same fauna with mammals
(proboscidians, suids, rhinocerotids and equids) indi-
cating a biochronological age of 3.5 Ma, congruent
with more recent 10beryllium cosmonuclid dating
(Lebatard et al. 2008).
Geological and palaeontological survey in the
Djurab desert from 1994 to 1997 yielded three new fos-
siliferous areas, biochronologically dated to: (i) the
Early Pliocene (4–4.5 Ma), at Kollé (Brunet et al.
1998); (ii) the Mio-Pliocene boundary (5–5.5 Ma), at
Kossoum Bougoudi (Brunet et al. 2000); and (iii) the Figure 2. Mandible holotype specimen (KT12-95-H1) of
Late Miocene (ca 7 Ma), at Toros-Menalla (TM) A. bahrelghazali (Brunet et al. 1996).
(Brunet et al. 2002a,b). To date, more than 500 fossili-
ferous localities have been discovered in the Djurab In 2001, the M.P.F.T. unearthed a new hominid,
desert, representing upto now around 20 000 vertebrate S. tchadensis (Brunet et al. 2002a,b), from the locality
(mammals, reptiles, birds and fish) specimens. TM 266. The holotype cranium (figure 3), nicknamed

Phil. Trans. R. Soc. B (2010)

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Chadian hominids and Darwin’s prediction M. Brunet 3317

Figure 5. Stereolithocast of the S. tchadensis cranium, three-

Figure 3. Cranium holotype specimen (TM 266-01-060-1) dimensional reconstruction. Scale bar, 1 cm.
of S. tchadensis (Brunet et al. 2002a,b). Scale bar, 1 cm.

Figure 4. Right lower jaw paratype specimen (TM 266-02-

154-1) of S. tchadensis. Scale bar, 1 cm.

‘Toumaı̈’, is associated with a fauna (more than 70

species) of which the mammalian component indicates
a biochronological age estimate congruent with the
10
beryllium dating, close to 7 Ma (Vignaud et al.
2002; Lebatard et al. 2008). This earliest known
hominid, S. tchadensis, unearthed at least 2600 km
west of the Rift valley, is a new milestone suggesting
that an exclusively eastern or southern African origin
of the hominid clade is unlikely to be correct.
The discovery of S. tchadensis occurred in a particu- Figure 6. Illustration of the Toumaı̈ head.
lar scientific context. With three new Late Miocene
species, Ar. kadabba (5.2 – 5.8 Ma, Ethiopia), Or.
show original associations of characters and morpho-
tugenensis (ca 6 Ma, Kenya) and S. tchadensis
types that lead us to revise our definitions of the
(ca 7 Ma, Chad), our roots went deeper, from
Hominidae per se. In fact, we have to study our
3.6 Ma in the 1970s to about 7 Ma today.
evolutionary history within completely new paradigms.
Since 1994, all these discoveries have had a scienti-
But, as palaeontologists and palaeoanthropologists,
fic impact equivalent to that of Dart’s naming of
we have always to remember that our interpretations
Australopithecus africanus (Dart 1925). During the
have, at most, a life expectancy that usually does not
last 10 years the framework of the hominid evolution-
go beyond the next new major fossil discovery.
ary story has changed markedly. Now, we have a new
understanding of the environments inhabited by early
hominids, and the models established in the 1980s
must be reconsidered. Potential representatives of the 3. THE CHADIAN EARLY HOMINIDS
earliest members of the human clade are now twice The material referred to as the Chadian australopithe-
as old and are shown to be spread much wider over cine ‘Abel’ is an anterior lower jaw (figure 2), with the
the African continent. Moreover, the hominids body missing beyond the P4 level, and to a right P3.
described during the last 15 years, while extending This pre-human has a new mosaic of derived and
the geographical and temporal limits of our family, primitive anatomical characters such as: a flat mental
Phil. Trans. R. Soc. B (2010)
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3318 M. Brunet Chadian hominids and Darwin’s prediction
surface of the lower jaw; a subvertical symphysis, bul-
bous in its outline with a shallow genioglossal fossa;
and an incisiform and very asymmetric canine with a
strong bifid lingual crest. Each premolar exhibits a
three pulp canal rooting pattern and the P4s are sub-
molariform with a large talonid. This original combi-
nation of anatomical features has been interpreted as
being sufficiently distinct to name a new species: Aus-
tralopithecus barhelghazali (Brunet et al. 1996).
To date, only three Late Miocene species may claim
the ‘enviable status’ of being among the earliest
hominids. Two of them are from eastern Africa: Ar.
kadabba (5.8 – 5.2 Ma, Ethiopia; Haile-Selassie
2001; Haile-Selassie et al. 2004; Haile-Selassie &
Woldegabriel 2009) and Or. tugenensis (ca 6 Ma,
Kenya; Senut et al. 2001; Galik et al. 2004; Ohman
et al. 2005; White 2006); the third one, the oldest
known hominid, is from central Africa: S. tchadensis
(7 Ma, Chad; Brunet et al. 2002a,b, 2005). The geo-
graphical location of S. tchadensis, 2600 km west of
the Rift Valley, along with its great antiquity, suggests
an early (at least by 6 Ma) widespread hominid distri-
bution (Sahel and eastern Africa). The material
referred to as the Chadian hominid ‘Toumaı̈’ consists
of a distorted but nearly complete cranium
(figure 3), as reconstructed in three-dimensions
(figures 5 and 6), associated with several mandibular
specimens (figure 4) and isolated teeth. Sahelanthropus
tchadensis displays a unique combination of primitive
and derived characters. Identifiable derived features
of S. tchadensis are: an anteriorly-positioned foramen
magnum linked to a rather short basioccipital and a
sub-horizontal nuchal plane; a downward lipping of
the nuchal crest; lower jaw with a vertical symphysis
with weak transverse tori; and for the dentition, the
anatomical characters are: a non-honing C/P3 complex;
no diastema between C and P3; small-crowned canines
with a long root, the upper one without any honing
distal crest and the lower one with a large distal tubercle,
both shoulders being very low; a P3 with a strongly slop-
ing buccal surface; postcanine teeth with maximum
radial enamel thickness intermediate between chimpan-
zees and australopithecines; and bulbous, slightly
crenulated postcanine occlusal morphology. It is inter-
esting to note that all the hominid mandibular
specimens from TM have the same root pattern in the
postcanine teeth, with two roots and three separate
pulp canals for each premolar (Brunet et al. 2002a,b,
2004, 2005; Vignaud et al. 2002; Guy et al. 2005;
Zollikofer et al. 2005; Brunet 2006, 2009a,b).
As known since Darwin, all these derived characters
show that S. tchadensis cannot be related to an ape
(chimpanzees or gorillas) but clearly suggest that it
must be related to later bipedal hominids, and may
be temporally close to the common ancestor of chim-
panzees and humans (Brunet et al. 2002a,b, 2005;
Guy et al. 2005; Zollikofer et al. 2005).
Scientifically it is impossible to understand why
some authors ignore these derived characters and con-
centrate on primitive ones to reach the conclusion that
S. tchadensis is related to modern apes and even more
precisely to a palaeogorilla (Wolpoff et al. 2002, 2006;
Pickford 2005). This attempt to undermine the clear
affinity of the Chadian hominid is curious mainly
Phil. Trans. R. Soc. B (2010)
when it is coming from, among others, two who have
not yet had the opportunity to check Toumaı̈ casts in
their laboratory. Is it what they believe, or is it only
because they want to keep Orrorin as the earliest
hominid?
The East Side scenario of Coppens (1983) empha-
sized the major role of savannah in early hominid
evolution. Are the earliest known hominid environments
in agreement with such a model?
4. THE LATE MIOCENE HOMINID
ENVIRONMENTS AS WE KNOW THEM
In Chad, the sedimentological evidence from the Late
Miocene TM fossiliferous area demonstrates that, at
least since 7 Ma, successive wet (mega-lake Chad
events) and arid periods (desertic events) occurred.
These successive events are identified by a sedimento-
logical series comprising aeolian sandstones (desertic
episode); perilacustrine sandstones (lacustrine trans-
gression); and green pelite and diatomite (true
lacustrine environment; Vignaud et al. 2002; Schuster
et al. 2006). Sahelanthropus tchadensis and its associ-
ated vertebrate remains have been uncovered from
the perilacustrine sandstones (Anthracotheriid Unit).
Sedimentological data are in agreement with this
mosaic of environments, indicating a vegetated perila-
custrine belt between lake and desert (Vignaud et al.
2002). The Okavango Delta in central Kalahari (Bots-
wana) appears to be a good modern analogue in
presenting similar habitat diversity (mosaic of lacus-
trine and riparian waters, swamps, patches of forest,
wooded savannah, grassland and desertic areas).
Although the precise habitat of the TM 266 hominid
among this mosaic of landscapes available is still
uncertain, it was probably a wooded one (Brunet
et al. 2005). Other significant hominid discoveries
associated with wooded environments in Middle
Awash, Ethiopia (Ardipithecus ramidus and Ar.
kadabba) and Lukeino, Kenya (Or. tugenensis) also
rule out the role played by an open environment
or savannah in favouring the acquisition of bipedal
posture in the course of hominid evolution. Thus,
sedimentological and faunal data rather suggest
wooded environments for Ar. ramidus (White et al.
1994; Woldegabriel et al. 1994) and Ar. kadabba
(Woldegabriel et al. 2001; Haile-Selassie &
Woldegabriel 2009). In 2001 those authors noted: ‘It
therefore seems increasingly likely that early hominids
did not frequent open habitats until after 4.4 Myr.
Before that, they may have been confined to woodland
and forest habitats’ (p. 177). Moreover, according to
the recent description of a partial skeleton of Ar. rami-
dus (White et al. 1994, 2009a,b) from Aramis, Ethiopia
at 4.4 Ma, it appears that this hominid may be the same
new evolutionary grade as are the three late Miocene
taxa. It was a climbing biped, both terrestrial and
arboreal, with an opposable grasping big toe (without
arched feet and walking flat-footed), living in a
woodland landscape (Lovejoy 2009; Lovejoy et al.
2009a,b,c,d; Suwa et al. 2009a,b; White et al. 2009a,b).
A wooded habitat (open woodland with denser
stands of trees in the vicinity) has been also suggested
for the Kenyan Or. tugenensis (Pickford et al. 2002).
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Chadian hominids and Darwin’s prediction
This is of fundamental importance since the three late
Miocene taxa, Ar. kadabba, Or. tugenensis and
S. tchadensis, were all probably habitual bipeds. All
these Late Miocene hominids demonstrate that the
savannah hypothesis is now falsified.
5. NEW PARADIGMS . . . FOR A NEW EARLY
HOMINID STORY
During the last 150 years, most of the models for
hominid evolution have been overturned by successive
discoveries. This fact obviously highlights the impor-
tance of fieldwork, as our understanding of our
evolutionary story has, at most, a life expectancy that
usually does not go beyond new findings.
Twenty years ago, available fossil hominid remains
led us to consider eastern African savannah as the
cradle of mankind. Now, it appears that the earliest
members of our family have favoured wooded environ-
ments, and were not restricted to eastern or southern
Africa but were rather living in a wider geographical
region, including at least central and eastern Africa.
In the last decade, the number of recognized
hominid taxa and the length of our geological roots,
from 3.6 Ma in the 1970s to 7 Ma today, have
doubled. These new hominids, while extending the
geographical and temporal limits of our family, are
Late Miocene ones with new associations of anatom-
ical characters representing a new evolutionary grade.
In Chad, the radiometrical dating of S. tchadensis
indicates that the divergence between chimpanzee
and human lineages occurred before 7 Ma, which
is earlier than generally (Kumar & Hedges 1998;
Pilbeam 2002) or more recently thought by the
molecular phylogenists (Patterson et al. 2006).
Besides, from a palaeobiogeographical point of
view, published results derived from fieldwork show
that central Africa was, at least between 3 and 7 Ma,
a crossroad region marked by sporadic faunal
exchanges with northern and eastern Africa (Brunet
et al. 1995, 1996, 1997, 1998, 2000, 2002a,b, 2004;
Brunet & White 2001; Geraads et al. 2001; Vignaud
et al. 2002; Boisserie et al. 2003, 2005; Likius et al.
2003; Mackaye et al. 2005; Peigné et al. 2005;
Lihoreau et al. 2006).
Better identification of the migratory patterns and
the faunal exchanges between northern, central, east-
ern and southern Africa during the Mio-Pliocene is a
key element that is indispensable for a new under-
standing of the origin and dispersal of the first
members of the human clade and therefore its evol-
utionary history. We need more data from these
geographical areas and notably from north-eastern
Africa (e.g. Libya, Egypt and Sudan).
Finally, for a better understanding of the early
human story palaeontologists and palaeoanthropolo-
gists need more data, and thus will have to conduct
more and more geological and palaeontological field
surveys.
We especially thank the Chadian authorities (Ministère de
l’Education Nationale de l’Enseignement Supérieur et
de la Recherche, Université de N’Djamena/Departement
de Paleontologie, Center National d’Appui à la Recherche-
CNAR); the Ministere Français de l’Enseignement
Phil. Trans. R. Soc. B (2010)
M. Brunet 3319
supérieur et de la Recherche: Université de Poitiers;
Agence Nationale de la Recherche—Projet ANR
05-BLAN-0235; Center National de la Recherche
Scientifique (CNRS: Département INEE, and ECLIPSE);
the Ministère des Affaires Etrangères (DCSUR, Paris and
Projet FSP 2005-54 de la Coopération Franco-
Tchadienne, Ambassade de France à N’Djamena); the
Région Poitou-Charentes; the NSF programme RHOI
(USA) and the Armée Française (Mission d’Assistance
Militaire and dispositif Epervier). We thank all the
members of the Mission Paléoanthropologique Franco-
Tchadienne, including all our friends and colleagues who
participated in acquisition of the field data; G. Florent and
C. Noël for their administrative guidance; and X. Valentin
for his technical support.
A lot of thanks go to our colleagues A. Walker and E.-G.
Emonet for the review and editing of our manuscript. All
the drawings are due to the talent of S. Riffaut.
ENDNOTE
1
M.P.F.T.: Mission Paléoanthropologique Franco-Tchadienne, an
international scientific collaboration between Collège de France,
University of Poitiers, University of N’Djamena and CNAR (N’Dja-
mena) including now more than 60 researchers from 10 countries.
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Phil. Trans. R. Soc. B (2010) 365, 3323–3331

doi:10.1098/rstb.2010.0064

Phylogeny of early Australopithecus: new

fossil evidence from the Woranso-Mille
(central Afar, Ethiopia)
Yohannes Haile-Selassie*
Department of Physical Anthropology, The Cleveland Museum of Natural History, 1 Wade Oval Drive,
Cleveland, OH 44106, USA
The earliest evidence of Australopithecus goes back to ca 4.2 Ma with the first recorded appearance of
Australopithecus ‘anamensis’ at Kanapoi, Kenya. Australopithecus afarensis is well documented
between 3.6 and 3.0 Ma mainly from deposits at Laetoli (Tanzania) and Hadar (Ethiopia). The
phylogenetic relationship of these two ‘species’ is hypothesized as ancestor– descendant. However,
the lack of fossil evidence from the time between 3.6 and 3.9 Ma has been one of its weakest points.
Recent fieldwork in the Woranso-Mille study area in the Afar region of Ethiopia has yielded fossil
hominids dated between 3.6 and 3.8 Ma. These new fossils play a significant role in testing the pro-
posed relationship between Au. anamensis and Au. afarensis. The Woranso-Mille hominids
(3.6 – 3.8 Ma) show a mosaic of primitive, predominantly Au. anamensis-like, and some derived
(Au. afarensis-like) dentognathic features. Furthermore, they show that, as currently known, there
are no discrete and functionally significant anatomical differences between Au. anamensis and
Au. afarensis. Based on the currently available evidence, it appears that there is no compelling evidence
to falsify the hypothesis of ‘chronospecies pair’ or ancestor–descendant relationship between
Au. anamensis and Au. afarensis. Most importantly, however, the temporally and morphologically
intermediate Woranso-Mille hominids indicate that the species names Au. afarensis and Au. anamensis
do not refer to two real species, but rather to earlier and later representatives of a single phyletically
evolving lineage. However, if retaining these two names is necessary for communication purposes, the
Woranso-Mille hominids are best referred to as Au. anamensis based on new dentognathic evidence.
Keywords: Australopithecus afarensis; Australopithecus ‘anamensis’; phylogeny;
Woranso-Mille; Ethiopia

1. INTRODUCTION
The genus Australopithecus was named in the first quar-
ter of the twentieth century (Dart 1925) and includes
at least seven species from South Africa, Tanzania,
Kenya, Ethiopia, and Chad (Dart 1925; Broom
1938; Leakey 1959; Arambourg & Coppens 1968;
Johanson et al. 1978; Brunet et al. 1995; Asfaw et al.
1999). Some workers assign three of these species
(Australopithecus boisei, Australopithecus aethiopicus and
Australopithecus robustus) to a different genus, Par-
anthropus (Broom 1938), based largely on
morphological specializations related to trophic par-
ameters (Clarke 1977; Grine 1986, 1988; Wood &
Ellis 1986; Wood & Chamberlain 1987; Turner &
Wood 1993). Some palaeontologists have even moved
the type species of the genus, Australopithecus
africanus into Paranthropus (e.g. Cela-Conde & Altaba
2002; see also Cela-Conde & Ayala 2007), leaving
Australopithecus with only three species. Whether
Australopithecus is a paraphyletic (Strait et al. 1997) or
monophyletic (Tobias 1967) genus, most researchers
* yhailese@cmnh.org
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3323
agree that one of its species gave rise to the genus
Homo, possibly Australopithecus garhi from the Middle
Awash region of Ethiopia (Asfaw et al. 1999; but see
Strait & Grine 2004).
It was only 30 years ago that Australopithecus afaren-
sis was recognized as the ‘oldest indisputable evidence
of the family Hominidae’ at 3.6 Ma ( Johanson et al.
1978; see Kimbel & Delezene 2009 for detailed
review). However, at the end of the twentieth and
beginning of the twenty-first centuries, a number of
new hominid taxa were recovered, some of which are
twice as old (the family Hominidae is here defined
following Haile-Selassie 2001 and Haile-Selassie et al.
2004). During the 1990s, the discovery of Ardipithecus
ramidus (1994, Ethiopia, 4.4 Ma; White et al. 1994,
1995; Semaw et al. 2005) was followed by Australo-
pithecus ‘anamensis’ (1995, Kenya, 3.9 – 4.2 Ma;
Leakey et al. 1995, 1998; Ward et al. 1999, 2001).
More recent fieldwork in Ethiopia, Kenya and Chad
have pushed the record further into the Late Miocene
with the discovery of Ardipithecus kadabba (Haile-
Selassie 2001; Haile-Selassie et al. 2004, 2009),
Orrorin tugenensis (Senut et al. 2001; Pickford et al.
2002) and Sahelanthropus tchadensis (Chad, 6–7 Ma;
Brunet et al. 2002, 2005). The phylogenetic relation-
ships among these earlier hominids remain a point of
This journal is q 2010 The Royal Society
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3324 Y. Haile-Selassie Hominids from Woranso-Mille, Ethiopia
contention (see Haile-Selassie et al. 2004, 2009, for
details), and Pliocene hominid fossils are poorly sampled
from the 3.6–3.9 and 4.4–5.2 Ma time intervals.
The hominid-bearing Woranso-Mille palaeontolo-
gical study area (WORMIL) has been explored since
its discovery in 2004 (Haile-Selassie et al. 2007).
The fossiliferous deposits in the north and northwes-
tern parts of the study area sample the period
between 3.4 and 3.8 Ma (Deino et al. 2010), a time
frame poorly known in the hominid fossil record
(Kimbel et al. 2006). These ages were determined
using 40Ar/39Ar radiometric dating method (Deino
et al. 2010). The study area has thus far yielded
about 90 fossil hominid specimens, mostly from the
time period between 3.6 and 3.8 Ma. Additional
hominid specimens were collected from slightly
younger (3.4 –3.6 Ma) deposits. Most of these speci-
mens represent isolated teeth and partial jaws,
although they also include a 3.58 Ma partial skeleton
of Au. afarensis (Haile-Selassie et al. 2010a) and
additional fragmentary postcranial remains. Moreover,
a total of 4300 fossil specimens of diverse vertebrate
taxa have been collected thus far, representing more
than 25 mammalian genera and a number of new
species.
Here, a brief summary of early Australopithecus to
which the WORMIL hominids belong is presented,
followed by a brief description of the new hominids
and their phylogenetic relationships. Finally, a discus-
sion is presented on the evolutionary tempo and mode
of early Australopithecus and the proposed ancestor –
descendant relationship between Au. anamensis and
Au. afarensis in light of the new fossil evidence from
Woranso-Mille.
2. EARLY AUSTRALOPITHECUS
The origin of the genus Australopithecus remained elu-
sive until new discoveries from the Early Pliocene in
eastern Africa began to shed some light (White et al.
2006). Based on the currently available fossil evidence,
Au. anamensis is the earliest species of the genus. It is
documented from deposits in Kenya and Ethiopia,
dated between 4.2 and 3.9 Ma (Leakey et al. 1995,
1998; Ward et al. 2001; White et al. 2006).
The integrity and amount of variation in Au. afarensis
have been rigorously debated since its naming in the
1970s (Johanson et al. 1978, 1982; Johanson & White
1979; White et al. 1981, 1993, 2000; Kimbel et al.
1985, 2004; White 1985; Kimbel & White 1988;
Lockwood et al. 2000; Reno et al. 2003, 2005; Plavkan
et al. 2005, among others). Some argued that the
species hypodigm pooled from two asynchronous and
geographically disparate areas, Laetoli (Tanzania;
Leakey 1987; Leakey et al. 1987) and Hadar (Ethiopia),
represents more than one species (Leakey & Walker
1980; Olson 1981, 1985; Senut & Tardieu 1985;
Zihlman 1985). However, the discovery of more speci-
mens at Hadar since the early 1990s and detailed
analyses of the pooled hypodigm have demonstrated
that the amount of variation in Au. afarensis does not
significantly exceed what is observed in a single species
of extant taxa (Kimbel et al. 1985, 2004; Kimbel &
White 1988; Lockwood et al. 2000; White et al. 2000).
Phil. Trans. R. Soc. B (2010)
Further analysis of Au. afarensis mandibles and
teeth also indicated that there was a directional
trend toward an increase in mandibular size through
time, but not in the size of the teeth, contributing to
the larger range of variation seen in the species
(Lockwood et al. 2000; see also Kimbel et al.
2004). The postcranial anatomy of Au. afarensis is
inferred to indicate obligate bipedality (for example,
Lovejoy 1975, 1978; White 1980a,b; Latimer 1983,
1991; Latimer & Lovejoy 1989; Kramer 1999),
although some argued that it was partly arboreal
(for example, Stern & Susman 1981, 1983, 1991;
Jungers & Stern 1983; Stern 2000). The Laetoli foot-
prints, however, yield incontrovertible evidence that
Au. afarensis was fully bipedal (for example,
White & Suwa 1987).
3. THE WORANSO-MILLE FOSSIL HOMINIDS
A total of 55 hominid dentognathic (mostly isolated
teeth) and fragmentary postcranial elements have
been recovered from the Am-Ado (AMA), Aralee
Issie (ARI), Mesgid Dora (MSD) and Makah Mera
(MKM) collection areas of the WORMIL study
area (figure 1). Their age has been chronometrically
constrained to between 3.57 and 3.82 Ma (Deino
et al. 2009). The associated faunal assemblage is
dominated largely by cercopithecids, tragelaphines
and aepycerotines, among others, indicating a more
closed habitat with riverine gallery forest and
abundant water.
(a) Mandibles
Two mandibular fragments were recovered from the
MSD collection area. MSD-VP-5/16 is a well-pre-
served left mandible with M1 – 2, anteriorly broken at
the I2 level. It was found during the 2006 field
season from Mesgid Dora locality 5. Posteriorly, the
preserved corpus extends as far as slightly posterior
to the M3 level. The preserved corpus base is intact.
The entire ascending ramus is missing. MSD-VP-5/
50 is a left mandible with P3 – M3 found during the
2009 field season from Mesgid Dora locality 5. This
specimen is anteriorly broken lateral to the midline.
Posteriorly, part of the ascending ramus is preserved
although some parts of its base below the ascending
ramus are missing (figure 2).
MSD-VP-5/16 probably belongs to a female indi-
vidual largely owing to its small corpus size that is
comparable to A.L. 128-23 (White & Johanson
1982). However, the molars (M1 – 2) in MSD-VP-5/
16 are larger relative to the corpus dimensions.
Australopithecus afarensis-like mandibular features of
MSD-VP-5/16 include corpus robusticity (corpus
breadth at mid-M1/corpus height at mid-M1  100)
of 62.5, the presence of a lateral corpus hollow, and
a more vertical mandibular symphysis, as judged
from the preserved part of the anterior corpus
(Haile-Selassie et al. 2010b). The mandible’s greatest
anterior breadth, however, is at the canine level,
more like Au. anamensis (Leakey et al. 1995; Ward
et al. 1999; see Haile-Selassie et al. 2010b for details).
The anterior corpus of MSD-VP-5/50 is morpho-
logically more similar to Au. anamensis mandibles
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Hominids from Woranso-Mille, Ethiopia Y. Haile-Selassie 3325

(a)
40°28¢0≤E 40°30¢0≤E

AMA
11°32¢0≤N 11°32¢0≤N

ARI

MSD
MKM
M
illl
er
ive
r

11°30¢0≤N 11°30¢0≤N

KSD

0.5 1.0 2 km

40°28¢0≤E 40°30¢0≤E 40°32¢0≤E

(b) (i) Aralee Issie (ARI) (ii) Waki-Mille confluence (WMC) (iii) Korsi Dora (KSD) fossils rhyzoliths
Mesgid Dora (MSD) reworked tuff planar lamination in tuff
Makah Mera (MKM) tuff trough-cross stratification
in tuff
KT basalt carbonate
30 ARI-08-5
conglomerate nodules
10 KT WM-KSD-1&3 horizontal stratification
MLT? P5
(mean 3.570 ± 0.014) sandstone & desiccation cracks
30 ripple cross-stratification
KT pebbles, with
WM-ut-1 T is tuffaceous tuffaceous
20 (3.72 ± 0.03) MKM-08-13 siltstone & fossiliferous
0m sandstone reverse magnetic
MDT MDT P6
P4 ?P7 siltstone & polarity
MKM 20 WT WM-MD-5 (3.77 ± 0.04)MDT P2 ?P8 claystone normal magnetic
P1 0m skeleton
BRT (WM07/W-1) brown silty polarity
10 indeterminate
WT claystone
sandstone magnetic
MLT
polarity
BRT? 10 WM-W-2 (3.76 ± 0.02)
MSD bedded siltstone
MLT & sandstone
0m fault
laminated mudstone
& sandstone
0m bioturbated
WM-W-1 (3.82 ± 0.18)
WMC siltstone

Figure 1. (a) Satellite imagery showing the location of hominid collection areas in the Woranso-Mille palaeontological site.
(b) Stratigraphic sections showing the provenance and age of fossiliferous horizons.

than to those of Au. afarensis (figure 3). The corpus of KNM-KP 29281, KNM-KP 29287, KNM-KP
MSD-VP-5/50 is very deep and transversely narrow at 31713, and KNM-ER 20432 from Kanapoi and
the M1 and other molar levels. Its breadth at M1 Allia Bay (Ward et al. 2001; Kimbel et al. 2006).
(20.7 mm) is within the range seen in Au. afarensis Australopithecus afarensis mandibles are different in
(Kimbel et al. 2004) and Au. anamensis (Ward et al. having an almost vertical contour descending as far
2001), whereas its height at the same position as the corpus base. However, LH 4 is an exception
(44.6 mm) and its robusticity index (46.6) are slightly to this general characteristic of most Au. afarensis
outside the range documented for both groups. mandibles, showing a slight inferomedial sweep at
Australopithecus anamensis mandibles have a mean the C – P3 level (Kimbel et al. 2006). The ascending
robusticity index (53.6, n ¼ 3; Ward et al. 2001) ramus root of MSD-VP-5/50 is positioned more pos-
slightly lower than that of Au. afarensis (57.5, n ¼ 19; teriorly (mid-M2) with most of the M3 buccal face
Kimbel et al. 2004). A.L. 277-1 approaches MSD- visible laterally. However, the canine does not appear
VP-5/50 in terms of its robusticity index (48.4; to be aligned in the longitudinal axis of the postcanine
Kimbel et al. 2004) although the latter is absolutely tooth row, although it is seen in the other, much smal-
deeper and wider. ler mandible (MSD-VP-5/16). In Au. afarensis
The inferomedial sweep of the corpus contour at mandibles, the ascending ramus root is usually at
the C – P4 level seen in MSD-VP-5/50 is comparable M1. The overall morphology of MSD-VP-5/50, par-
to Au. anamensis mandibles (figure 3). This lateral ticularly the anterior lateral corpus profile, is
corpus profile has been described as uniquely intermediate between Kanapoi mandibles and LH 4
characteristic of Au. anamensis mandibles such as and serves, together with KNM-ER 20432, as a
Phil. Trans. R. Soc. B (2010)
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3326 Y. Haile-Selassie Hominids from Woranso-Mille, Ethiopia

(a) (b)

Figure 2. Occlusal, medial and lateral views of mandibular specimens from Woranso-Mille dated at 3.7–3.8 Ma. (a) MSD-VP-
5/16, left mandible with M1 – 2. (b) MSD-VP-5/50, left mandible with P3 –M3. Note the size variation between the two
mandibles and the deep corpus in (b). Scale bar, 5 cm.

(a) (b) (c)

lateral medial

(d) (e) (f)

sup. tr. torus

Figure 3. Cross sections of Au. anamensis and Au. afarensis mandibular corpora at distal P3. (a) KNM-KP 29281; (b) KNM-
ER 20432; (c) MSD-VP-5/50; (d) A.L. 400-1a (right side reversed); (e) A.L. 277-1 and (f) A.L. 417-1a. Modified from
Kimbel et al. (2006). Cross-section of MSD-VP-5/50 was acquired following the methods described by Kimbel et al.
(2006). Scale bar, 2 cm.

good transition from Kanapoi to Laetoli/Hadar lateral the mandibular features shared with Au. anamensis are the
mandibular corpus profiles (figure 3). maximum anterior symphyseal breadth being at the
These WORMIL mandibles show a mosaic of features canine (for example, MSD-VP-5/16; Ward et al. 1999)
shared with both Au. anamensis and Au. afarensis. Some of and the more posterior position of the ascending ramus

Phil. Trans. R. Soc. B (2010)

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

Hominids from Woranso-Mille, Ethiopia Y. Haile-Selassie 3327

(a) (b)

(c)
KNM-KP 34725 ARI-VP-1/190 A.L. 333-35

RdC LdC RdC RdC

0 cm 4

Figure 4. Dental remains from Woranso-Mille. (a) Occlusal (top row) and mesial (bottom row) views of ARI-VP-3/80g (LM2),
ARI-VP-1/90 (LM3), ARI-VP-3/80d (LM2) and ARI-VP-1/462 (LM1). These molars show the lingual slope on upper and
buccal slope on lower molars like Au. anamensis. (b) MSD-VP-5/50, ARI-VP-3/80a and ARI-VP-2/95, P3s from the
Woranso-Mille showing variation in P3 occlusal crown morphology. (c) Comparison of lower deciduous canine root length rela-
tive to crown height. KNM-KP 34 725 (Au. anamensis), ARI-VP-1/190 (Woranso-Mille) and A.L. 333-35 (Au. afarensis). Like
Au. anamensis, the Woranso-Mille specimen has longer root relative to the crown height compared with Au. afarensis. Image of
the Au. anamensis specimen was obtained from Carol Ward and A.L. 333-35 was made from cast.

root (MSD-VP-5/50, see figure 2; Haile-Selassie et al.
2010b), which is also shared with the earlier Ar. ramidus
(Suwa et al. 2009; White et al. 2009). The mandibular
features shared with Au. afarensis include the presence
of an incipient lateral corpus hollow (for example,
MSD-VP-5/16), usually described as characteristic of
this species. Judged from the preserved parts of MSD-
VP-5/16, the mandibular symphysis does not show the
more posteroinferiorly retreating condition seen in Au.
anamensis (Ward et al. 2001; Kimbel et al. 2006). How-
ever, MSD-VP-5/50 shows a more receding symphysis
as seen from the transverse cross-section at the P3 level.
(b) Dentition
In terms of the dentition, the upper and lower molars
have occlusally tapering lingual and buccal faces,
respectively, a trait documented in Au. anamensis
(Ward et al. 2001). As in Au. anamensis, the upper
molars, particularly M2 – 3, taper distally (figure 4a).
The deciduous lower canine (ARI-VP-1/190) is similar
in its crown morphology to Au. afarensis specimens such
as A.L. 333-35, LH 2, and DIK-1-1 from Hadar, Lae-
toli and Dikika, respectively (White 1977, 1980a,b;
Johanson et al. 1982; Alemseged et al. 2006). However,
ARI-VP-1/190 has a relatively much longer root and
less lingual relief as seen in Au. anamensis (figure 4c).
The known P3s from WORMIL show both Au. afaren-
sis-like (ARI-VP-2/95) and Au. anamensis-like
(ARI-VP-3/80, MSD-VP-5/50) occlusal morphology
and document variation in the morphology of the P3
(figure 4b). The P3 occlusal morphology of MSD-VP-
5/50 is more similar to KNM-ER 20 432 from Allia
Bay than to KNM-KP 27 286 from Kanapoi in its
mesiodistally elongated crown and asymmetry, clearly
defined mesial marginal ridge, and larger posterior
fovea. The lingual cusp is also hardly developed.
Enamel thickness, as measured on naturally frac-
tured WORMIL teeth, is also within the range seen
for both hypodigms. The postcranial elements are
not as informative owing to their fragmentary nature.
The dentognathic morphological observations,
Phil. Trans. R. Soc. B (2010)
however, indicate that the WORMIL specimens are
morphologically intermediate between Au. anamensis
and Au. afarensis.
4. PHYLOGENETIC RELATIONSHIPS
Ardipithecus ramidus from the Middle Awash and Gona
study areas in Ethiopia, dated between 4.3 and 4.6 Ma
(WoldeGabriel et al. 1994; Semaw et al. 2005), is con-
sidered to be the possible ancestor of Au. anamensis
although other possibilities cannot be ruled out
(White et al. 2006, 2009). Recent studies on a larger
sample of Ar. ramidus material, including a partial skel-
eton, from the Middle Awash show that Ar. ramidus and
Au. anamensis occupied different ‘adaptive plateaus’
(White et al. 2009). Although further investigation is
imperative to understand the full implication of these
adaptive differences, the ancestor–descendant relation-
ship between these two species remains one of the
alternatives given the currently available fossil evidence.
The temporal distribution and apparent, but lim-
ited, morphological differences between the
hypodigms currently divided into Au. afarensis and
Au. anamensis justified the retention of both species
names as a chronospecies pair (Leakey et al. 1995,
1998; Ward et al. 2001; Kimbel et al. 2006; White
et al. 2006). However, the discovery of the
WORMIL specimens dated at 3.7 – 3.8 Ma minimizes
the differences between the inferred chronospecies
pair and suggests that it represents a single lineage
and should probably be referred to by a single species
name in order to avoid taxonomic confusion. Australo-
pithecus anamensis is interpreted to have been an
obligate biped (Leakey et al. 1995, 1998; Ward et al.
2001), unlike Ar. ramidus, which was a facultative
biped with substantial arboreal adaptation (Lovejoy
et al. 2009). Australopithecus anamensis shares a
number of derived dental characters and locomotor
adaptations with Au. afarensis, and both are grouped
in the same ‘adaptive plateau’ (White et al. 2009).
The presence of temporal and spatial discontinuity in
their fossil record, rather than observed morphological
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3328 Y. Haile-Selassie Hominids from Woranso-Mille, Ethiopia
differences, was probably one of the apparent reasons
to distinguish them at the species level. The discovery
of the WORMIL hominids not only fills some part of
the spatial and temporal discontinuity, but also
reduces the inferred anatomical differences between
the two populations.
The phylogenetic relationship between the two time-
successive ‘species’ of Au. anamensis (3.9–4.2 Ma) and
Au. afarensis (3.0–3.6 Ma) has been addressed in detail
using various analytical methods (Leakey et al. 1995,
1998; Ward et al. 1999, 2001; White 2002; Kimbel
et al. 2006; White et al. 2006). Australopithecus anamen-
sis is suggested to have rapidly evolved from its putative
ancestor Ar. ramidus (White et al. 2006). However, this
remains to be more rigorously tested, particularly in
light of the new revelations about Ar. ramidus (e.g.
Lovejoy et al. 2009; Suwa et al. 2009; White et al.
2009). Australopithecus anamensis and Au. afarensis are
considered by most workers as a chronospecies pair
sampling a single phyletically evolving lineage, although
other alternatives have also been entertained (Kimbel
et al. 2006; White et al. 2006). Most analytical methods
have, thus far, failed to falsify the proposed ancestor–
descendant relationship, or unequivocally recognize
them as two distinct lineages.
The Woranso-Mille hominids dated at 3.6–3.8 Ma
are morphometrically intermediate between Au. afarensis
and Au. anamensis. They represent the best fossil homi-
nid sample that clearly bridges the temporal and
morphological gaps between Au. afarensis and Au. ana-
mensis, lending strong support to the suggestion that
they represent a chronospecies pair (White et al. 2009).
Therefore, every available line of evidence suggests that
Au. anamensis represents an earlier deme of Au. afarensis.
Their separation at a species level was clearly an artefact
of the lack of adequate fossils from the time between
Allia Bay (3.9 Ma) and Laetoli (3.6 Ma) than the pres-
ence of discrete and functionally significant anatomical
characters distinguishing the two groups.
Cladistic analysis on four site-samples of Au. afaren-
sis and Au. anamensis (Hadar, Laetoli, Allia Bay and
Kanapoi) demonstrated that the Au. anamensis– Au.
afarensis lineage is paraphyletic because the younger
Au. afarensis sample from Hadar appears to be the
sister taxon of Au. africanus (Kimbel et al. 2006,
p. 145). Moreover, even Au. afarensis is paraphyletic
since the Laetoli sample shares some dentognathic fea-
tures exclusively with Au. anamensis. The Woranso-
Mille specimens, regardless to which group they are
assigned, further demonstrate the paraphyly of not
only the entire Au. afarensis– Au. anamensis lineage,
but also that of Au. anamensis. Kimbel et al. (2006,
p. 146) suggested that the two most preferred solutions
for the taxonomic conundrum related to Au. afarensis
and Au. anamensis are the ‘recognition of a single evol-
utionary species or the maintenance of the status quo
. . .’. The evidence from Woranso-Mille strongly sup-
ports the former as the most parsimonious solution
and Au. africanus as the sister taxon of this species.
Haile-Selassie et al. (2010b) avoided specific assign-
ment of the Woranso-Mille specimens to either group.
Based on the dentognathic description and compari-
son, however, they showed that the Woranso-Mille
hominids shared more dental characters with Au.
Phil. Trans. R. Soc. B (2010)
anamensis than with Au. afarensis. New discoveries
from the 2009 field season support this observation
by yielding critical information on the anterior man-
dibular morphology of the Woranso-Mille hominids.
The transverse profile of MSD-VP-5/50 at posterior
P3 shows that the lateral mandibular corpus shape is
more like those from Allia Bay and Kanapoi than like
those of Au. afarensis (figure 3) shown by Kimbel
et al. (2006). If the Woranso-Mille hominids dated
between 3.7 and 3.8 Ma had to be assigned to one of
these two arbitrary groups, they could be put into
the earlier Au. anamensis with some confidence. The
temporal range of Au. anamensis would then be
extended to between 3.7 and 4.2 Ma. It should also
be noted that Au. anamensis from Asa Issie is bracketed
between 3.77 and 4.2 Ma (White et al. 2006).
Although this does not result in any changes in terms
of how these two groups are related to each other, it
would mean that specimens such as the Belohdeli
frontal (BEL-VP-1/1; Asfaw 1987), the hominid speci-
mens from Fejej (Fleagle et al. 1991; Kappleman et al.
1996; Grine et al. 2006a,b), and teeth and femur frag-
ment from Galili (Haile-Selassie & Asfaw 2000;
Macchiarelli et al. 2004; Viola et al. 2008) should be
recognized as Au. anamensis. However, this assignment
would simply be based on their geological age although
it gives great valence to the idea of Au. anamensis–Au.
afarensis being a chronospecies pair.
5. DISCUSSION
The 3.7 – 3.8 Ma WORMIL hominid specimens share
a number of dental characters with both Au. afarensis
and Au. anamensis. They are temporally and morpho-
logically intermediate between the two groups and
suggest that Au. anamensis and Au. afarensis do not
warrant an evolutionarily meaningful distinction at
the species level. The Woranso-Mille hominids clearly
connect Au. anamensis and Au. afarensis regardless of
which end of the continuum they belong to, and
suggest that the recognition of two different species
names for two temporally and morphologically con-
tinuous populations of a single phyletically evolving
species is confusing and unwarranted. Following the
currently available classification, the dental and man-
dibular morphological similarities of the WORMIL
specimens (dated at 3.7 – 3.8 Ma) with Au. anamensis
outweigh their similarity with Au. afarensis sensu stricto
(i.e. specimens from Hadar and Laetoli). If the two
names have to be retained, mainly for communication
purposes as some researchers suggest, the available but
limited evidence supports assignment of the
WORMIL hominids to Au. anamensis, extending the
temporal range of the latter group to 3.7 Ma.
There is considerable size range in the relatively
small WORMIL upper (n ¼ 9) and lower (n ¼ 19)
molar samples although they fall within the range of
both Au. anamensis and Au. afarensis. However, they
also represent some of the largest molars in the entire
Au. anamensis/Au. afarensis sample, particularly the
M3s (for example, ARI-VP-1/90, ARI-VP-1/215).
Lockwood et al. (2000) observed a statistically signifi-
cant temporal trend towards an increase in M3 crown
size (mainly by mesiodistal elongation) in Au. afarensis,
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Hominids from Woranso-Mille, Ethiopia
although they noted that outliers (Lockwood et al.
2000) and small sample sizes (White 1985) from
specific time periods could bias this observation. At
the same time, an increase in M3 crown area might
have been the general trend in the Au. anamensis–Au.
afarensis lineage, as seen in the shift from molars with
sloping buccal (lowers) and lingual (uppers) faces in
Au. anamensis to molars with more vertical lingual
and buccal faces in Au. afarensis, which would have
resulted in an increase in overall crown occlusal surface.
This increase in occlusal area would have resulted in
larger chewing surface, which could be linked to an
increase in trophic capability in using a wide variety of
resources (Teaford & Ungar 2000; Grine et al.
2006a,b), ranging from soft fruits and leaves to harder
and brittle fallback foods (Ungar 2004; Grine et al.
2006b). Although Au. afarensis was probably better
fitted (largely owing to its larger molars and thicker
enamel, among others) for a variety of food items
including fallback resources, dental microwear analyses
on a limited number of teeth fails to show differences in
the dietary preferences of Au. afarensis and Au. anamen-
sis (Grine et al. 2006a,b). However, this remains to be
tested with a larger sample of Au. anamensis.
6. CONCLUSION
Palaeontological fieldwork at a newly discovered fossi-
liferous area in the central Afar region of Ethiopia has
yielded new hominid fossil remains dated between 3.4
and 3.8 Ma. The temporal placement of these fossils
renders them crucial to test some of the outstanding
human evolutionary hypotheses such as the phylogen-
tic relationships between Ar. ramidus and Au.
anamensis, and the issue of ancestor – descendant
relationship between Au. anamensis and Au. afarensis.
The 3.7 – 3.8 Ma hominid specimens from the Wor-
anso-Mille clearly show that they are morphologically
intermediate between Au. anamensis and Au. afarensis
and their dental measurements overlap with both
groups, lending support to the hypothesis of Au. ana-
mensis/Au. afarensis being a chronospecies pair
representing a single lineage. Regardless of what part
of this ‘pair’ the Woranso-Mille hominids are assigned
to, however, they document the best example of the
presence of transitional populations in a single phyleti-
cally evolving hominid lineage.
Slightly younger fossil hominids (3.0–3.6 Ma) not
described here promise to shed some light on current
debates related to early middle Pliocene hominid diver-
sity. The Woranso-Mille palaeontological site has
opened a new window into the deep human past and
promises to yield more fossils relevant to answering
crucial questions in human evolutionary studies,
including the presence or absence of early hominid
diversity during the middle Pliocene.
I thank the Authority for Research and Conservation of
Cultural Heritage and the National Museum of Ethiopia of
the Ministry of Culture and Tourism for field and
laboratory permissions and facilities, the Afar Regional
Government, its local administrative units, and the Afar
people of Mille District, for facilitating and directly
participating in my research endeavours. I thank all of the
field participants who helped find the fossils and many
Phil. Trans. R. Soc. B (2010)
Y. Haile-Selassie 3329
others for discussion and access to their unpublished data.
I thank Stephanie Melillo for assistance with figures and
Liz Russell for photography. Finally, discussions with Bill
Kimbel, Denise Su, Gen Suwa, Carol Ward and Tim
White significantly improved the content of this
manuscript. The WORMIL project was financially
supported by National Science Foundation (NSF; grant nos
0234320, 0542037), The Leakey Foundation, Wenner-Gren
Foundation, and National Geographic Society.
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Phil. Trans. R. Soc. B (2010) 365, 3333–3344

doi:10.1098/rstb.2010.0039

Anterior dental evolution in the

Australopithecus anamensis –afarensis
lineage
Carol V. Ward1, *, J. Michael Plavcan2 and Fredrick K. Manthi3,4
1
Department of Pathology and Anatomical Sciences, University of Missouri, M263 Medical Sciences
Building, Columbia, MO 65212, USA
2
Department of Anthropology, University of Arkansas, 330 Old Main, Fayetteville, AR 72701, USA
3
Department of Earth Sciences, National Museums of Kenya, P.O. Box 40658, Nairobi, Kenya
4
Turkana Basin Institute, Stony Brook University, Stony Brook, NY 11794, USA
Australopithecus anamensis is the earliest known species of the Australopithecus – human clade and is
the likely ancestor of Australopithecus afarensis. Investigating possible selective pressures underlying
these changes is key to understanding the patterns of selection shaping the origins and early evol-
ution of the Australopithecus – human clade. During the course of the Au. anamensis – afarensis
lineage, significant changes appear to occur particularly in the anterior dentition, but also in jaw
structure and molar form, suggesting selection for altered diet and/or food processing. Specifically,
canine tooth crown height does not change, but maxillary canines and P3s become shorter mesio-
distally, canine tooth crowns become more symmetrical in profile and P3s less unicuspid. Canine
roots diminish in size and dimorphism, especially relative to the size of the postcanine teeth.
Molar crowns become higher. Tooth rows become more divergent and symphyseal form changes.
Dietary change involving anterior dental use is also suggested by less intense anterior tooth wear
in Au. afarensis. These dental changes signal selection for altered dietary behaviour and explain
some differences in craniofacial form between these taxa. These data identify Au. anamensis not
just as a more primitive version of Au. afarensis, but as a dynamic member of an evolving lineage
leading to Au. afarensis, and raise intriguing questions about what other evolutionary changes
occurred during the early evolution of the Australopithecus – human clade, and what characterized
the origins of the group.
Keywords: Australopithecus anamensis; Australopithecus afarensis; dental evolution

1. INTRODUCTION clade is only sketchy at present. Even so, emerging evi-

Fossil evidence documenting the first 4 Myr of homi-
nin evolution has grown substantially over the past
two decades. While several early taxa have been ident-
ified (Ardipithecus, Sahelanthropus and Orrorin), much
of our understanding of what the earliest members of
the Australopithecus –human clade were like still
comes from the best-known species of Australopithecus,
Australopithecus afarensis. However, Au. afarensis only
appears as early as 3.6 Ma and is not well represented
in the fossil record until 3.4 – 3 Ma (review in Kimbel
et al. 2006, see also White et al. 2000). The new fossils
from Woranso-Mille, Ethiopia (Haile-Selassie et al.
2010), are 3.7 – 3.8 Ma and probably part of this lin-
eage as well. Australopithecus anamensis is the earliest
known member in this clade, appearing by 4.17 Ma
in Kenya and Ethiopia, and is the likely ancestor of
Au. afarensis. Unfortunately, Au. anamensis is relatively
poorly represented in the fossil record, so our under-
standing about this first 400 000 to about 800 000
years of the evolution of the Australopithecus – human
* Author for correspondence (wardcv@missouri.edu).
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
dence from what few fossils are known is beginning to
hint that Au. anamensis was a species in transition and
may offer important insights into the origins of a
number of key hominin traits.
A previous detailed investigation of morphological
changes through time in the successive site samples
of Au. anamensis and Au. afarensis (Kimbel et al.
2006) documented a series of apomorphies that pro-
gressively appear throughout these samples, involving
primarily the dentition, but also some aspects of maxil-
lary and mandibular form. The pattern of the
appearance of these traits strongly supports the
hypotheses of anagenetic evolution of Au. anamensis
to Au. afarensis.
One of the most important apomorphies of the Aus-
tralopithecus – human clade is habitual terrestrial
bipedality with loss of significant climbing abilities.
Unfortunately, little is known about the postcranial
skeleton of Au. anamensis. Australopithecus anamensis
is only known from a femoral shaft, along with some
unpublished vertebral fragments, partial metatarsal,
eroded distal pedal phalanx and manual phalanx, all
from Asa Issie (White et al. 2006), a distal humerus,
capitate, partial manual phalanx and partial tibia
from Kanapoi (Patterson & Howells 1967;

3333 This journal is q 2010 The Royal Society

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3334 C. V. Ward et al. Dental evolution in Australopithecus
Leakey et al. 1995, 1998), and a nearly complete
radius from Allia Bay (Patterson & Howells 1967;
Heinrich et al. 1993; Leakey et al. 1995, 1998). The
tibial diaphysis is oriented orthogonally to the talo-
crural joint, as is that of all later hominins, indicating
a knee placed directly over the ankle during the
single-limb support phase of terrestrial bipedal gait
(Ward et al. 1999b). However, more cannot be said
at the present time about the details or extent of its
adaptation to terrestrial bipedality. In almost all other
major features, the known Au. anamensis postcranial
elements resemble those attributed to Au. afarensis.
The exception may be in the capitate, which appears
to have separate dorsal and plantar articular facets
for MC2 like in extant African apes, and unlike
Australopithecus, Homo, Ardipithecus, Proconsul (Beard
et al. 1986; Lovejoy et al. 2009) or the unknown
3.5 Ma hominin from South Turkwel, Kenya (Leakey
et al. 1998; Ward et al. 1999a). This small feature
may indicate some differences in locomotor or manip-
ulative function, but until more fossils are recovered
our ability to infer postcranial variation among species
is highly limited, and little more than can be said about
whether the same pattern of locomotor or manipula-
tive ability seen in Au. afarensis also characterized
Au. anamensis.
Even less is known about its cranial anatomy. Only a
temporal bone and some maxillary fragments are
known. Australopithecus anamensis appears to have a
smaller external auditory porus than later hominins,
and a potentially more obtuse angle of the tympanic
plate along with a weakly developed articular eminence
(Leakey et al. 1995; Ward et al. 2001). However, little
can be said of the functional or evolutionary signifi-
cance of this morphology without more cranial fossils.
In contrast to the skeleton and skull, there are sev-
eral aspects of the jaws and teeth that are preserved
for both Au. anamensis and Au. afarensis, enabling sig-
nificant comparisons to be made in these elements.
Previous research has noted evolutionary changes in
relative canine size, canine and premolar morphology,
mandibular and maxillary contours and incisor
dimensions (Leakey et al. 1995; Ward et al. 2001;
Kimbel et al. 2006; White et al. 2006). However, the
relative paucity of fossils attributable to Au. anamensis
obscures detailed understanding of the quality, quan-
tity and integration of many features that impact
hypotheses about the evolution of adaptations in this
lineage.
Overall, while the Kanapoi and Allia Bay fossils are
distinguishable from those at Laetoli and Hadar, Au.
anamensis is generally considered to be just an early
member of the Au. afarensis lineage, with a few isolated
morphological plesiomorphies. However, there is
general consensus that Au. afarensis demonstrates
evidence of a greater emphasis on the ability to masti-
cate tougher or more abrasive food items, possibly
associated with shifts in habitat or resource exploitation
(Teaford & Ungar 2000; Ward et al. 2001; White et al.
2006) and/or broadening potential ecological niches.
New fossil evidence provides even more evidence for
shifting adaptations throughout this lineage.
The purpose of this paper is to review and summar-
ize the morphology of the jaws and teeth of
Phil. Trans. R. Soc. B (2010)
Au. anamensis and Au. afarensis based on previously
published fossils, integrate data from some newly dis-
covered specimens from Kanapoi (Manthi et al. in
preparation) which provide new insights and consider
the suite of differences seen between these taxa in an
adaptive and evolutionary context. We note that most
change occurs in the anterior portion of the face and
jaws, with the most dramatic alterations occurring at
or near the canine–premolar complex, but that patterns
of change within teeth in proportions and shape often
are uncorrelated. We propose that these changes
signal possible dietary change and/or altered use of
the anterior dentition in food processing in the early
evolution of the Australopithecus–human clade, in
conjunction with shifts in masticatory adaptations.
2. CANINE TOOTH SIZE, DIMORPHISM
AND THE CANINE/P3 COMPLEX
The evolution of the canine teeth and mandibular
honing premolar in hominins has received a great
deal of attention ever since Darwin (1871). Canine
tooth size reduction is one of the few defining features
of the hominin clade (Wolpoff 1980; Greenfield 1992;
Haile-Selassie 2001, 2004; White et al. 2006, 2009;
Suwa et al. 2009) and is recognized as a signal of
important behavioural and adaptive changes (Plavcan &
Van Schaik 1997). For example, recent discussion of
Ardipithecus ramidus places great emphasis on the
importance of the canine/premolar complex for infer-
ring changes in behaviour and diet—an assessment
with a long tradition in anthropology (e.g. Darwin
1871; Brace 1971; Leutenegger & Kelly 1977; Wolpoff
1978, 1979, 1980; Lovejoy 1981, 2009).
At this point, two major features in hominin canine
evolution are widely accepted. First, male canine teeth
reduced in size relative to a likely ape ancestral con-
dition, with a concomitant reduction of canine sexual
dimorphism, early in the hominin lineage (Brace
1963; Jungers 1978; Wolpoff 1980; Greenfield 1992;
Suwa et al. 2009). Second, by Au. afarensis, the
canine honing complex is reduced or lost (Greenfield
1992; Haile-Selassie 2001, 2004; Kimbel et al. 2006;
White et al. 2006). It is widely assumed that the loss
of the hone is associated with selection for use of the
tooth in diet, probably in food acquisition. The most
explicit functional statement is that the mandibular
canine changes to a more diamond-shaped profile so
that the mesial crest can occlude with the lateral
maxillary incisor (Greenfield 1992; Haile-Selassie
2004). This observation is used to support the
hypothesis that canine reduction and changes in
morphology are a consequence of selection for incor-
poration of the tooth into a functional incisal battery
(Greenfield 1992).
While it may seem that canine crown reduction is a
necessary precursor to alterations in canine form for
other, presumably dietary, functions, an alternative
hypothesis has been proposed. It is possible that
canine tooth crown shape change is integrally linked
to selection for the use of the canine in food processing
and so would have occurred concomitantly with size
reduction, not after it (Greenfield 1992). Such
reduction could be linked in two ways—first would
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Dental evolution in Australopithecus
be a general selective pressure for the use of canines in
food processing that results in crown size reduction fol-
lowing relaxation of selection for the use of the tooth as
a weapon. Second would be that selection for canine
crown reduction would only be linked with changes in
tooth form associated with dietary use of the tooth fol-
lowing an initial canine crown reduction and loss of
dimorphism through a separate, unspecified mechan-
ism. In other words, one model posits that canine
tooth size in all primates, including hominins, reflects
a balance between conflicting selection pressures for
large canines as weapons and small canines for food
acquisition (Greenfield 1992), and the other posits
that selection for dietary functions only occurred after
canine dimorphism was lost, with a secondary crown
reduction associated with the development of occlusal
features that transform the canine into a tool for food
processing and/or acquisition.
The large sample of Ar. ramidus fossils from 4.4 Ma
strongly suggests that substantial reduction in male
canine crown size and loss of significant dimorphism
probably occurred near the origin of hominins and
may not be apomorphic for the Australopithecus–
human clade (White et al. 1994, 1995; Suwa et al.
2009). Indeed, Au. anamensis canine crowns appear to
be approximately the same overall size as those of
Ar. ramidus. Comparisons of associated dentitions
demonstrate Au. anamensis had slightly larger basal
dimensions of its canines relative to postcanine tooth
size than did Au. afarensis (Ward et al. 2001). Overall,
individual tooth sizes do not differ between the species,
with the exception of the maxillary canine mesiodistal
dimension and some dimensions of P3 and P4. The
few preserved canine crowns in Au. anamensis appear
no more variable, or presumably dimorphic, than those
of Au. afarensis so there appears to be no evidence of
evolution of dimorphism during this time period, either.
However, a single large Au. anamensis mandibular
canine alveolus (KNM-KP 29287; Ward et al. 2001),
and to some extent a canine root with heavily worn
crown from Fejej, Ethiopia (FJ-4-SB-1a; Fleagle
et al. 1991), suggested potentially greater canine
crown size sexual dimorphism early in this lineage
than previously appreciated, with the implication that
canine dimorphism decreased at some point in the
Au. anamensis – afarensis lineage. If so, this would be
evidence of social and/or dietary evolution.
Three new associated dentitions from Kanapoi have
clarified details of canine size and proportions of Au.
anamensis (Manthi et al. in preparation), provided new
data on canine proportions and morphology, and
suggested that Au. anamensis is a key taxon for
understanding the adaptive significance of changes in
canine form.
KNM-KP 47951 has the largest mandibular root of
any known hominin (figure 1). Comparison of man-
dibular root size in Au. anamensis with those Au.
afarensis, extant great apes and Homo reveals that
root size variation in Au. anamensis was very strong,
most like Pongo in magnitude (figure 1, table 1), imply-
ing strong dimorphism. This stands in stark contrast to
Au. afarensis, which shows much less variation in root
dimensions, and is intermediate to extant Homo and
Pan in mean size. Unlike the roots, mandibular
Phil. Trans. R. Soc. B (2010)
C. V. Ward et al. 3335
canine crowns are similar in all dimensions in Au. ana-
mensis and Au. afarensis, and both have slightly larger
and more dimorphic crowns than do modern
humans, as also reported for Ar. ramidus (Suwa et al.
2009) but less so than in extant apes. Therefore, not
only was there a clear dissociation between crown
size and root size in Au. anamensis, such that size
and dimorphism in the crowns were lost while size
and dimorphism in the roots were retained, but the
loss of root size dimorphism occurred sometime
during the evolution of Au. anamensis into Au. afaren-
sis. Interestingly, not only does KNM-KP 47951
demonstrate that the large alveolus of KNM-KP
29287 did not imply unusual crown size dimorphism,
it also demonstrates that the canine root of KNM-KP
29287 would not have been unusually large, and may
in fact have been a small male. It would not, however,
have supported a larger crown than those preserved for
Au. anamensis (Plavcan et al. 2009).
Even with the new data, no dimensions of the man-
dibular canine crowns (length, breadth or height) differ
between species (figure 1, table 2). However, there are
dimensional differences in the maxillary canines (see
also Ward et al. 2001; White et al. 2006) (figure 2,
table 2). Australopithecus anamensis and Au. afarensis
are equivalent in maxillary canine crown height and
buccolingual breadth, but Au. anamensis maxillary
canines are mesiodistally longer than are those of
Au. afarensis (figure 3a, tables 2 and 3). Proportion-
ately, Au. anamensis canines are almost exactly
intermediate in basal crown shape (measured as mesio-
distal length relative to buccolingual breadth) between
extant great apes and Au. afarensis (figure 3a). Further-
more, Au. afarensis canine basal shape proportions are
identical to those of extant Homo, after accounting for
their size difference. The apparent progressive decrease
in relative canine size from Au. ramidus to Au. afarensis,
through Au. anamensis (White et al. 2006), tracks
mesiodistal length only, but not overall size of the tooth.
The change in canine basal proportions reflects
change in canine – P3 function. It has long been
noted that the Au. afarensis canine/premolar complex
loses its ‘honing’ function, in the sense that the distal
edge of the maxillary canine no longer exclusively
wears against the labial surface of the mandibular P3
as in other primates (Wolpoff 1979; Greenfield 1992;
Haile-Selassie 2004). Metrically, it is only the maxil-
lary canine and mandibular premolar—the honing
teeth—that change basal shape (figure 3b) to become
less elongate in outline. Mandibular canines and
maxillary P3s do not. This implies no overall selection
to reduce the teeth, but only selection to alter contact
between the honing pair. So, while there may have
been a loss of honing with early hominins (Haile-
Selassie 2001, 2004; Brunet et al. 2002), canine – P3
occlusal relationships continue to evolve.
In addition to basal outlines, the canines and P3
change other aspects of their crown shape significantly
from Au. anamensis to Au. afarensis, strongly
suggesting that selection favoured an altered function
of these teeth. Both mandibular and maxillary canines
become more symmetrical in lingual profile. Maxillary
canines have higher shoulders and shorter mesial
crests, and mandibular canines have lower mesial
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3336 C. V. Ward et al. Dental evolution in Australopithecus

(a) 35 (b) 50
45
30
40
crown height (mm) 25

root length (mm)

35
20 30
25
15 20
10 15
10
5
5
0 0

(c) 25 (d ) 25

20 20
crown MD (mm)

root MD (mm)
15 15

10 10

5 5

0 0
(e) 18 ( f ) 18
16 16
crown BL (mm)

root BL (mm)

14 14
12 12
10 10
8 8
6 6
4 4
2 2
0 0
py rilla

s
. a ens

na is
is

gm a
s

s
ns

na is
is
tro aeu

H yte

tro aeu

H dyte
ill
. a ns
es

s
es
Au apie

Au aren
Au api

or
m

m
od

Au fare
o
gm

o
.g

.g
gl

gl
.s

.s

f
py

.a
G

.a
P.

P.
P.

P.

Figure 1. Dental dimensions for mandibular canine crowns and roots for extant great apes, humans, Au. anamensis and
Au. afarensis. Arrows indicate new specimen KNM-KP 47951. Data in table 1. (a) Crown height, (b) root length,
(c) crown mesiodistal, (d) root mesiodistal, (e) crown buccolingual and ( f ) root buccolingual.

shoulders and a less narrow, blade-like outline
(figure 3c). Lower premolars develop a larger metaconid,
and the protoconid shifts buccally. Marginal ridges
become proportionately more distinctive, and the
anterior fovea opens in a more occlusal direction
(Leakey et al. 1995, 1998; Ward et al. 2001; Haile-
Selassie 2004; Suwa et al. 2009; White et al. 2006).
These shape changes increase transverse contact area
between maxillary and mandibular teeth, most logically
owing to increased use of the canine in food acquisition
or preparation, and perhaps the premolar in mastication
as well.
The fossils demonstrate that canine shape changed
significantly along with a shift in canine – P3 occlusal
relationships in the Au. anamensis – afarensis lineage,
while canine size remained approximately the same.
It is also notable that Au. afarensis canine crowns
show the same basal proportions as in Homo
Phil. Trans. R. Soc. B (2010)
(figure 3a), demonstrating that the major proportional
changes in canine dimensions in hominin evolution
happened between 3.9 and 3.4 Ma.
The dissociation between crown size and shape
changes demonstrates that selection impacting crown
shape was independent of that causing crown height
reduction. This in turn bears on hypotheses that
purport to explain the adaptive significance of canine
crown size reduction in hominins (Brace 1963;
Bailit & Friedlaender 1966; Wolpoff 1969, 1980;
Calcagno & Gibson 1988). Crown height was reduced
prior to the appearance of Au. anamensis, if Ar. ramidus
indeed reflects the ancestral hominin condition (Suwa
et al. 2009), and certainly by the origins of the
Australopithecus – human clade. Data now suggest that
crown height did not reduce in order to provide
room for expanding postcanine dentitions (Jungers
1978), because basal dimensions and root size did
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Dental evolution in Australopithecus C. V. Ward et al. 3337

Table 1. Descriptive statistics for mandibular canine dimensions of extant combined-sex and fossil samples. All data are in
millimetres. Data for Gorilla, Pongo, Pan troglodytes and Homo were collected for this project. Data for Pan pansicus were
taken from Plavcan (1990) and do not include values for root dimensions. Height, crown height; BL, buccolingual; MD,
mesiodistal; RBL, root buccolingual; RMD, root mesiodistal; RL, root length.

height BL MD RBL RMD RL

Gorilla gorilla
n 50 50 50 50 50 50
min. 12.65 9.18 11.53 8.65 11.12 22.02
max. 31.25 16.26 21.66 16.03 21.4 45.27
mean 20.89 12.44 15.55 11.89 15.17 33.18
standard deviation 5.47 2.32 2.82 2.41 3.03 4.13
CV 26.2 18.6 18.1 20.3 20.0 12.4
Pongo pygmaeus
n 16 17 17 17 17 16
min. 13.58 7.97 11.08 7.4 10.2 20.35
max. 26.82 14.53 17.8 14.17 17.52 41.04
mean 19.52 10.49 13.83 10.12 13.39 27.56
standard deviation 4.18 2.51 2.13 2.48 2.31 6.09
CV 21.4 23.9 15.4 24.5 17.25 22.1
Pan troglodytes
n 30 30 30 30 30 30
min. 12.51 7.98 10.1 7.6 8.19 19.99
max. 25.5 15.22 17.17 14.92 16.9 38.0
mean 17.63 10.93 12.8 10.43 12.18 28.59
standard deviation 3.52 1.77 1.92 1.76 2.26 5.03
CV 20.0 16.2 15.0 16.9 18.6 17.6
Pan paniscus
n 29 30 30 — — —
min. 9.5 5.88 7.88
max. 16.13 9.13 11.88
mean 12.27 7.13 9.66
standard deviation 2.02 0.88 1.16
CV 16.5 12.3 12.0
Homo sapiens
n 36 36 36 36 36 36
min. 7.67 5.45 5.94 3.7 5.82 10.94
max. 12.65 7.9 9.13 6.58 8.99 20.2
mean 9.99 6.72 7.67 5.36 7.49 15.96
standard deviation 1.23 0.64 0.71 0.61 0.68 2.18
CV 12.3 9.5 9.3 11.4 9.1 13.6
Australopithecus afarensis
n 6 10 11 9 9 3
min. 10.9 6.9 9.3 6.4 8.8 20.91
max. 17 10.6 13.9 9.5 13.1 24.29
mean 13.12 8.48 10.88 7.82 10.54 22.77
standard deviation 2.22 1.25 1.38 1.08 1.31 1.72
CV 16.9 14.7 12.7 13.8 12.4 7.5
Australopithecus anamensis
n 3 7 7 9 8 3
min. 10 6.6 9 5.9 8.2 20.2
max. 15.71 10.40 13.90 10.3 13.81 31.79
mean 13.27 8.81 11.04 7.99 10.44 26.86
standard deviation 2.94 1.32 1.66 1.43 1.72 5.99
CV 22.2 15.0 15.0 17.9 16.5 22.3

not reduce concomitantly with crowns. Crown height
also did not reduce in order to enhance an incisal
or biting function (Szalay 1975; Wolpoff 1980;
Greenfield 1992) because shape change in the
crown did not accompany crown height reduction.
Following a loss of function of the canine teeth as
weapons (for behavioural reasons, or following
masticatory changes precluding the use of projecting
canines), male canine size—especially crown height—
reduced to the size of those of female extant apes,
as has occurred in other primates (Plavcan et al.
1995). However, canine shape becomes altered
simultaneously with mandibular lateral incisor breadth
(Ward et al. 2001) and premolar form only with the
appearance of Au. afarensis in the absence of further
crown height reduction.

Phil. Trans. R. Soc. B (2010)

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3338 C. V. Ward et al. Dental evolution in Australopithecus

(a) 45 Table 2. Probabilities from t-tests for significant differences

between Au. anamensis and Au. afarensis canine crown areas
40
and linear dimensions using ln-transformed data. Numbers
35 are for two-tailed probabilities. Area is calculated as the length
crown height (mm)

times the breadth of the crown dimensions. Abbreviations as

30
in table 1; mand, mandibular; max, maxillary.
25
20 area MD BL RMD RBL height

15 max 0.546 0.007 0.226 0.009 0.625 0.211

10 mand 0.482 0.208 0.98 0.831 0.843 0.971

5
0 any event, it is now clear that crowns and roots did
(b) 25 not change shape and size as part of a unimodal selec-
tion pressure that drove the canines to the modern
human form. Rather, the patterns of morphological
20 change suggest to us that the selective pressure shaping
crown MD (mm)

canine form during the evolution of Au. anamensis and

15 early Au. afarensis was distinct from that of the earliest
hominins, and of later Homo. This function almost cer-
tainly related to food acquisition or processing, but in
10
a manner distinctive to early Australopithecus.

5
3. MANDIBULAR AND MAXILLARY
MORPHOLOGY
0 Other morphologies distinguishing Au. anamensis and
(c) 25 Au. afarensis also are related to the change in canine
tooth size, and in morphology of the canine/premolar
complex. In particular, canine tooth root size affects
20 the occlusal outline of the anterolateral corner of the
mandible. The mandible of Au. anamensis is distinct
crown BL (mm)

15 from that of Au. afarensis in having an inflated alveolar

profile along the roots, so that the canines are set ante-
riorly to the postcanine tooth rows (figure 4) (Ward
10
et al. 2001). In the male mandible, the effect of a
large root is particularly notable. In contrast, in
5 Au. afarensis, the broadest region across the anterior
mandible is found adjacent to P3, and the canines
0 are set medial to the premolars. There also is less vari-
ation in this contour among mandibles, presumably
py lla

tro eus

H ytes

ns

is
A. ensi

es
ie
P. ori

related to less canine root size dimorphism than in

a

am
od

ap
gm

ar
.g

gl

.s

an
af

Au. anamensis. Certainly, canine size is correlated

G

A.

with mandibular form in primates (Plavcan &

P.

Daegling 2006). Another factor influencing the

Figure 2. Dental dimensions for maxillary canine crowns for
extant great apes, humans, Au. anamensis and Au. afarensis.
Data in table 3. (a) Crown height, (b) crown mesiodistal,
and (c) crown buccolingual.
It could be possible that smaller canine roots in
Au. afarensis could be related to decreased loading of
the canines in puncturing or crushing (Spencer
2003), but microwear studies in Au. afarensis imply
that, in fact, use of the canine for these activities prob-
ably was greater in Au. afarensis than in apes (Ryan &
Johanson 1989). Comparisons with Au. anamensis
microwear will be necessary to explore this possibility
further.
To date, the fossil record is insufficient to evaluate
whether these events in canine and premolar evolution
were indeed simultaneous, but they are so within the
current resolution available in the fossil record. In
Phil. Trans. R. Soc. B (2010)
relatively broad anterior portion of the mandible in
Au. anamensis is that the lower lateral incisors are
relatively broader than in Au. afarensis (Ward et al.
2001). Both canine root breadths and incisor breadth
would affect anterior mandibular size and shape.
The maxilla of Au. anamensis, and early Au. afarensis
from Laetoli (Garusi 1; Puech 1986; Puech et al. 1986),
appears to have narrowly spaced, relatively straight
maxillary tooth rows, also seen in the Woranso-Mille
sample (Haile-Selassie et al. 2010). They also have
rounded margins of the lateral nasal aperture. Both of
these features are plausibly related to reduction in
canine tooth root size. Canine root length may not be
related to maxillary shape (Cobb & Willis 2008;
Plavcan et al. 2009), but root basal area would certainly
affect maxillary breadth in this region and thus the
supporting bone.
Thus, the selective force that shaped canine root
size reduction is plausibly linked to pressures that
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Dental evolution in Australopithecus C. V. Ward et al. 3339

(c)
(a) 3.3
Au. anamensis
ln (crown mesiodistal length) (mm)

2.9

2.5

2.1

1.7
1.7 1.9 2.1 2.3 2.5 2.7 2.9 3.1
ln (crown buccolingual breadth) (mm)

Au. afarensis
(b) 1.6
crown mesiodistal/buccolingual

1.4

1.2

1.0

0.8

0.6 p < 0.05 p < 0.05

mandibular maxillary
canine P3 canine P3

Figure 3. Illustrations of canine shape differences between Au. anamensis and Au. afarensis. (a) Scatterplot of ln-transformed
maxillary canine mesiodistal length compared with buccolingual breadth. Open squares: Gorilla gorilla, Pan paniscus, P. troglo-
dytes, Pongo pygmaeus; open triangles: Homo sapiens; grey diamonds: Au. afarensis; black circles: Au. anamensis. Australopithecus
anamensis retains relatively long canines mesiodistally and are most similar in proportions to extant apes. Australopithecus afar-
ensis canines are similar buccolingually but are mesiodistally shorter than those of Au. anamensis. Humans have the same
proportions as seen in Au. afarensis, but are smaller overall. (b) Basal proportion differences are seen only in the maxillary
canine and mandibular premolar, the teeth that hone, but not mandibular canine or maxillary premolar, illustrating that
observed shape changes are associated with a further reduction in honing and a shift in occlusal relationships in this complex.
(c) Morphologic differences in canines and P3. Australopithecus anamensis has a lower mesial crown shoulder and longer mesial
crest in the maxillary canine, a narrower, more blade-like mandibular crown with pronounced distal tubercle and a more
unicuspid P3 with centrally placed paraconid compared with Au. afarensis. Data in tables 1 and 3. Scale bar, 1 cm.

altered mandibular and possibly maxillary geometry. (Hylander 1984, 1985; Ravosa 2000). Australopithe-
Teaford & Ungar (2000) noted that mandibular cus anamensis had a correspondingly large post-
corpus robusticity is intermediate in Au. anamensis incisive planum and strongly developed mandibular
between that of great apes and later hominins, tori, probably related to this overall geometry. A
suggesting an increase in adaptation to resist heavier wider geometry in Au. afarensis would reduce
masticatory stresses with Au. afarensis. That Au. forces from wishboning owing to pull of the external
afarensis was adapted to greater masticatory stresses masticatory muscles and bone (Hylander 1985).
is also suggested by the increased height of its More divergent tooth rows also decrease symphyseal
molar crowns (Leakey et al. 1995; Ward et al. torsional stresses. It is notable, therefore, that
1999b, 2001). Australopithecus afarensis mandibles despite altered mandibular geometry, symphyseal
also tend to have more posteriorly divergent tooth robusticity still tends to be relatively greater in Au.
rows than does Au. anamensis, whose tooth rows afarensis than Au. anamensis.
are narrower and more parallel, more like those of Given the effects of mandibular geometry on sym-
extant apes (Ward et al. 2001). Narrow tooth rows physeal stresses, it may be that selection for more
increase symphyseal stresses owing to wishboning divergent tooth rows influenced the reduction of lateral
and torsion of the mandible during mastication incisor breadth and canine root size in order to reduce

Phil. Trans. R. Soc. B (2010)

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3340 C. V. Ward et al. Dental evolution in Australopithecus

Table 3. Descriptive statistics for maxillary canine crown Thus, the mandibular morphology of Au. afarensis
dimensions of extant combined-sex and fossil samples. implies selection for the ability to process harder-
Abbreviations as in table 1. to-chew foods, possibly opening up new niches.
However, it is not only the masticatory system that
height BL MD has changed; reduction in lateral incisor breadth
and reshaping of the canine crowns and the canine –
Gorilla gorilla
n 50 50 50
premolar complex also suggest that selection for
min. 12.14 10.26 12.54 altered function of the anterior dentition in food pro-
max. 41.56 22.12 23.23 cessing occurred in the transition from Au. anamensis
mean 22.08 13.88 17.17 to Au. afarensis.
standard deviation 7.44 2.78 3.24
CV 33.7 20.0 18.9
Pongo pygmaeus 4. TOOTH WEAR
n 18 18 18 One feature not previously appreciated from published
min. 12.74 8.09 11.11 fossils is that for those specimens showing substantial
max. 30.45 15.43 18.56 tooth wear, there appears to be differentially heavy
mean 20.15 11.80 14.76 anterior tooth wear in Au. anamensis compared with
standard deviation 6.15 2.19 2.72 Au. afarensis. Quantitative comparisons of gross wear
CV 30.5 18.6 18.4 patterns are difficult owing to the fragmentary preser-
Pan troglodytes vation of the dentitions, but qualitative comparisons
n 30 30 30 can be made. Overall, Au. anamensis appear to have
min. 11.86 8.09 9.63 higher frequencies of heavier tooth wear than seen in
max. 27.27 14.25 19.31 Au. afarensis.
mean 18.05 10.56 12.82 Three out of four known Au. anamensis maxillae
standard deviation 4.03 1.79 2.31
that preserve molars and anterior teeth all have heavy
CV 22.3 17.0 18.0
anterior wear relative to that of the molars (figure 5).
Pan paniscus KNM-KP 29283 has dentine exposure crossing both
n 24 30 30 lingual cusps of M1 and M2. Its incisors and canines
min. 8.63 6.13 8.63 preserve only a narrow band of enamel labially, but
max. 20.38 11.13 14.38
were wearing onto the roots lingually. The new speci-
mean 13.40 8.01 10.54
standard deviation 3.48 1.44 1.56 men, KNM-KP 47952 (Manthi et al. in preparation),
CV 26.0 18.0 14.8 also has unusually high anterior tooth wear, with only
1–2 mm of enamel remaining along the lingual surfaces
Homo sapiens of its incisors and canines. In apparent contrast, dentine
n 50 50 50
min. 6.48 6.56 5.96
is only exposed on M2 as a tiny pit on the paracone.
max. 12.26 9.82 8.49 Even if this molar is not associated, which it almost cer-
mean 9.28 8.24 7.45 tainly is, there is an unusually heavy amount of anterior
standard deviation 1.23 0.71 0.57 wear. Another Kanapoi fossil, KNM-KP 30498, has
CV 13.3 8.6 7.7 M2 preserved, but on M1 has a small area of dentine
Australopithecus afarensis
exposed only on the paracone. Its I1 is worn all the
n 8 8 8 way up to the basal tubercle, probably about halfway
min. 9.2 9.3 8.9 through the original length of the tooth. The canine
max. 15.4 12.5 11.6 of this same specimen is worn almost up to its mesial
mean 12.35 10.7 9.81 or distal tubercles. In fact, no unworn incisors are
standard deviation 2.18 1.00 0.84 known from Au. anamensis at all, except those of
CV 17.7 9.3 8.6 young individuals whose teeth are either not yet or
Australopithecus anamensis barely in occlusion, and/or who exhibit little or no
n 3 7 8 molar wear. The only relatively unworn maxilla with
min. 12 8.8 9.91 canine is ASI-VP-2/344 from Aramis, which has no
max. 16 11.2 12.4 dentine exposure on M2 but still exhibits apical wear
mean 14.4 10.20 11.10 on its canine (White et al. 2006). This specimen
standard deviation 2.12 0.75 0.82 appears comparable in wear to teeth in the Au. afarensis
CV 14.7 7.4 7.4 maxilla AL 200-1.
In contrast, no comparably heavy differential wear
is found in the associated maxillary dentitions of
Au. afarensis at Hadar or Laetoli, and none is as heavily
the breadth of the anterior mandible in Au. afarensis. worn as any of the three Kanapoi specimens. The M2s
This may have co-occurred with widening of the pos- of AL 444 (Kimbel et al. 2004) are more worn than
terior part of the mandible, too. In order to maintain those of KNM-KP 47952, but less than those of
appropriate occlusal relationships, this could also KNM-KP 29283, but most of the incisor and
have led to concomitant reduction in maxillary canine crowns are intact in AL 444. AL 199-1 and
canine root dimensions, and corresponding reduction AL 200-1 have less wear on their molars than any
in maxillary inflation along the canine juga and lateral Au. anamensis maxilla, and while they have some
nasal aperture. wear on the incisors and canines, it is not heavy. The
Phil. Trans. R. Soc. B (2010)
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Dental evolution in Australopithecus C. V. Ward et al. 3341

Figure 4. Top row photos: occlusal views of all three Kanapoi mandibles, from left to right KNM-KP 29281, KNM-KP 29287,
KNM-KP 31713. Bottom row line drawings: several mandibles of Au. afarensis, from left to right: LH 4, AL 123-23, AL 333w-60,
AL 266-1, AL 400-1a, AL 277-1 and AL 198-1. Arrows denote anterolateral inflection of occlusal outline. Note the canine roots
set medial to that of P3 in the Au. afarensis, and in contrast that the canines are set anterior to the P3 in the Au. anamensis fossils so
that the anterolateral corner of the occlusal profile is formed by the canine juga in this earlier species. Scalar bar, 0–4 cm.

KNM-KP 30498 KNM-KP 47952 KNM-KP 29283

Figure 5. Lingual views (top) of anterior teeth of KNM-KP 30498 and KNM-KP 47952 and occlusal views (bottom) of these
anterior teeth and their associated molars. KNM-KP 29283 shown in medial (top) and occlusal (bottom) views for compari-
son. KNM-KP 30498 preserves I1, C, P3, M1 and M3 crowns, relevant teeth reversed to show all as if they were from the left
side. KNM-KP 47952 preserves I1, I2, C and M2. All three specimens show relatively heavy anterior wear relative to molar
wear. See text for discussion. Scalar bar, 0–4 cm.

Phil. Trans. R. Soc. B (2010)

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3342 C. V. Ward et al. Dental evolution in Australopithecus
most worn published Au. afarensis incisor is AL 198-
17a (Johanson et al. 1982) which is comparable to
that of KNM-KP 30498. Unfortunately it is not
associated with any postcanine teeth, so further
comparison cannot be made.
Mandibular tooth wear is not directly comparable
to maxillary wear, but even in sufficiently preserved
mandibular dentitions, anterior tooth wear is at least
as great or greater on the teeth relative to the molars
in Au. anamensis when compared with Au. afarensis.
The Au. afarensis mandible with the most heavily
worn molars, AL 198-1, has dentine exposed across
the occlusal face of M1 and buccal cusps of M2, but
still has most of its canine crown preserved. It is only
slightly less worn anteriorly than the Au. anamensis
type mandible KNM-KP 29281. The most heavily
worn mandibular dentition of all is the Au. anamensis
specimen FJ-4-SB-1a from Fejej, Ethiopia (Fleagle
et al. 1991), which has a similar level of molar wear
to AL 198-1, yet it has dentine exposure over almost
the entire P3 cusp and the associated canine is
almost completely worn to the root, preserving only
a narrow band of enamel.
In summary, no anterior teeth are known from
Hadar in which the entire crown is missing, yet
many specimens attributed to Au. anamensis are very
heavily worn. All individuals with sufficiently heavy
molar wear to expose dentine on M2 have very heavily
worn anterior teeth in Au. anamensis, whereas this is
not the case for Au. afarensis. Only expanding sample
sizes will provide an adequate test of how typical this
distinction is, but current fossils are suggestive.
There could be three possible explanations for this,
which are not mutually exclusive, and all hint at selec-
tion for altered involvement of the anterior dentition.
The first possibility is that the anterior permanent den-
tition erupts earlier relative to the molars in
Au. anamensis than Au. afarensis, and that there was
a shift to delay eruption of the incisors and canines
in Au. afarensis relative to molar development. The
second would be ingesting or biting foods with
higher levels of tannins, which might increase intra-
oral friction and cause higher tooth wear (Prinz &
Lucas 2000). The third possibility is that there is a
difference between these samples in patterns of food
processing involving the anterior dentition in which
the teeth are suffering greater mechanical abrasion
(Teaford & Ungar 2000). Under any of these scen-
arios, anterior tooth use or dietary properties
probably would have differed between Au. afarensis
and Au. anamensis.
We suggest that the chemical hypothesis does not
provide the most satisfactory explanation because rela-
tive anterior wear appears to decrease in concert with
shape changes in incisor breadth, canine length and
crown shape, as well as premolar proportions and
crown morphology. The combination of changes in
both wear gradient and dental morphology hints at a
mechanical factor. Detailed study of anterior tooth
microwear and dental growth patterns are needed to
help test the various hypotheses of altered tooth wear
between these species. Regardless, no matter what
the explanation, the pattern suggests a shift in diet or
anterior tooth use of some sort.
Phil. Trans. R. Soc. B (2010)
5. SUMMARY AND CONCLUSIONS
The discovery of new fossils, even though representing
only a small portion of the anatomy of Au. anamensis,
dictates a more careful, circumspect view of the role of
this taxon in hominin evolution, and thereby the pat-
tern of the origin of the adaptive suite of behaviours
and characters shaping the early evolution of the Aus-
tralopithecus –human clade. Australopithecus anamensis
documents a morphology in the anterior face and den-
tition that is clearly transitional between a more
primitive hominin form, and that seen in Au. afarensis.
Given that the fossil record consists of mainly
teeth and jaws, it should come as no surprise that
the evidence suggests that any adaptive shift from
Au. anamensis – afarensis lineage was related to diet.
The data from the new Kanapoi fossils, in combi-
nation with previously published data, demonstrate
that adaptively significant differences exist between
Au. anamensis and Au. afarensis. These morphologies
are not isolated, but seem to reflect an adaptive shift
to a diet involving heavier mastication and at the
same time altered use of the anterior dentition in
food processing.
Taken together, the greatest known differences
between Au. anamensis and Au. afarensis are associated
with evolutionary changes within the canine/P3 com-
plex, and with adaptations for coping with increasing
masticatory loads on the postcanine dentition. It has
long been supposed that reduction in canine crown
height accompanied selection for an increased ability
to masticate tougher or harder foods, as well as with ori-
gins of habitual terrestrial bipedality. Ardipithecus
ramidus demonstrates that crown height reduction is
not linked to increased ability to masticate tougher or
harder foods (White et al. 1994; Suwa et al. 2009),
and Au. anamensis demonstrates that shape change
altering occlusal relationships between the canine and
premolar, and reduction in canine crowns and roots
were dissociated. Even though the canine/P3 complex
changed form in the Au. anamensis/Au. afarensis lineage,
canine crown size itself remained stable, while the den-
tition and mandible showed progressive changes that
suggest adaptation to heavy loads.
The dissociation between changes in root and
crown size is distinctive in the evolution in Au. ana-
mensis – afarensis. Given that Ardipithecus also has
large roots relative to its crowns (Suwa et al. 2009),
the Au. anamensis condition appears primitive for
hominins. A reduction in root size is achieved with
the appearance of Au. afarensis, a species in which
the premolars are more molariform, lower lateral inci-
sors less broad and maxillary canine crowns are
mesiodistally shorter with concomitant shorter mesial
crests, mandibular canines less blade-like and more
symmetrical in profile. Tooth rows are less parallel
and anterolateral mandibular and maxillary contours
less inflated, probably related to the presence of smal-
ler canine roots. An association between root size
reduction and a shift to a more functionally
advantageous jaw morphology is worth investigating.
Furthermore, the new Kanapoi fossils highlight the
nature of Au. anamensis as a truly transitional species
between a more primitive condition to what is seen
in Au. afarensis, and to some extent later hominins.
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Dental evolution in Australopithecus
Australopithecus anamensis was not just a primitive ver-
sion of Au. afarensis, it was the species at the root of the
Australopithecus – human clade in which some key
aspects of Australopithecus morphology were develop-
ing (see also Haile-Selassie et al. 2010). At the same
time, not all of the characteristics seen in Au. afarensis
were present at the origin of the Australopithecus –
human clade, so not all distinguish members of this
clade from its sister taxa.
Whether apparent dietary evolution co-occurred with
shifts in locomotor or manipulative adaptations, body
size, dimorphism, cranial morphology or brain size
during the early evolution of the Australopithecus–
human clade can only be elucidated with more fossils
from the time of first occurrence of Australopithecus
(4.17 Ma) and Au. afarensis from Hadar (3.4–3.0 Ma).
We hypothesize that Au. anamensis is best viewed as
not simply a primitive precursor to Au. afarensis, but
rather part of a dynamic morphological transition from
a primitive, ape-like morphology to the unique set of
morphological adaptations and behaviours that charac-
terized the australopithecine bauplan and the early
evolution of the Australopithecus–human clade.
We thank the National Museums of Kenya, Emma Mbua,
Robert Moru, the Royal Museum of Central Africa,
Cleveland Museum of Natural History and United States
National Museum for access to specimens. We thank Chris
Dean, Bill Kimbel, Meave Leakey, Faydre Paulus, Matt
Ravosa, Peter Ungar and Bernard Wood for assistance,
advice and helpful discussions. We thank Alan Walker and
Chris Stringer for generously inviting us to participate in
this symposium. We thank the Wenner Gren Foundation,
Leakey Foundation, Turkana Basin Institute and National
Science Foundation for support in various aspects of this
project.
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Phil. Trans. R. Soc. B (2010) 365, 3345–3354

doi:10.1098/rstb.2010.0033

Molar microwear textures and the diets

of Australopithecus anamensis
and Australopithecus afarensis
Peter S. Ungar1,*, Robert S. Scott2, Frederick E. Grine3
and Mark F. Teaford4
1
Department of Anthropology, University of Arkansas, Old Main 330, Fayetteville, AR 72701, USA
2
Department of Anthropology, Rutgers University, New Brunswick, NJ, USA
3
Departments of Anthropology and Anatomical Sciences, Stony Brook University, Stony Brook, NY, USA
4
Center for Functional Anatomy and Evolution, Johns Hopkins University, Baltimore, MD, USA
Many researchers have suggested that Australopithecus anamensis and Australopithecus afarensis were
among the earliest hominins to have diets that included hard, brittle items. Here we examine dental
microwear textures of these hominins for evidence of this. The molars of three Au. anamensis and 19
Au. afarensis specimens examined preserve unobscured antemortem microwear. Microwear textures
of these individuals closely resemble those of Paranthropus boisei, having lower complexity values
than Australopithecus africanus and especially Paranthropus robustus. The microwear texture complex-
ity values for Au. anamensis and Au. afarensis are similar to those of the grass-eating Theropithecus
gelada and folivorous Alouatta palliata and Trachypithecus cristatus. This implies that these Au. ana-
mensis and Au. afarensis individuals did not have diets dominated by hard, brittle foods shortly
before their deaths. On the other hand, microwear texture anisotropy values for these taxa are
lower on average than those of Theropithecus, Alouatta or Trachypithecus. This suggests that the
fossil taxa did not have diets dominated by tough foods either, or if they did that directions of
tooth – tooth movement were less constrained than in higher cusped and sharper crested extant
primate grass eaters and folivores.
Keywords: Australopithecus; molar; diet; microwear textures

1. INTRODUCTION (a) Background

Researchers have recognized for more than three
decades that patterns of microscopic use wear on
teeth hold the potential to provide information about
the diets of early hominins (e.g. Grine 1977, 1981,
1986; Puech 1979; Ryan 1980; Walker 1981; Ungar
et al. 2006). Many studies of hominin dental micro-
wear have been published over the past thirty years,
including feature-based quantitative analyses of
molar occlusal surface microwear in Australopithecus
afarensis 1 and Australopithecus anamensis (Grine et al.
2006a,b). Data presented here extend this work by
comparing the microwear textures of these species
with those of other early hominins and recent primate
taxa with known diets. Results indicate that sampled
Au. anamensis and Au. afarensis individuals tend to
have relatively simple microwear surface textures vary-
ing in degree of anisotropy. This pattern is comparable
to that previously reported for Paranthropus boisei
(Ungar et al. 2008), but differs from that of Au. africa-
nus, and especially of Paranthropus robustus (Scott et al.
2005; see also Grine 1986).
* Author for correspondence (pungar@uark.edu).
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3345
Australopithecus anamensis and Au. afarensis have
traditionally been argued to be the earliest hominins
to show an adaptive shift from diets dominated by
soft, sugary forest fruits to hard and brittle or abrasive
foods (Ward et al. 1999; Teaford & Ungar 2000; White
et al. 2000; Wood & Richmond 2000; Walker 2002;
Macho et al. 2005). Australopithecus afarensis, for
example, has long been noted to have thickly enam-
elled, large and flat crowned cheek teeth and
robustly constructed crania and mandibles, at least
when compared with our nearest living relatives, the
chimpanzees (e.g. McHenry 1984; Hylander 1988;
White et al. 2000). This enhanced craniodental toolkit
has led workers to suggest that ‘nuts, seeds, and hard
fruit may have been an important component to the
diet of this species’ (Wood & Richmond 2000).
These hominins have also been thought to have had
dietary adaptations intermediate between those of
frugivorous forest apes and later hominins. White
et al. (2000), for example, considered them to have
taken the ‘initial functional steps that would eventually
culminate in the far more derived, specialized mastica-
tory apparatus of later hominid species’ such as
Au. africanus and especially Par. boisei and
Par. robustus. As White et al. (1981) noted, while
Au. africanus showed several craniodental features
foreshadowing the functional specializations seen in
This journal is q 2010 The Royal Society
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3346 P. S. Ungar et al. Pliocene hominin microwear textures
Paranthropus, Au. afarensis retained at least some more
primitive traits, such as relatively larger front teeth and
less swollen and inflated cusps on their postcanines.
Picq (1990) further suggested that the height and
thickness of the Au. afarensis mandibular corpus, and
robusticity of the symphysis, were intermediate
between those of chimpanzees on the one hand and
those of Au. africanus and especially Paranthropus
species on the other. He argued the same for the
height of the ramus and size of the mandibular
condyle.
Picq (1990) used these lines of evidence to build a
scenario in which Au. afarensis was still dependent on
the fruits of the forest, but seasonally sought sustenance
in more open settings with ‘tougher foods containing
abrasive structures’ and ‘nuts protected by skins or a
hard shell’. Ungar & Teaford (2001) called this a
‘mixed forest–savanna resource adaptation’. Ungar
(2004) further noted that the degree of differences in
occlusal slope and relief between Au. afarensis and
chimpanzees are as expected for differences in ‘fallback’
foods, suggesting that the early hominins may have pre-
ferred soft, sugar-rich fruits, but had the ability to make
more effective use of hard, brittle resources as seasonal
availabilities required.
Following its initial description, Au. anamensis
quickly took on the role of ‘intermediate form’ in
terms of dietary adaptation between the earlier Ardi-
pithecus and Au. afarensis. Like Au. afarensis, Au.
anamensis had thicker post-canine tooth enamel and
larger average cheek teeth than Ardipithecus, again
suggesting a dietary shift towards harder foods or
more abrasive ones (Ward et al. 1999; Teaford &
Ungar 2000; Wood & Richmond 2000; Walker 2002;
Suwa et al. 2009). Still, in comparison with Au. afaren-
sis, Au. anamensis molars were ‘not very high-crowned’
(Walker 2002), and the larger values for enamel thick-
ness in Au. anamensis when compared with Ar. ramidus
may reflect, at least in part, increased tooth size in
the former (Suwa et al. 2009, supporting online
material). Further, Au. anamensis lacked changes in
the geometry of the mandible and maxilla seen in
Au. afarensis, Au. africanus and especially Paranthropus
(Ward et al. 1999), such as greater mandibular corpus
robusticity, which might buttress the jaw against higher
peak force magnitudes or repetitive loading in mastica-
tion (Teaford & Ungar 2000). These differences led
Teaford & Ungar (2000) to speculate that hard and
perhaps abrasive foods may have become even more
important components of the diet of Au. afarensis.
Walker (2002) suggested that changes from
Au. anamensis to Au. afarensis were carried to extremes
in Au. africanus and especially Paranthropus.
The microwear evidence paints a somewhat more
complex picture. One might predict heavy pitting
associated with hard-object consumption in Au. ana-
mensis and Au. afarensis and an increase in pitting
from the earlier to the later species. Contrary to expec-
tation though, both show fairly fine features and
microwear surfaces dominated by striations rather
than pits (Grine et al. 2006a,b; Suwa et al. 2009,
supporting online material). This pattern is more
similar to that seen in the tough food folivore
Gorilla gorilla beringei than in hard-object feeders,
Phil. Trans. R. Soc. B (2010)
such as the grey-cheeked mangabey Lophocebus
albigena and the brown capuchin, Cebus apella.
Further, the microwear pattern for these hominins is
remarkably homogeneous between specimens across
both time and paleoecological context. Grine et al.
(2006a,b) suggest that these results highlight the
difference between ‘faculty’ and ‘biological role’
(Bock & von Wahlert 1965) or dietary potential and
what an animal eats on a day-to-day basis. As a
result, Grine et al. (2006a,b) suggested that the shift
in diet-related adaptive morphology in Au. anamensis
and Au. afarensis may relate more to occasional but
critical fallback food exploitation than to preferred
resources.
We might predict, if Au. africanus and especially
Par. boisei and Par. robustus show further craniodental
specializations for the consumption of hard, brittle
foods, that samples of these species should have
more individuals showing high levels of microwear pit-
ting or surface complexity with fewer fine, parallel
striations and with texture anisotropy, compared with
Au. afarensis and especially Au. anamensis.
Here we present the first microwear texture analysis
of Au. afarensis and Au. anamensis for comparison with
Au. africanus, Par. boisei and Par. robustus. Microwear
texture analysis has proved to provide a three-
dimensional characterization of microwear surfaces
free from the need to identify and measure individual
features (e.g. Ungar et al. 2003, 2007a,b, 2008; Scott
et al. 2005, 2006, 2009a; El-Zaatari 2008; Krueger
et al. 2008; Ungar & Scott 2009; Krueger & Ungar
in press). While microwear texture analysis and con-
ventional feature-based analyses to date have yielded
similar results for other hominins (compare Grine
(1986) with Scott et al. (2005) and Ungar et al.
(2006) with Ungar & Scott (2009)), texture analyses
are particularly well suited for between-studies com-
parisons, because data collected are free from
observer measurement error. Further, microwear tex-
ture results for Au. africanus, Par. robustus and Par.
boisei are available in the literature for comparison
(Scott et al. 2005; Ungar et al. 2008). Indeed, only
texture data are available for Par. boisei.
Microwear texture analysis studies indicate that
hard-object feeding extant primates (and other mam-
mals) tend to have higher average levels of texture
complexity and lower levels of anisotropy on their
molar occlusal surfaces than seen in tough food
eaters (see Ungar et al. 2007b for a review). Here we
test the hypothesis that interpretations of craniodental
functional morphology described above are reflected in
microwear texture patterns. If so, Au. afarensis and
especially Au. anamensis specimens should show less
surface complexity and more anisotropy than those
of Au. africanus, and especially Par. boisei and
Par. robustus.
2. MATERIAL AND METHODS
Dental microwear texture data are presented here for
the molar teeth of Au. anamensis from Kanapoi and
Allia Bay in Kenya and Au. afarensis from the Laetolil
Beds in Tanzania and the Hadar Formation in Ethio-
pia. Specimens included in this study are the same as
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Pliocene hominin microwear textures P. S. Ungar et al. 3347

Table 1. Microwear texture analysis data for Au. anamensis and Au. afarensis.

specimen Asfc epLsar1.8 Smc HAsfc9 HAsfc81

Au. anamensis
KNM-ER 35236 0.97466 0.00307 0.15015 0.58516 0.71286
KNM-KP 29287 0.80791 0.00299 0.20908 0.34424 0.58869
KNM-KP 34725 1.30999 0.00244 0.50835 0.38439 0.83670
Au. afarensis
AL 128-23 0.64728 0.00122 0.70776 0.30052 0.37230
AL 145-35 0.87280 0.00337 0.26841 0.45188 0.56429
AL 188-1 0.53380 0.00390 0.34143 0.29913 0.33684
AL 200-1b 0.70342 0.00572 0.21016 0.40769 0.57363
AL 225-8 1.06196 0.00594 0.26836 0.61132 0.99634
AL 288-1i 0.68804 0.00184 1.20858 0.34728 0.49713
AL 333-74 0.53915 0.00602 0.50798 0.24058 0.33415
AL 333w-12 1.16543 0.00374 0.27184 0.45849 0.50411
AL 333w-1a 0.71150 0.00553 0.59957 0.32997 0.37838
AL 333w-57 0.69913 0.00382 0.34153 0.26405 0.31046
AL 333w-59 0.19077 0.00285 0.94135 0.34335 0.38715
AL 333w-60 0.77945 0.00515 0.41635 0.31759 0.36561
AL 366-1 0.85189 0.00090 0.59981 0.35013 0.42788
AL 400-1a 0.72866 0.00223 0.41634 0.26509 0.38790
AL 486-1 0.97104 0.00139 0.15015 0.38916 0.44262
AL 487-1c 0.46932 0.00236 0.26690 0.36286 0.39707
LH4 0.54767 0.00163 2.40210 0.27204 0.29177
LH 15 1.07480 0.00419 0.20835 0.72182 0.87299
LH 22 0.82274 0.00319 0.59962 0.25273 0.31400

those employed in feature-based SEM microwear
analyses reported by Grine et al. (2006a,b).
All permanent molars available to us were first
examined to determine the suitability for microwear
analysis. Those that preserved wear facets were
cleaned with cotton swabs soaked in alcohol or acetone
to remove adherent dirt or preservatives. Moulds of
occlusal surfaces were then made using President Jet
Regular Body vinyl dental impression material
(Coltène-Whaledent Corp.), and casts were produced
from these molds using Epotek 301 epoxy and
hardener (Epoxy Technologies Inc.).
Replicas were examined by light microscopy and
SEM as necessary to determine the suitability for
microwear analysis following the criteria described by
Teaford (1988). Most specimens had occlusal surfaces
obscured by taphonomic damage and so had to be
excluded from this study. In the end, the molars of
only three of the Au. anamensis specimens and 19
Au. afarensis individuals available to us were found to
preserve unobscured antemortem occlusal surface
microwear. A list of all specimens considered can be
found in Grine et al. (2006a,b) and those included in
this study are presented in table 1.
All specimens included in this study were analysed
using a Sensofar Plm white-light confocal profiler
(Solarius, Inc.) with an integrated vertical scanning
interferometer. Three-dimensional point clouds were
collected for ‘phase II’ facets (the buccal occlusal sur-
faces of lower molars and the lingual occlusal surface
of uppers) using a 100 long working distance objec-
tive. The point clouds sampled elevations at intervals
of 0.18 mm along the x- and y-axes, with a vertical res-
olution of 0.005 mm. Data were obtained for four
adjacent fields on facets 9 or 10n, for a combined
Phil. Trans. R. Soc. B (2010)
work envelope of 276 mm  204 mm. The feature-
based study of these specimens reported in Grine
et al. (2006a,b) used a pixel resolution of 0.25 mm
and combined sample area of 0.04 mm2.
Resulting point clouds were analysed using TOOTH-
Frax and SFRAX scale-sensitive fractal analysis (SSFA)
software (Surfract Corp.). SSFA as applied to micro-
wear research is described in detail elsewhere (e.g.
Scott et al. 2006). The basic premise is that surface
texture varies with scale of observation, and that this
variation can be used to characterize functionally rel-
evant aspects of microwear. SSFA texture variables
included in this study are area-scale fractal complexity
(Asfc), anisotropy (epLsar), scale of maximum com-
plexity (Smc) and heterogeneity of complexity
(HAsfc). Values for individual specimens are reported
as medians of the four fields sampled for each
specimen.
Area-scale fractal complexity is a measure of change
in roughness with scale. The faster a measured surface
area increases with resolution, the more complex the
surface. Anisotropy is characterized as variation in
lengths of transect lines measured at a given scale
(we use 1.8 mm) with orientations sampled at 58 inter-
vals across a surface. An anisotropic surface will have
shorter transects in the direction of the surface pattern
than perpendicular to it (e.g. a transect that cross-cuts
parallel scratches must trace the peaks and valleys of
each individual feature). Thus, a heavily pitted surface
typically has high Asfc and low epLsar values, whereas
one dominated by homogeneous, parallel striations has
low Asfc and high epLsar values. Other variables used
to characterize microwear surface texture include
Smc, the scale range over which Asfc is calculated,
and HAsfc, variation of Asfc across a surface (in this
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3348 P. S. Ungar et al. Pliocene hominin microwear textures

Table 2. Summary statistics for early hominins.

Au. anamensis Au. afarensis Au. africanus Par. boisei Par. robustus

n 3 19 10 7 9
Asfc
mean 1.031 0.740 1.522 0.625 3.543
s.d. 0.256 0.236 0.387 0.268 1.449
epLsar
mean 0.003 0.003 0.004 0.003 0.002
s.d. 0.000 0.002 0.002 0.002 0.001
Smc
mean 0.289 0.565 1.834 0.516 0.216
s.d. 0.192 0.521 4.256 0.269 0.053
HAsfc9
mean 0.438 0.368 0.617 0.460 1.054
s.d. 0.129 0.124 0.259 0.136 0.564
HAsfc81
mean 0.713 0.461 1.004 0.621 2.101
s.d. 0.124 0.187 0.367 0.232 1.026

case, each field of view was divided into a 3  3 grid ¼
HAsfc9, and a 9  9 grid ¼ HAsfc81). High Smc values
should correspond to more complex coarse features.
High HAsfc values are observed for surfaces that vary
in complexity across a facet.
Statistical analyses focused on comparisons of micro-
wear textures of Au. afarensis with those of Au. africanus
and Par. robustus from South Africa as reported in Scott
et al. (2005) and with Par. boisei from eastern Africa as
reported by Ungar et al. (2008). Australopithecus anamen-
sis data could not be compared statistically with those of
the other hominins given an available sample of only
three specimens, although newly recovered specimens
(e.g. Haile-Selassie, this volume) hold the potential for
larger microwear datasets in the future. First, differences
in central tendencies between taxa were assessed using a
MANOVA performed on ranked data (Conover & Iman
1981) for all variables (Asfc, epLsar, Smc, HAsfc9 and
HAsfc81). Individual ANOVAs and multiple comparisons
tests were used to determine the sources of significant
variation. Both Tukey’s honestly significant difference
(HSD) and Fisher’s least significant difference (LSD)
tests were used to balance risks of type I and type II
errors (Cook & Farewell 1996). Values of p , 0.05 for
Tukey’s HSD tests may be assigned significance with
some confidence, whereas values of p , 0.05 on Fisher’s
LSD but not Tukey’s LSD tests are considered
suggestive but of marginal significance.
Degree of variance in microwear textures within
taxa may be as important for distinguishing species
as differences in central tendencies, especially given
differences in foraging and feeding strategies between
primates. With this in mind, raw data for each variable
were transformed for Levene’s test following the pro-
cedure described by Plavcan & Cope (2001) to
compare distribution variances between taxa. A
MANOVA was used to assess the variation in variance
between taxa, and as with the comparisons of central
tendencies, ANOVAs and multiple comparisons tests
were used to determine the sources of significant
variation as needed.
Complexity and anisotropy results for Au. anamensis
and Au. afarensis were also compared with those for a
Phil. Trans. R. Soc. B (2010)
series of extant primates with known differences in
feeding behaviors to put the microwear texture analysis
results for these hominins in the context of modern
primate diets. The baseline series includes: (i) the
mantled howler, Alouatta palliata and the silvered leaf
monkey, Trachypithecus cristatus, C. apella and
L. albigena from the dataset reported by Scott et al.
(2005); (ii) G. gorilla beringei, G. g. gorilla, Pan
troglodytes and the orangutan Pongo pygmaeus from
Ungar et al. (2007b); and (iii) the yellow baboon
Papio cynocephalus and the gelada baboon Theropithecus
gelada from Scott et al. (2009b). The mantled howler
and silvered leaf monkey are typically characterized
as folivores, whereas the brown capuchin and grey-
cheeked mangabey are considered to be hard-object
fallback feeders. Among the great apes, chimpanzees
are the most frugivorous, and gorillas, especially the
G. g. beringei sample considered here (the Fossey col-
lection at the US National Museum of Natural
History), are the most folivorous (see references in
Ungar et al. 2007b). Orangutans are intermediate in
their diets. Finally, geladas are specialized grass
eaters, whereas yellow baboons have a more catholic
diet including fruits, leaves and animal prey (see Post
1982; Norton et al. 1987; Dunbar 1988; Altmann
1998; Pochron 2000; Bentley-Condit 2009).
3. RESULTS
Results for Au. anamensis and Au. afarensis are presented
in tables 1–4 and are illustrated in figures 1 and 2.
(a) Comparisons with other fossil hominins
The early hominins are well-separated from one another
by microwear texture complexity. First, the specimens
from South Africa have higher Asfc values on average
than those from eastern Africa, regardless of the species
considered. Within the eastern African sample, Au. ana-
mensis may have slightly higher complexity on average
than Au. afarensis or Par. boisei, but larger samples of
Au. anamensis are really needed to evaluate this (only
one Au. anamensis specimen is outside the range of
Au. afarensis or Par. boisei). No significant variation in
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Pliocene hominin microwear textures P. S. Ungar et al. 3349

Table 3. Analyses of hominin microwear texture data (central tendencies). All data rank transformed to mitigate violation of
assumptions inherent to parametric statistics (Conover & Iman 1981). *p , 0.05 for Fisher’s LSD test, **p , 0.05 for both
Tukey’s HSD and Fisher’s LSD tests (shown in italic).

value F d.f. p-value

multivariate test results

Wilks’s l 0.037 205.783 539 0.000
Pillai trace 0.963 205.783 539 0.000
Hotelling–Lawley trace 26.382 205.783 539 0.000
ANOVA test results Asfc epLsar Smc HAsfc9 HAsfc81
F 32.397 2.735 4.056 12.096 23.204
d.f. 443 443 443 443 443
p-value 0.000 0.041 0.007 0.000 0.000
paired comparisons Asfc epLsar Smc HAsfc9 HAsfc81
Au. afarensis  Au. africanus 219.279** 26.037 21.084 215.421** 219.616**
Au. afarensis  Au. anamensis 29.579* 1.596 12.649 26.421 212.982*
Au. afarensis  Par. boisei 4.564 2.977 22.613 28.421 28.887*
Au. afarensis  Par. robustus 227.357** 13.263* 16.705** 227.088** 229.982**
Au. africanus  Au. anamensis 9.700 7.633 13.733 9.000 6.633
Au. africanus  Par. boisei 23.843** 9.014 21.529 7.000 10.729*
Au. africanus  Par. robustus 28.078* 19.300** 17.789** 211.667* 210.367*
Au. anamensis  Par. boisei 14.143* 1.381 215.262 22.000 4.095
Au. anamensis  Par. robustus 217.778** 11.667 4.056 220.667** 217.000**
Par. boisei  Par. robustus 231.921** 10.286 19.317** 218.667** 221.095**

Table 4. Analyses of hominin microwear texture data (variance). Microwear data transformed for Levene’s test (X 0 ¼ jX—
mean (X)j) following Plavcan & Cope (2001). *p , 0.05 for Fisher’s LSD test, **p , 0.05 for both Tukey’s HSD and
Fisher’s LSD tests (shown in italic).

value F d.f. p-value

multivariate test results

Wilks’s l 0.127 5.627 20 130 0.000
Pillai trace 1.254 3.837 20 168 0.000
Hotelling–Lawley trace 4.174 7.827 20 150 0.000
ANOVA test results Asfc epLsar Smc HAsfc9 HAsfc81
F 24.38 3.828 3.822 4.476 10.296
d.f. 443 443 443 443 443
p-value 0.000 0.010 0.010 0.004 0.000
paired comparisons Asfc epLsar Smc HAsfc9 HAsfc81
Au. afarensis  Au. africanus 20.140 0.000 22.087** 20.118 20.157
Au. afarensis  Au. anamensis 20.009 0.001* 0.181 20.010 0.048
Au. afarensis  Par. boisei 20.035 0.000 0.090 20.023 20.072
Au. afarensis  Par. robustus 21.078** 0.001** 0.282 20.305** 20.68**
Au. africanus  Au. anamensis 0.131 0.001 2.268* 0.107 0.205
Au. africanus  Par. bosei 0.105 0.000 2.177* 0.095 0.084
Au. africanus  Par. robustus 20.938** 0.001* 2.368** 20.187* 20.523**
Au. anamensis  Par. boisei 20.026 20.001* 20.091 20.012 20.120
Au. anamensis  Par. robustus 21.069** 0.000 0.101 20.294* 20.728**
Par. boisei  Par. robustus 21.043** 0.001** 0.191 20.282** 20.608**

complexity is noted between Au. afarensis and Par. boisei.
Within the South African sample, Par. robustus has more
complex microwear surfaces on average than Au. africa-
nus. The Par. robustus sample also shows significantly
greater variation in its complexity values than do any
of the other taxa. All other taxa have similar levels of
within-species variation in complexity.
The species do not differ as much in anisotropy as
they do in complexity, though Par. robustus has both
a lower average epLsar and less variability in this vari-
able than either Au. africanus or Au. afarensis. The
Par. robustus sample also has a lower average scale of
maximum complexity than Au. afarensis, Au. africanus
Phil. Trans. R. Soc. B (2010)
or Par. boisei, though no other significant differences in
Smc central tendencies are noted. In addition, Au. afri-
canus has significantly greater variation in Smc values
than Au. afarensis, Par. robustus and (marginally) both
Au. anamensis and Par. boisei. It should be noted
though that the high Au. africanus variance is driven
by a single outlier with an extremely high Smc value.
The Par. robustus sample also has higher average
HAsfc values than Au. anamensis, Au. afarensis, Par.
boisei or (at least marginally) Au. africanus. In addition,
Au. africanus has higher HAsfc values than Au. afaren-
sis. Further, Par. boisei has marginally lower HAsfc
values than Au. africanus, but marginally higher
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3350 P. S. Ungar et al. Pliocene hominin microwear textures
(a)
(b)
Figure 1. Photosimulations of molar microwear surfaces of
(a) Au. anamensis and (b) Au. afarensis generated from
point cloud data collected using the white-light confocal
profiler. Each image represents a surface 208 mm  280 mm.
heterogeneity (at least for HAsfc81) than Au. afarensis.
Finally, Par. robustus has more variation in its HAsfc
values than Au. anamensis, Au. afarensis, Au. africanus
and Par. boisei.
In summary, Au. afarensis microwear textures are
most similar to those of Par. boisei, with the only differ-
ence being a marginally higher average value for one of
the heterogeneity measures. Australopithecus afarensis
also has lower complexity on average and less hetero-
geneity than Au. africanus, as well as less variation in
scale of maximum complexity (though the latter
result is driven largely by a single outlier). Australo-
pithecus afarensis differs most markedly from Par.
robustus. Australopithecus afarensis has lower complexity
and heterogeneity of complexity, higher scale of maxi-
mum complexity, and marginally higher anisotropy.
The degree of variation in anisotropy values is also
greater for Au. afarensis, though the variation in com-
plexity and heterogeneity are greater in Par. robustus.
In fact, Par. robustus is very much the ‘outlier’ com-
pared with the other taxa in most cases. This
hominin tends towards a greater spread in and larger
average values for complexity, scale of maximum com-
plexity and heterogeneity of complexity, though less
spread in, and lower values for anisotropy.
Results for Au. anamensis are more difficult to have
confidence in, given its sample size, though these do sep-
arate clearly from Par. robustus. There are some
additional ‘hints’ suggested by the data if the patterns
hold with larger samples. Australopithecus anamensis has
marginally higher average complexity and lower variation
Phil. Trans. R. Soc. B (2010)
in anisotropy than either Au. afarensis or Par. boisei, as
well as marginally higher heterogeneity than Au. afaren-
sis. These results will be of limited interpretability
until larger samples are available for study.
(b) Comparisons with extant primates
Microwear complexity and anisotropy results for Au.
anamensis and Au. afarensis are illustrated alongside
data for living primates in figure 3. These hominins
are on the low end for both Asfc and epLsar, both in
their means and in their variations, when considered
in light of the extant primate baseline. The distri-
butions and central tendencies of complexity values
for these hominins are most comparable to those
reported for A. palliata, T. gelada and T. cristatus.
They lack the degrees of dispersion in Asfc seen in
the other primates, especially C. apella, P. cynocephalus
and L. albigena. In contrast, the anisotropy values
for the hominins are most different from those for
A. palliata, T. gelada and T. cristatus and are more
similar to those of the other primates, especially
P. troglodytes and P. cynocephalus.
4. DISCUSSION
(a) Microwear and the diets of Au. anamensis
and Au. afarensis
Dental microwear texture analysis results suggest that
neither the Au. anamensis nor the Au. afarensis individ-
uals included in this study had diets dominated by
hard, brittle foods in the days, weeks or perhaps even
months prior to their deaths. While these species
have been suggested to show an adaptive shift from
diets dominated by soft forest fruits to hard, brittle
foods (e.g. Ward et al. 1999; Teaford & Ungar 2000;
White et al. 2000; Wood & Richmond 2000; Walker
2002), none of the specimens examined exhibit the
high microwear surface texture complexity expected
of a hard-object feeder. The distribution of Asfc
values more closely resembles those of the grass-
eating T. gelada and the folivores A. palliata and
T. cristatus than hard-object feeding L. albigena or
C. apella.
The anisotropy results for Au. anamensis and
Au. afarensis are, on the other hand, most different
from those of A. palliata, T. cristatus and T. gelada
among the baseline series. These three extant primates
have higher average anisotropy values than the early
hominins. High anisotropy is often taken as a proxy
for tough food consumption and repetitive chew
cycles with opposing teeth moving past one another
along constrained paths. At first glance, this might
suggest that Au. anamensis and Au. afarensis specimens
sampled also avoided tough foods in the period prior
to death, although the combination of low anisotropy
and low complexity averages in Au. anamensis and
Au. afarensis is unusual for primates. Most extant pri-
mate samples published to date have either high
anisotropy averages combined with low complexity
values, associated with the consumption of tough
foods, or low anisotropy combined with high complexity
averages consistent with a hard-brittle item diet.
We propose that Au. anamensis and Au. afarensis may
have indeed consumed tough foods, but that their
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Pliocene hominin microwear textures P. S. Ungar et al. 3351

(a) 0.008
0.007

anisotropy (epLsar1.8)
0.006
0.005
0.004
0.003
0.002
0.001

0 1 2 3 4 5 6
complexity (Asfc)
(b) 4.5
heterogeneity (HAsfc81)

4.0
3.5
3.0
2.5
2.0
1.5
1.0
0.5

0 2 4 6 8 10 12 14 16
scale of maximal complexity (Smc)
Figure 2. Plots of (a) anisotropy versus complexity and (b) heterogeneity of complexity versus scale of maximum complexity
(below) for early hominin individuals considered by taxon. Open triangle, Au. afarensis; filled triangle, Au. africanus; open
circle, Par. boisei; filled circle, Par. robustus; diamond, Au. anamensis.

0.01 A. palliata G. g. gorilla

0.005
0
0.01 T. gelada G. gorilla beringei
0.005
0
0.01 T. cristatus P. troglodytes
0.005
0
0.01 Au. afarensis L. albigena
0.005
0
0.01
Au. anamensis P. cynocephalus
0.005
0
0.01 P. pygmaeus C. apella
0.005

0 5 10 15 20 0 5 10 15 20
Figure 3. Plots of anisotropy versus complexity for various extant primates, compared with data for Au. anamensis and
Au. afarensis.

anisotropy values are low because their dentognathic Kay & Hiiemae 1974), wherein food items are milled
morphology did not limit occlusal movements to the between opposing surfaces. The combination of flat
degree presumed for primates with steeper occlusal sur- teeth and tough foods would be expected to result in a
faces, such as A. palliata, T. cristatus and T. gelada. The combination of low complexity and low anisotropy.
flatter teeth of early hominins offer fewer constraints to Still, the relationship between microwear feature aniso-
masticatory movements during food fracture and may tropy and occlusal topographic relief remains to be
therefore allow ‘grinding’ action (sensu Simpson 1933; investigated fully.
Phil. Trans. R. Soc. B (2010)
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3352 P. S. Ungar et al. Pliocene hominin microwear textures
(b) Comparisons with other early hominins
Studies of craniodental functional morphology have
suggested to several researchers a tendency towards
increasing specialization for hard objects from Au.
anamensis to Au. afarensis, Au. africanus and finally
Par. robustus and Par. boisei (see White et al. 1981,
2000; Ward et al. 1999; Teaford & Ungar 2000;
Wood & Richmond 2000; Walker 2002). Australopithe-
cus africanus evinces a higher average Asfc than Au.
afarensis, and Par. robustus has an even higher average
Asfc value. The same is true for heterogeneity and vari-
ation in the scale of maximum complexity (though the
latter result appears to be driven by a single outlier).
These findings are all consistent with an increasing
component of hard, brittle items in the diet of Au. afri-
canus compared with Au. afarensis and Par. robustus
compared with Au. africanus.
On the other hand, the distribution of Asfc values
for Par. boisei is very similar to that of Au. afarensis.
Further, while the sample for Au. anamensis is too
small for a reasonable comparison with other taxa,
its mean Asfc value and heterogeneity are, if anything,
slightly higher than that of Au. afarensis. Thus, if high
texture complexity is considered to be a proxy for the
consumption of hard, brittle items, there is no evi-
dence for an increase in the role of such foods in the
diet from Au. anamensis to Au. afarensis to Par. boisei.
Ungar et al. (2008) remarked on the apparent
discordance between microwear in Par. boisei and bio-
mechanical models for this species based on
craniodental functional morphology. They proposed
that Par. boisei may represent a hominin example of
Liem’s Paradox, wherein craniodental specializations
developed as an adaptation to processing less pre-
ferred, mechanically challenging foods, even though
the microwear suggests that these hominins rarely con-
sumed such foods. This does not, however, explain
either the microwear differences between Par. boisei
and Par. robustus (given similarities in their gnathoden-
tal adaptations) or the similarities between Par. boisei,
Au. anamensis and Au. afarensis (given differences in
their gnathodental adaptations).
The story becomes even more complicated when we
consider these taxa in their presumed phylogenetic
contexts, especially the purported anagenetic lineage
leading from Au. anamensis to Au. afarensis, Par. aetho-
picus and finally Par. boisei (Kimbel et al. 2006; Rak
et al. 2007). Many workers have suggested an ances-
tor – descendant relationship between Au. anamensis
and Au. afarensis (Ward et al. 1999, 2001; White
et al. 2000, 2006; Walker 2002). Such relationships
are consistent with numerical cladistic studies (Strait
et al. 1997; Strait & Grine 2004) and with changes
in dentognathic characters among temporally succes-
sive samples from Kanapoi, Allia Bay, Laetoli and
Hadar (Kimbel et al. 2006).
Studies of cranial morphology have suggested that
the pattern of intracranial venous sinus drainage is
shared between Au. afarensis and Paranthropus species
for the exclusion of Au. africanus and Homo (Falk &
Conroy 1983; Kimbel 1984; Falk 1988), and
additional fossils have reinforced this similarity
(Kimbel et al. 2004; de Ruiter et al. 2006). Kimbel
et al. (2004) have, moreover, identified an additional
Phil. Trans. R. Soc. B (2010)
six cranial characters that Au. afarensis shares with
one or more species of Paranthropus, although they
regarded them, like the pattern of intracranial venous
drainage, as being homoplastic. Most recently, simi-
larities in ramal morphology between Au. afarensis
and Par. robustus mandibles have been observed by
Rak et al. (2007), who interpreted them as synapomor-
phies, suggesting that Au. afarensis and Par. robustus are
united in a single clade and that this possibly includes
Par. aethiopicus and Par. boisei, although no fossils
attributable to the latter two species preserve the rel-
evant anatomy. The evidence suggesting an
ancestor – descendant relationship between Au. afaren-
sis and Paranthropus, and particularly that for an Au.
afarensis – Par. aethiopicus – Par. boisei lineage in eastern
Africa, is not wholly inconsistent with their hypoth-
esized cladistic relationships (Strait et al. 1997;
Kimbel et al. 2004; Strait & Grine 2004).
Similarities in microwear texture results for Au.
anamensis, Au. afarensis and Par. boisei may make
sense if these taxa comprise an anagenetic lineage
and all shared food-type preferences. One possible
scenario might be increasing craniodental specializ-
ations through the lineage for repetitive loading given
consumption of tough foods in the face of morphologi-
cal constraints imposed by relatively flat cheek teeth.
This would be consistent with a C4 isotope signature
in Par. boisei (van der Merwe et al. 2008) and the con-
sumption of tough grasses or sedges, assuming that the
specimens examined thus far are representative.
Carbon stable isotope studies of Au. anamensis, Au.
afarensis and additional Par. boisei specimens would
provide a valuable test of this hypothesis.
On the other hand, if Par. boisei and Par. robustus
form a clade excluding Au. africanus, the two early
hominins from South Africa probably independently
increased their consumption of hard, brittle foods as
evidenced by increased pit percentages in both homi-
nins. In any case, the microwear texture patterns of
the eastern African early hominins are more similar
to one another than to those of the South African
early hominins, independent of whether one is
considering Australopithecus or Paranthropus.
So in the end, what can be said of the microwear of
Au. anamensis and Au. afarensis? We may reasonably
infer that specimens examined for this study did not
have a diet dominated by hard and brittle foods, at
least shortly before death. Picq (1990) proposed that
Au. afarensis often consumed soft foods that were not
fracture resistant, but had craniomandibular adap-
tations for seasonal consumption of hard, brittle
foods. Grine et al. (2006a,b) further suggested that tra-
ditional microwear results for both Au. anamensis and
Au. afarensis are best explained by food preferences
for less mechanically challenging foods, though as
Ungar (2004) noted, their occlusal morphology
would have allowed the consumption of hard, brittle
items in times of dietary stress when favored foods
were unavailable. The microwear texture analysis
data presented here cannot be used to falsify the
notion of rare hard-object feeding, but it also provides
no evidence for it. Whether or not the craniodental
specializations seen in Au. anamensis and Au. afarensis
are adaptations for the occasional consumption of
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Pliocene hominin microwear textures
hard, brittle foods, however, their microwear texture
patterns are consistent with the regular consumption
of softer and or tougher items.
We are grateful to curators at the National Museums of
Ethiopia, Kenya and Tanzania for permission to examine and
make moulds of specimens in their care and thank Alejandro
Peréz-Peréz for his assistance with preparing these replicas.
Kristin Krueger helped with the preparation of figure 1. This
study was funded by the US National Science Foundation.
ENDNOTE
1
One of us (F.E.G.) prefers the nomen Praeanthropus afarensis, as use
of the generic name Australopithecus for Au. anamensis and Au. afar-
ensis probably violates the criterion of monophyly (Grine & Strait
2000). Because of the lack of consensus among the authors on the
taxonomy of these hominins, we employ here the more commonly
used nomenclature.
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Phil. Trans. R. Soc. B (2010) 365, 3355–3363

doi:10.1098/rstb.2010.0086

An enlarged postcranial sample confirms

Australopithecus afarensis dimorphism
was similar to modern humans
Philip L. Reno1,*, Melanie A. McCollum3,4, Richard S. Meindl2,3
and C. Owen Lovejoy2,3,*
1
Department of Developmental Biology, Stanford University School of Medicine, 279 Campus Drive,
Beckman 300, Stanford, CA 94305-5329, USA
2
Department of Anthropology, and 3School of Biomedical Sciences, Kent State University,
Lowry Hall Room 226, Kent, OH 44242-0001, USA
4
Department of Cell Biology, University of Virginia, Charlottesville, VA 22902, USA
In a previous study, we introduced the template method as a means of enlarging the Australopithecus
afarensis postcranial sample to more accurately estimate its skeletal dimorphism. Results indicated
dimorphism to be largely comparable to that of Homo sapiens. Some have since argued that our
results were biased by artificial homogeneity in our Au. afarensis sample. Here we report the results
from inclusion of 12 additional, newly reported, specimens. The results are consistent with those of
our original study and with the hypothesis that early hominid demographic success derived from a
reproductive strategy involving male provisioning of pair-bonded females.
Keywords: A.L. 333; taphonomy; monogamy; skeletal dimorphism; modelling

1. INTRODUCTION Any given assemblage of Au. afarensis fossils was

Accurately inferring early hominid sexual dimorphism
is an important element in interpreting their paleobiol-
ogy. We previously concluded that skeletal size
dimorphism in Australopithecus afarensis was signifi-
cantly lower than that of gorillas and could not be
statistically distinguished from that of modern
humans (Reno et al. 2003, 2005). These findings,
which contrast with previous assessments (Zihlman &
Tobias 1985; McHenry 1991; Lockwood et al. 1996),
were achieved through the use of the ‘template
method’. This method relied on the A.L. 288-1 partial
skeleton (‘Lucy’), as a source of simple ratios between
femoral head diameter (FHD) and other skeletal
dimensions. These ratios were then used to obtain
estimates of FHD for skeletal dimensions that were
also measurable in A.L. 288-1. Postcranial variation
within the (thus maximized) Au. afarensis sample
from the Middle Awash region of Ethiopia (‘Com-
bined Afar’, CA) and that within the temporally and
geographically constricted Au. afarensis sample from
Afar Locality 333 were then compared with boot-
strapped samples of modern humans, chimpanzees
and gorillas. This method was specifically designed
to overcome problems inherent in calculating sexual
dimorphism from a small number of specimens
whose sexes must be judged a priori on the basis of
size (e.g. Zihlman & Tobias 1985; McHenry 1991).
* Authors for correspondence (preno@stanford.edu; olovejoy@aol.
com).
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
formed by a combination of random sampling and var-
ious taphonomic processes. The effect of these
processes on sample variation can be modelled by
bootstrapping from taxa of known dimorphism.
Humans (Homo sapiens), chimpanzees (Pan troglodytes)
and gorillas (Gorilla gorilla) represent the three genera
most closely related to early hominids and essentially
encompass the entire range of primate skeletal sexual
dimorphism. Because the sex of any Au. afarensis
element is essentially unknown, sampling with regard
to sex of extant taxa is allowed to vary freely. That is,
the sex ratio in each iteration is allowed to vary by
simple probability (i.e. the binomial expansion). In
sufficiently small samples, this can occasionally result
in samples composed of only one sex. In order to
simulate the Au. afarensis assemblages as precisely as
possible (and limit the variation introduced by
sampling different anatomical locations), bootstrapped
samples of living hominoids were required to exactly
match the anatomical compositions of the A.L. 333
and the CA samples (e.g. the number of proximal
tibias included in each bootstrapped sample was
required to exactly match the number of proximal
tibias represented in the Au. afarensis sample being
simulated). For each iteration, each postcranial
metric was converted to a FHD based on ratios calcu-
lated from a template specimen that was also randomly
chosen to serve as the equivalent of A.L. 288-1.
A.L. 333 probably represents a simultaneous
death assemblage (White & Johanson 1989;
Behrensmeyer et al. 2003). In our previous analysis
(Reno et al. 2003), two separate simulations of A.L.
333 were generated. In one, each of 22 postcranial

3355 This journal is q 2010 The Royal Society

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3356 P. L. Reno et al. Au. afarensis skeletal dimorphism
metrics preserved at the site was randomly drawn from
our complete samples of extant taxa (N  50). This
exactly modelled A.L. 333 in being composed of as
many as 22 separate individuals. However, it is unli-
kely that each A.L. 333 specimen in fact represents
one of 22 different individuals. Based on mandibular
dentitions, the minimum number of individuals
(MNI) at the site is nine (White & Johanson 1989).
Therefore, in a second simulation, we randomly
selected nine individuals to serve as the source of all
22 metrics. This ensures that many individuals are
multiply represented in the sample of metrics. Our
procedures assume only that each ‘death’ assemblage
(fossil sample or extant simulation) was a random
sample of its parent population—the biological species
from which each was derived (i.e. Au. afarensis,
H. sapiens, P. troglodytes and G. gorilla).
These samples have been challenged as not being
representative of the Au. afarensis size distribution
(Plavcan et al. 2005; Scott & Stroik 2006). The ration-
ale has been that because ‘Lucy-sized’ individuals
are absent from the A.L. 333 assemblage, it must
over-sample large, presumably male, adult individuals.
If true, then our lower estimates of skeletal dimorph-
ism in A.L. 333 may have been flawed by biased
sampling during the accumulation, fossilization and/
or recovery of the assemblage.
This argument is now subject to a simple test.
Additional postcranial elements of Au. afarensis have
now been reported for both A.L. 333 and other
Middle Awash localities (Kimbel et al. 2004; Drapeau
et al. 2005; Harmon 2006). Inclusion of these
additional 12 specimens raises our postcranial
sample to 41 and more than doubles the number of
individuals represented from non-A.L. 333 localities.
This expanded sample provides an opportunity
to more accurately assess size dimorphism in
Au. afarensis and determine whether smaller Lucy-
sized individuals were disproportionately lacking
from A.L. 333.
2. MATERIAL AND METHODS
In addition to the 29 fossil specimens in our original
study (Reno et al. 2003), we have now added four
specimens from A.L. 333 and eight from other
Middle Awash localities (Kimbel et al. 2004; Drapeau
et al. 2005; Harmon 2006; table 1). Metrics from these
specimens (some as yet undescribed), as well as their
homologues from the A.L. 288-1 partial skeleton,
were provided by William Kimbel.
Details of the template method and our bootstrap-
ping procedures are described in Reno et al. (2003,
2005). Since those publications, we have observed
that the template method yields extreme FHD esti-
mates in rare cases where a small or large skeletal
metric is paired with a template specimen with an unu-
sual metric to FHD ratio (all within the bounds of
natural variation). While such pairings are infrequent,
they nevertheless have the potential to confound
results by artificially inflating dimorphism statistics in
extant samples. As a means of correcting bias from
such cases, we now systematically discard estimated
FHDs that are more than 10 mm above or below the
Phil. Trans. R. Soc. B (2010)
observed range of the extant taxon being sampled. How-
ever, this correction is potentially quite conservative as
the relative size range of many metrics is actually
greater than that of FHD (see below).
The three bootstrap simulations reported here were
performed separately to model the following enlarged
Au. afarensis samples: (i) 26 specimens from the A.L.
333; (ii) 15 non-333 specimens from other Hadar
localities and Maka; and (iii) 41 specimens in the
CA sample. The 15 specimens in the non-333
sample must represent 15 separate individuals. There-
fore, 15 metrics were each randomly drawn from the
entire chimpanzee, human or gorilla samples. In con-
trast, it is unlikely that 26 different individuals
contributed to the A.L. 333 sample. Therefore, for
each iteration, a separate random subsample of nine
chimpanzee, human or gorilla individuals (based
upon an MNI from mandiblar dentitions (White &
Johanson 1989)) served as the pool from which 26
metrics were then drawn. For the CA simulations, a
‘hybrid’ was created for each iteration in which 26
metrics representing A.L. 333 were sampled from
nine randomly selected individuals. These were com-
bined with an additional 15 drawn from the entire
sample to represent non-333 individuals.
Plavcan et al. (2005) argued that only five to eight
individuals contributed to the A.L. 333 postcranial
sample, and it is certainly hypothetically possible that
some of the (at least) nine known adult individuals
did not contribute to the postcranial sample. However,
our simulations already permit sampling of fewer than
nine individuals because not all nine individuals
selected for each iteration are necessarily randomly
sourced for the 26 metrics used to simulate
A.L. 333. Therefore, it was unnecessary to perform
additional simulations from isolated comparative
samples artificially restricted to less than nine potential
contributors.
Both the coefficient of variation (CV) and the bino-
mial dimorphism index (BDI) were calculated in each
simulation. The CV was calculated using the small
sample correction (Sokal & Rohlf 1995). The BDI
was defined specifically for the calculation of sexual
dimorphism in samples of unknown sex. It rests
upon three assumptions: (i) both sexes are present in
each sample; (ii) every specimen has an equal prob-
ability of being male or female, but (iii) when any
two specimens are potentially of a different sex, the
larger is always male. Using this algorithm, a sample
of n yields a total of n 2 1 possible sex allocations
and therefore n 2 1 skeletal dimorphism estimates.
The BDI is then the weighted average of the n 2 1
dimorphism values based on the probability of each
sex allocation occurring under the binomial expansion.
Note that in light of the assumption that males are
always larger than females, the BDI tends to overesti-
mate dimorphism in minimally dimorphic species.
Two estimates of dimorphism (actual DM: male
mean/female mean based on known sex) were calcu-
lated for each extant sample drawn. The first used
estimated FHD dimensions estimated for each speci-
men by the template method (template sexual
dimorphism: TSD) to measure dimorphism, and the
second used the original FHDs for each randomly
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Au. afarensis skeletal dimorphism P. L. Reno et al. 3357

Table 1. Australopithecus afarensis sample used for simulations.

estimated estimated FHD/GMEAN

metric specimen(s) FHD GMEAN ratio

HHD: max. diameter of humeral head A.L. 333-107a 39.4 32.6 1.21
OLCB: ML width of humerus measured tangent to the A.L. 137-48A 32.6 27.0 1.21
superior margin of the olecranon fossa A.L. 137-50b 38.3 31.6 1.21
A.L. 223-23b 35.3 29.2 1.21
A.L. 322-1 27.9 23.1 1.21
A.L. 333-29 33.2 27.4 1.21
A.L. 333w-31 34.3 28.4 1.21
Mak VP 1/3 37.8 31.3 1.21
CAPD: max. diameter of capitulum A.L. 333w-22 39.5 32.7 1.21
A.L. 444-14b 37.2 30.4 1.22
RHD: max. diameter of the radial head A.L. 333x-14c 44.3 36.6 1.21
A.L. 333x-15c 44.5 36.8 1.21
ULB: ML width of ulna immediately distal to radial A.L. 333x-5 37.1 30.6 1.21
facet A.L. 333w-36 29.8 24.6 1.21
A.L. 438-1ab 40.9 33.8 1.21
FHD: max. diameter of femoral head A.L. 152-2b 33.1 27.4 1.21
A.L. 288-1ap 28.6 23.6 1.21
A.L. 333-3 40.9 33.8 1.21
A.L. 827b 38.1 31.5 1.21
TRCD: max. femoral shaft diameter immediately below A.L. 211-1 36.4d 30.1 1.21
lesser trochanter A.L. 333-95c 35.3d 29.1 1.21
Mak VP 1/1 34.4d 28.4 1.21
FNKH: femoral neck height normal to long axis at A.L. 333-117 38.7 32.0 1.21
midpoint A.L. 333-123b 33.0 27.2 1.21
A.L. 333-142b 30.1 24.8 1.21
GSTB: AP femoral width immediately above A.L. 333-4 35.2 29.1 1.21
gastrocnemius tubercles A.L. 333w-56 33.6 27.8 1.21
A.L. 333-140b 30.2 24.9 1.21
CNDC: ML distance between centers of medial and A.L. 129-1b 27.9 23.0 1.21
lateral tibial condyles A.L. 333x-26 38.5 31.8 1.21
A.L. 333-42 36.7 30.3 1.21
PRXTB: max. ML tibial bicondylar breadth A.L. 330-6b 37.4 30.9 1.21
DSTTB: AP articular length at ML mid-point of A.L. 333-6 37.2 30.8 1.21
articular surface of distal tibia A.L. 333-7 42.9 35.5 1.21
A.L. 333-96 38.4 31.7 1.21
A.L. 545-3b 31.9 26.1 1.22
FIBD: max. ML diameter of distal fibula A.L. 333-9A 42.8 35.4 1.21
A.L. 333-9B 38.9 32.1 1.21
A.L. 333w-37 37.8 31.3 1.21
A.L. 333-85 40.6 33.5 1.21
TAL: max. AP length of talus A.L. 333-147b 36.0 29.8 1.21
a
Because of slight eccentricity in this specimen the average of the mediolateral (ML) and anteroposterior (AP) diameters was used instead.
b
Specimens new to this analysis.
c
These specimens lack epiphyseal fusion and are not strictly adults. They were included because they constitute three of the largest fossils
in the sample and their omission would further decrease fossil dimorphism estimates.
d
These values are based on a slightly different metric than the one used in the previous analysis (AP subtrochanteric diameter reported by
Lovejoy et al. (1982)) and therefore differ from those reported in Reno et al. (2003). The new metric corresponds more closely with that
taken from the comparative samples and better reflects the relative size of these specimens (i.e. 333-3 is clearly larger than any of these
three specimens).

selected individual (direct sexual dimorphism: DSD)
to determine it. Comparison of TSD and DSD
assesses the effect of using a template specimen to esti-
mate dimorphism. Because calculation of dimorphism
statistics (BDI and CV) for Au. afarensis requires use
of a template specimen (A.L. 288-1), these can be
assessed only by comparison with TSD produced by
the simulations.
3. RESULTS
Table 1 lists each Au. afarensis specimen used in the
current analysis, the metric from which its FHD was
calculated using the template (A.L. 288-1) and the
resulting estimated FHD. Also included in table 1
are estimated geometric means (GMEAN) of all
included metrics that could also be calculated by the
template method in addition to the FHD. These are
included to illustrate that the results of the template
method do not depend on the choice of FHD to
measure sample dimorphism. Note that ratios between
estimated FHD and estimated GMEAN are always
identical. Thus, any measure of sample variation
(i.e. CV or BDI) will be identical and any scalar
metric from the template will produce the same
result. Therefore, any species-specific allometric

Phil. Trans. R. Soc. B (2010)


3358 P. L. Reno et al.
50
45
estimated femoral head diameter (mm)
40
35
30
25
20
A.L. 333
Figure 1. Estimated FHD for individual Au. afarensis speci-
mens included in this analysis. Circles, original specimens;
triangles, specimens new to this analysis.
relationships with FHD have no effect on the outcome
of the procedure.
Estimated FHDs for each of the original 29 speci-
mens of Reno et al. (2003) plus the 12 additional
specimens included in the present analysis are shown
in figure 1. As it demonstrates, the new specimens
increase representation of small individuals at A.L.
333 but not to the extreme range represented by the
smallest individuals of the non-333 sample. On the
other hand, the new specimens expand the upper
size range of the non-333 sample (although not to
the extent observed in A.L. 333) and appreciably
increase the representation of intermediate-sized
individuals in the non-333 sample such that there is
no longer any potential demarcation between large
and small specimens in the combined CA sample.
These novel specimens provide little reason to con-
clude that A.L. 333 under-represents small Lucy-
sized individuals. To the contrary, given the large
number of intermediate-sized specimens, it is quite
possible that such extremely small individuals may
actually be over-represented in the non-333 sample.
Table 2 presents samples sizes, CVs, actual DM and
the BDI for each metric. Dimorphism in humans is
intermediate between non-dimorphic chimpanzees
and highly dimorphic gorillas for nearly all characters
(only the chimpanzee capitulum (CAPD) BDI and
CV are slightly greater than humans). However,
within each taxon, the extent to which skeletal
metrics differ between the sexes varies extensively.
Significantly, variation in FHD in all three hominoid
taxa is low in comparison to that observed for most
other skeletal metrics (thus, FHD will have a smaller
relative range). Given these findings, the template
method can be expected to overestimate the means
and dispersions of direct dimorphism values.
Although the BDIs correlated well with the actual
dimorphism observed for each metric, they tended
Phil. Trans. R. Soc. B (2010)
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Au. afarensis skeletal dimorphism
non-333
to overestimate size dimorphism in the minimally
dimorphic species (compare values in chimpanzees
and gorillas; table 2). As noted above, this is an
expected finding because males are always assumed
to be larger than females.
Frequency histograms of dimorphism values gener-
ated by simulating the A.L. 333, CA and non-333
samples are provided in figure 2. As expected,
human dimorphism values were found to be inter-
mediate between those of chimpanzees and gorillas.
Also as expected (see discussion above), template-
derived size dimorphism statistics tended to
overestimate direct dimorphism values (table 3). For
each iteration, a Pearson correlation coefficient was
computed between the resulting template-derived
estimated FHDs and the directly measured FHDs.
The means and standard deviations of these corre-
lation coefficients for all simulations are presented in
table 4. The strength of the correlation between
template and direct values varied among species as a
direct consequence of their relative dimorphism. As
expected, in non-dimorphic chimpanzees, the error
in estimating FHD was relatively high compared with
the size range of the species. In contrast, in highly
dimorphic gorillas, it was relatively low. The patterns
of correlation observed between template FHD and
direct FHD in the extant taxa verify that the template
method satisfactorily reflects actual dimorphism levels
in these samples.
As in our original analysis, BDI and CV calculated
for Au. afarensis were most similar to those of humans
(figure 2). This was true not only of the A.L. 333 and
CA samples, but also for the non-333 sample.
Table 5 presents exact counts of the number of
iterations that fell above or below the Au. afarensis
value in each simulation. As these data demonstrate,
dimorphism within the expanded A.L. 333 sample
increased from a BDI of 1.167 in our previous analy-
sis to a value of 1.195 here, which places Au. afarensis
dimorphism in the middle of the distribution of
human values. However, because of its small sample
size (modelled as representing nine individuals), it is
statistically indistinguishable from any of the three
hominoids.
Unlike the results for A.L. 333, dimorphism within
the expanded CA sample decreased from a BDI of
1.222 in our original study to 1.209 here, a value
that is significantly different from that of both the
extremely dimorphic gorillas and the minimally
dimorphic chimpanzees. The slightly higher dimorph-
ism value of 1.213 calculated for the non-333 sample
also differed significantly from that of gorillas using a
directional test (which is appropriate considering
gorillas set the upper range of primate dimorphism).
Because of its reliance on estimated rather than
actual FHDs, the template method contributes an
additional source of error to estimates of dimorphism.
In order to ensure that this error is not a function of
the size of the template specimen—a potential concern
given the unusually small size of A.L. 288-1—we com-
pared dimorphism values generated by different sized
templates. Template size has no systematic effect
(figure 3), and therefore our results are not biased by
the small size of A.L. 288-1.
Phil. Trans. R. Soc. B (2010)
Table 2. Sample sizes and dimorphism statistics for individual metrics measured directly from chimpanzee, human and gorilla specimens. Metrics are explained in table 1.

species HHD OLCB CAPD RHD ULB FHD TRCD FNEKH GSTB CNDC PRXTB DSTTB FIBD TALUS GMEAN

chimpanzees
male (n) 23 23 23 22 23 23 23 23 23 23 23 23 22 19 18
female (n) 25 25 25 25 25 25 25 25 25 25 25 25 25 24 24
CV 6.64 9.42 9.49 6.65 9.03 6.48 7.80 7.27 7.31 7.40 5.98 8.20 6.72 6.23 5.32
actual DM 1.066 1.073 1.090 1.038 1.059 1.049 1.054 1.032 1.029 1.036 1.041 1.003 1.052 1.029 1.043
BDI 1.115 1.163 1.165 1.113 1.155 1.114 1.133 1.123 1.126 1.127 1.103 1.147 1.110 1.106 1.093
difference 0.049 0.090 0.075 0.075 0.096 0.065 0.079 0.091 0.097 0.091 0.062 0.144 0.058 0.077 0.050
humans
male (n) 25 25 25 25 25 25 25 25 25 25 25 25 25 25 25
female (n) 25 25 25 25 25 25 25 25 25 25 25 25 25 25 25
CV 8.92 11.08 9.17 8.87 13.07 8.81 9.64 11.00 8.67 10.17 7.73 12.07 9.67 8.02 8.02
actual DM 1.170 1.176 1.124 1.151 1.203 1.157 1.142 1.178 1.100 1.173 1.134 1.183 1.116 1.135 1.151
BDI 1.169 1.202 1.161 1.160 1.237 1.161 1.165 1.199 1.151 1.186 1.140 1.214 1.166 1.141 1.153
difference 20.001 0.026 0.037 0.009 0.034 0.004 0.023 0.021 0.051 0.013 0.006 0.031 0.050 0.006 0.002
gorillas
male (n) 24 25 25 24 25 25 25 25 25 25 25 25 23 21 19
female (n) 25 25 25 25 25 25 25 25 25 25 25 25 25 22 22
CV 14.92 18.09 15.02 14.60 16.74 12.66 12.66 14.00 14.98 14.23 13.62 13.80 16.06 10.98 13.29
Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

actual DM 1.325 1.390 1.300 1.296 1.324 1.258 1.225 1.258 1.297 1.275 1.279 1.257 1.330 1.208 1.279
BDI 1.305 1.378 1.297 1.290 1.324 1.252 1.242 1.268 1.299 1.284 1.271 1.259 1.325 1.208 1.264
Au. afarensis skeletal dimorphism

difference 20.020 20.012 20.003 20.006 0.000 20.006 20.003 0.010 0.002 0.009 20.008 0.002 20.005 0.000 20.015
P. L. Reno et al.
3359
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3360 P. L. Reno et al. Au. afarensis skeletal dimorphism

(a) 300
1.195 11.23
250
A.L. 333 200
150
100
50
0
(b) 300
1.209 11.89
Combined Afar

250
200
150
100
50
0
1.05 1.10 1.15 1.20 1.25 1.30 1.35 1.40 1.45 1.50 1.55 1.60

(c) 300
1.213 12.03
250
200
non-333

150
100
50
0
1.05 1.10 1.15 1.20 1.25 1.30 1.35 1.40 1.45 1.50 1.55 1.60 4 6 8 10 12 14 16 18 20 22 24 26 28
BDI CV

Figure 2. Frequency histograms of dimorphism values generated by simulating the (a) A.L. 333, (b) Combined Afar and
(c) non-333 assemblages using chimpanzee (white bars), human (grey bars) and gorilla (black bars) comparative samples
(1000 iterations each). The vertical line in each plot indicates dimorphism for the Au. afarensis sample.

Table 3. Summary statistics from each of the extant hominoid simulations.

chimpanzee human gorilla

TSD DSD TSD DSD TSD DSD

A.L. 333 simulation: 1000 iterations

actual DM
mean 1.045 1.053 1.152 1.160 1.290 1.258
s.d. 0.050 0.046 0.052 0.040 0.060 0.046
BDI
mean 1.155 1.102 1.198 1.140 1.272 1.206
s.d. 0.029 0.027 0.037 0.036 0.053 0.051
CV
mean 9.29 6.05 11.50 8.21 14.94 11.78
s.d. 1.59 1.31 1.90 1.74 2.26 2.07
Combined Afar simulation: 1000 iterations
actual DM
mean 1.049 1.051 1.155 1.159 1.297 1.258
s.d. 0.036 0.030 0.038 0.026 0.041 0.029
BDI
mean 1.162 1.108 1.203 1.150 1.292 1.227
s.d. 0.025 0.014 0.031 0.025 0.037 0.032
CV
mean 9.52 6.24 11.55 8.50 15.49 12.21
s.d. 1.33 0.82 1.54 1.16 1.54 1.18
non-A.L. 333: 1000 iterations
actual DM
mean 1.057 1.050 1.162 1.156 1.305 1.258
s.d. 0.053 0.033 0.054 0.029 0.061 0.032
BDI
mean 1.161 1.107 1.194 1.148 1.294 1.223
s.d. 0.037 0.019 0.042 0.025 0.052 0.033
CV
mean 9.67 6.43 11.36 8.67 16.14 12.54
s.d. 2.00 0.94 2.18 1.29 2.31 1.39

Phil. Trans. R. Soc. B (2010)

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Table 4. Means and standard deviations of the correlations
between actual and estimated FHD computed for each of
the 1000 iterations.
chimpanzee human
A.L. 333
mean 0.453 0.620
s.d. 0.179 0.145
Combined Afar
mean 0.498 0.642
s.d. 0.132 0.102
non-333
mean 0.565 0.675
s.d. 0.190 0.147
4. DISCUSSION
The present study is based on dimorphism estimates
generated from 41 fossils representing a minimum of
20 separate individuals. While we look forward to the
potential of adding more fossils when available, it is
likely that the sample is now reaching a ‘critical
mass’ such that additional specimens are unlikely to
appreciably change the dimorphism estimates. Results
confirm our previous conclusions that dimorphism is
only minimal to moderate in Au. afarensis. Skeletal
variation in the CA sample differs significantly from
those of gorillas and chimpanzees but cannot be stat-
istically distinguished from that of modern humans
(table 5). Significantly, the dimorphism values calcu-
lated for the non-333 sample demonstrate that the
results obtained for the combined sample are not
biased in any way by the composition of A.L. 333, a
finding that renders moot all criticisms of our original
study which relied on this argument (i.e. Plavcan et al.
2005; Scott & Stroik 2006). Incorporation of four
additional individuals of small to intermediate body
size did indeed increase the dimorphism in the A.L.
333 sample, just sufficient to prevent statistical signifi-
cance in its difference from gorillas (table 5). However,
as is confirmed by both the lower dimorphism values
actually calculated for this sample (figure 2), and the
nearly equivalent ranges of variation observed between
the A.L. 333 and non-333 samples (figure 1), this
finding reflects A.L. 333’s small sample size (n ¼ 9),
as sample size has a profound impact on adequately
inferring dimorphism (Koscinski & Pietraszewski
2004). Indeed, the A.L. 333 locality, which represents
one of the most complete and taphonomically
unbiased hominid sites ever found, still probably pro-
vides the most accurate sample of Au. afarensis
dimorphism. It should also be noted, in addition,
that an upper limit to dimorphism within this species
is set by combining specimens from geographically
and temporally distinct sites (i.e. the total CA
sample), as this practice must enhance the variance
beyond that typical of local demes.
The inclusion of new specimens also reinforces the
fact that, while A.L. 333 preserves a number of large
specimens, and multiple small individuals have been
recovered from non-333 localities, the majority of
Au. afarensis specimens are intermediately sized
(figure 1). It is thus also noteworthy that the CA
Phil. Trans. R. Soc. B (2010)
Au. afarensis skeletal dimorphism P. L. Reno et al. 3361
sample, which includes both large and small size
extremes, can reject both low chimpanzee and high
gorilla-like dimorphism. This also stresses the need
to maximize sample size to include the numerous
gorilla intermediate sized specimens, as this tends to ensure
that more complete yet extreme-sized individuals (i.e.
0.819
A.L. 288-1, A.L. 128/129 and A.L. 333-3) do not
0.087 unduly influence dimorphism estimates (e.g. Gordon
et al. 2008).
0.831 It is clear that our method of assessing skeletal
0.056 dimorphism within the A.L. 333 assemblage is appro-
priate regardless of any sex bias due to sampling error
0.832
(e.g. as argued by Plavcan et al. (2005) and Scott &
0.091 Stroik (2006)). Moreover, the presence of small juven-
ile specimens preserved at A.L. 333 suggests that no
systematic size sorting occurred during the formation
of the assemblage. As noted above, because the sex
of each postcranial element in the Au. afarensis
sample is unknown, the numbers of males and females
included within the bootstrapped samples were
allowed to vary freely. Therefore, the bootstrapped
simulations produced all possibilities with respect to
sex composition. Indeed, some of our simulations gen-
erated samples containing only one sex.
That Au. afarensis displayed only moderate size
dimorphism is consistent with the minimal size
dimorphism observed in Ardipithecus ramidus (Suwa
et al. 2009; White et al. 2009). Indeed, given the
absence of appreciable skeletal size dimorphism in
both Pan and Ardipithecus, there is now strong evi-
dence that the last common ancestor of
chimpanzees, bonobos and humans also displayed
minimal skeletal dimorphism and that it probably
increased in hominids subsequent to 4.4 Ma.
Recently, Lawler (2009) established that ecological
factors (e.g. substrate preference or feeding niche)
often produce dimorphism ratios that differ substan-
tially from those predicted by simple sexual selection
theory (e.g. the ‘tournament sex’ of Devore & Lovejoy
(1985)). Lovejoy (1981, 1993, 2009) has argued that a
provisioning model favours the selection of large males
by females because greater body mass increases both
mobility and predator resistance in males. Also, selec-
tion of small females by males reduces that female’s
fat/protein requirements and thereby lowers compe-
tition with the male’s offspring for nutrient-rich
foods. In addition, the obviously minimal intermale
aggression in Ar. ramidus, as now established by the
multiple trait shifts in its sectorial canine complex
(including those of size, crown form, eruption time
and upper/lower canine differences (Suwa et al.
2009; White et al. 2009)), makes it even more unlikely
that extreme dimorphism would evolve so rapidly in
Au. afarensis via direct male – male competition for
mates. Instead, moderate dimorphism appears to be
an ecologically driven feature in the hominid lineage
that probably continued into later taxa (i.e. Au. africa-
nus (Harmon 2009)), and although most probably the
result of sexual selection, it was probably not driven by
direct male – male agonistic competition for mates, but
rather by ecologically driven male and female choice.
Indeed, it would seem that there are now two compet-
ing explanations for the increase in skeletal dimorphism
from 4.4 Ma (Ar. ramidus, White et al. 2009) to 3.2 Ma
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3362 P. L. Reno et al. Au. afarensis skeletal dimorphism

Table 5. Simulations of Au. afarensis dimorphism from three different fossil assemblages. These are exact counts of
values that fall less than or greater than the Au. afarensis value. Each count can be transformed into a proportion by dividing
by 1000.

chimpanzee human gorilla

fossil assemblage
dimorphism less than greater than less than greater than less than greater than

A.L. 333
BDI 1.195 905 95 484 516 74 926
CV 11.23 878 122 447 553 51 949
Combined Afar
BDI 1.209 960 40 607 393 8 992
CV 11.89 954 46 597 403 7 993
non-333
BDI 1.213 916 84 698 302 50 950
CV 12.03 870 130 627 373 35 965

1.5 30
chimpanzee 25 chimpanzee
1.4
1.3 20
BDI

CV
15
1.2 10
1.1 5
1.0 0

1.5 30
human 25 human
1.4
1.3 20
BDI

CV

15
1.2 10
1.1 5
1.0 0

1.5 gorilla 30 gorilla

1.4 25
1.3 20
BDI

CV

15
1.2 10
1.1 5
1.0 0
template specimen by increasing FHD template specimen by increasing FHD

Figure 3. Box and whisker plots showing range of sample dimorphism values generated for each template specimen. Template
specimens are arrayed by increasing FHD. Boxes indicate interquartile range, whiskers 95% interval; circles are outliers.

(A.L. 333, Kimbel et al. 1994): (i) an increase in
male – male agonism for mate selection or (ii) the
enhancement of male resistance to predation in
response to occupation of novel environments by the
more ecologically expansive Australopithecus radiation,
including the invasion of new predator-rich environ-
ments such as lake margins, savannas and veldts.
Given that the former of these two choices would
likely depress sub-adult survivorship and increase
parenting load on females, when coupled with the
now clear adaptive radiation of Australopithecus that
followed Ar. ramidus, the latter of these two seems
far more likely.
5. CONCLUSIONS
The template method is a robust technique for esti-
mating size variance in early hominids and is the
only method currently available with which sample
sizes sufficient for statistical reliability are likely to be
generated from rare early hominid fossils. It should
be noted, moreover, that this method is fully appli-
cable to other species of fossil hominoids, so long as
a partial skeleton and a sufficiently large series of unas-
sociated fossils with homologous anatomical sites are
available (e.g. Proconsul (Walker & Teaford 1989;
Ward et al. 1993), Ar. ramidus (White et al. 2009)
and Au. africanus (Clarke 1999)). For South African
Australopithecus, however, special consideration of
taphonomic variables will have to be made, since
cave assemblages are probably the result of carnivore
kills (Brain 1981). Because no specific size-sorting
mechanism has been identified for A.L. 333, this site
remains an appropriate venue for examination of skel-
etal dimorphism in Au. afarensis.
We thank Yohannes Haile-Selassie of the Cleveland Museum
of Natural History for access to primate skeletons and to
Lyman Jellema for technical assistance. William Kimbel

Phil. Trans. R. Soc. B (2010)

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Au. afarensis skeletal dimorphism
kindly provided metrics to unpublished fossil specimens. We
also thank Alan Walker and Chris Stringer for organizing the
discussion meeting and the staff of the Royal Society for
ensuring its success.
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Phil. Trans. R. Soc. B (2010) 365, 3365–3376

doi:10.1098/rstb.2010.0070

The cranial base of Australopithecus

afarensis: new insights from the
female skull
William H. Kimbel1,* and Yoel Rak2
1
Institute of Human Origins, School of Human Evolution and Social Change, Arizona State University,
Tempe, AZ, USA
2
Department of Anatomy, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
Cranial base morphology differs among hominoids in ways that are usually attributed to some com-
bination of an enlarged brain, retracted face and upright locomotion in humans. The human
foramen magnum is anteriorly inclined and, with the occipital condyles, is forwardly located on a
broad, short and flexed basicranium; the petrous elements are coronally rotated; the glenoid
region is topographically complex; the nuchal lines are low; and the nuchal plane is horizontal.
Australopithecus afarensis (3.7 – 3.0 Ma) is the earliest known species of the australopith grade in
which the adult cranial base can be assessed comprehensively. This region of the adult skull was
known from fragments in the 1970s, but renewed fieldwork beginning in the 1990s at the Hadar
site, Ethiopia (3.4 – 3.0 Ma), recovered two nearly complete crania and major portions of a third,
each associated with a mandible. These new specimens confirm that in small-brained, bipedal
Australopithecus the foramen magnum and occipital condyles were anteriorly sited, as in humans,
but without the foramen’s forward inclination. In the large male A.L. 444-2 this is associated
with a short basal axis, a bilateral expansion of the base, and an inferiorly rotated, flexed occipital
squama—all derived characters shared by later australopiths and humans. However, in A.L. 822-1
(a female) a more primitive morphology is present: although the foramen and condyles reside ante-
riorly on a short base, the nuchal lines are very high, the nuchal plane is very steep, and the base is as
relatively narrow centrally. A.L. 822-1 illuminates fragmentary specimens in the 1970s Hadar
collection that hint at aspects of this primitive suite, suggesting that it is a common pattern in
the A. afarensis hypodigm. We explore the implications of these specimens for sexual dimorphism
and evolutionary scenarios of functional integration in the hominin cranial base.
Keywords: Australopithecus; cranial base; bipedality

1. INTRODUCTION The 3.7 – 3.0 Myr old hominin species

As the critical intersection of the locomotor, neural and
masticatory systems, the cranial base is a frequently
consulted source for insight into the evolution of the
human head in phylogenetic and functional–adaptive
contexts. A great deal of experimental and comparative
research on extant primates has been conducted to elu-
cidate the relative influence of each of these systems on
cranial base form (e.g. Lieberman et al. 2000), but the
fossil record—especially its earlier segments—is less
often studied because of small samples, poor preser-
vation, and/or inaccessible endocranial spaces. Yet,
the ultimate test of hypotheses regarding the conjunc-
tion of structural innovations and their purported
functions in an adaptive context is the relative timing
of their first appearances in taxa potentially ancestral
(or at least sister) to the extant taxa targeted by most
of this research. Therefore, it is important to glean as
much information as possible from the available fossil
remains.
* Author for correspondence (wkimbel.iho@asu.edu).
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3365
Australopithecus afarensis is usually considered to be
the plesiomorphic (‘primitive’, African apelike) sister
taxon to subsequent australopiths and the genus
Homo (e.g. Kimbel et al. 2004; Strait & Grine 2004).
Relative to these successor taxa, the skull and dentition
of A. afarensis is characterized by numerous primitive
features, many of which are part of, or at least influ-
enced by, the masticatory system (see Kimbel &
Delezene 2009, for a recent review). The cranial
base was spottily represented in the initial (1970s)
hypodigm of the species; a single partial calvaria of
an adult male individual from A.L. 333 (ca 3.2 Ma)
was the principal source of information until the first
complete adult skull of the species was recovered
in 1992 (A.L. 444-2, a large adult male, ca 3 Ma).
These specimens showed that, in contrast to the primi-
tive morphology of the temporal bone (e.g. low-relief
mandibular fossa, tubular tympanic element, highly
inflated squama, asterionic notch sutural pattern, etc.),
the calvaria is derived in its anteriorly positioned fora-
men magnum and occipital condyles on a short, broad
cranial base—features shared with modern humans.
The female calvaria of A. afarensis was until recently
known only from fragments of the calotte, and while
This journal is q 2010 The Royal Society
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3366 W. H. Kimbel & Y. Rak A. afarensis cranial base
these hinted at several morphological differences from
the larger (male) skulls, particularly in aspects of occi-
pital squama form, interpreting this morphology in the
context of the entire skull was not possible. Fieldwork
in the 2000s rectified this with the recovery of a nearly
complete skull of a small, probably female individual,
A.L. 822-1. This specimen adds information on vari-
ation in A. afarensis cranial base form, casts
previously known fragmentary remains of small
(female) individuals of this species in a new light,
Figure 1. The reconstructed A.L. 822-1 skull, oblique view.
Approximately 45% natural size.
(a)
Figure 2. Pattern of distortion in the A.L. 822-1 reconstruction. (a) Basal view. Note the asymmetric positions of the temporal
bones, resulting from deformation of the (anatomical) left side. (b) Superior view. Note the offset of the face in relation to the
calvarial midline. Red line denotes anatomical midline.
Phil. Trans. R. Soc. B (2010)
and reveals an apparently unique (in the extant African
hominoid context) pattern of sexual dimorphism in
the australopith cranial base. Our more comprehensive
description of the A.L. 822-1 skull is in preparation,
but here we focus on the cranial base of this specimen
and its substantive role in illuminating these issues.
2. THE A.L. 822-1 SKULL
The skull A.L. 822-1 was found by the late Dato
Adan, an Afar member of the Hadar Research Project,
during the 2000 field season. It was recovered from the
surface of sediments of the Hadar Formation’s KH-1
sub-member and is estimated to be approximately
3.1 Ma (C. Campisano 2009, personal communi-
cation). It is the third adult individual from Hadar to
preserve both the mandible and cranium (A.L. 444-2,
KH-2 sub-member, ca 3 Ma and A.L. 417-1, SH-3
sub-member, ca 3.3 Ma, are the other two).
The specimen was recovered in approximately 200
fragments, which have been cleaned, reconstructed
and reassembled to constitute most of an adult skull
with almost all of the dentition (figure 1). The recon-
struction of the original specimen reveals remnant
distortion, owing to both warping and crushing, in
(i) the failure of the palatal and calvarial midlines to
align, (ii) the temporal bones’ placement on different
coronal planes, and (iii) some bilateral compression
of both palatal and mandibular arches (figure 2). We
describe in detail this deformation and the steps
taken to correct it in our comprehensive comparative
study currently in preparation. The data and analyses
presented here are based on our final restoration
using casts of the original fossil.
The A.L. 822-1 skull presents numerous character-
istics diagnostic of A. afarensis (see Johanson et al.
1978; White et al. 1981, 1993, 2000; Rak 1983;
(b)
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A. afarensis cranial base W. H. Kimbel & Y. Rak 3367

A.L. 822-1
0 25 50 75 100

22.5 25.0 27.5 30.0 32.5 mm 27.5 30.0 32.5 35.0 37.5 40.0 42.5 mm
mandibular condyle ML breadth (n = 6) mandible corpus depth @ M1 (n = 20)

10.5 11.0 11.5 12.0 12.5 13.0 13.5 14 mm 9.0 9.5 10.0 10.5 11.0 11.5 12.0 12.5 mm
mandibular M1 breadth (n = 18) maxillary canine breadth (n = 12)
Figure 3. Box-plot metrical profile of A.L. 822-1. Data for A.L. 822-1 shown in Hadar A. afarensis sample distribution.
Bold vertical line indicates value for A.L. 822-1; rectangle defines the 25th and 75th quartiles; diamond defines the mean
and 95% CI; short vertical line within rectangle defines the median.

Figure 5. Hadar cranium A.L. 444-2. Note the low position

of the compound temporal/nuchal crest (arrow), which
approximates the biasterion line, a phylogenetically derived
condition of other mature males of A. afarensis. Approxi-
mately 50% natural size.

Figure 4. Lateral view of A.L. 822-1 ‘final’ restoration (cast),

showing the superiorly extended position of the nuchal lines
as expressed by W. E. Le Gros Clark’s nuchal area height
index: maximum height of nuchal lines (upper horizontal
line) above Frankfurt Horizontal (lower horizontal line) as
a percentage of maximum cranial vault height above FH
(vertical line).
Kimbel et al. 1984, 1994, 2004; Kimbel & Delezene
2009). These include:
— strongly prognathic, biconvex maxillary subnasal
surface,
— narrow midface (nasal aperture and interorbital
block),
— mild sagittal convexity of the low frontal squama,
— medial to lateral supraorbital thickness gradient,
— posteriorly convergent temporal lines,
— steeply inclined nuchal plane,
— low upper scale (la-i) and long lower scale (i-o) of
occipital squama,
Phil. Trans. R. Soc. B (2010)
— sharply angled articular surface of the occipital
condyle,
— flattened, horizontally oriented tympanic elements,
— hollowed lateral surface of the mandibular corpus
(beneath the premolars) with high ramal root and
narrow extramolar sulcus,
— marked topographic step down from mesial P3 to
the distal-P3 to M3 occlusal platform.
The A.L. 822-1 skull is most probably that of a female.
Its overall cranial dimensions are small, closely
approximating those of the very small though
incomplete Hadar adult calvaria A.L. 162-128
(Kimbel et al. 1982). The mastoid process is much
smaller than the mastoids of male crania such as
A.L. 333-45, A.L. 333-84 and A.L. 444-2. Consistent
with its small external dimensions, our preliminary
estimate of endocranial volume (using mustard seed)
is 385 cc, which is similar to that estimated for A.L.
162-28 (375 – 400 cc) and smaller than the estimates
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3368 W. H. Kimbel & Y. Rak A. afarensis cranial base

Table 1. Nuchal area height index in hominoids. Negative Two large (presumptive male) A. afarensis crania
value indicates nuchal area height is below Frankfurt have nuchal area height index values slightly higher
Horizontal. Comparative data from Kimbel et al. (2004). than the australopith average of 10 per cent (A.L.
333-45, in which FH is based on the ‘composite
nuchal area height reconstruction’ of Kimbel et al. 1984, 13%; A.L.
taxon/specimen index (%) 444-2, 12%). For A.L 822-1, however, the value is
Australopithecus afarensis
ca 23 per cent, about 9 per cent higher than for any
A.L. 444-2 13 other measurable, undistorted australopith cranium
A.L. 333-45 (recon.) 12 and about midway between chimpanzee and human
A.L. 822-1 23 means (figure 4). The relatively high index value is
Australopithecus africanus consistent with the visibly steep nuchal plane in A.L.
Sts. 5 10 822-1, which faces posteroinferiorly at ca 678 to the
Australopithecus boisei
FH. (The usual way of expressing nuchal plane steep-
OH 5 11 ness is the inclination of the inion – opisthion chord
KNM-ER 406 7 relative to FH; for A.L. 822-1, this angle is 428. How-
KNM-ER 13 750 23 ever, when the foramen magnum is anteriorly
KNM-ER 732 12 located—as it is in all australopiths (see below)—the
Australopithecus aethiopicus inion – opisthion chord angle can understate the steep-
KNM-WT 17 000 14 ness of the more lateral surfaces on which the mass of
Homo sapiens (n ¼ 10) 22 the nuchal muscles insert.)
Pan troglodytes male (n ¼ 10) 51 The superiorly extensive, steeply angled nuchal
Pan troglodytes female (n ¼ 10) 47 plane of A.L. 822-1 illuminates the morphology of
Gorilla gorilla male (n ¼ 10) 108 other less complete A. afarensis crania. In A. afarensis
Gorilla gorilla female (n ¼ 10) 67 partial calvariae A.L. 162-28 and KNM-ER 2602,
the nuchal plane is steep and the superior nuchal
lines highly arched; the transition between nuchal
for clearly male crania A.L. 333-45 (ca 485 cc) and and occipital planes across the superior nuchal lines
A.L. 444-2 (ca 550 cc; Holloway & Yuan 2004). As is smooth and convex; and the nuchal plane consists
shown in figure 3, the condyle of the A.L. 822-1 of bilateral, posterolaterally directed plates that
mandible is the second smallest in mediolateral merge at a median topographic peak (Kimbel et al.
diameter among six Hadar condyles, and its maxillary 1984, 2004; Kimbel 1988). While neither fossil can
canine breadth falls near the top of the smallest be oriented precisely on FH, their anatomical simi-
quartile in the Hadar sample distribution (n ¼ 12). larity to A.L. 822-1 is remarkable. Both specimens
Other aspects of A.L. 822-1 cranial morphology are small presumptive females that bear compound
consistent with female status are discussed below. temporal/nuchal crests; although A.L. 822-1 does
not, the temporal lines sweep laterally towards the
3. THE CRANIAL BASE OF A.L. 822-1 asteria within a few millimetres of the highly arched
(a) Nuchal area height and morphology of the superior nuchal lines. Except for the relatively low
occipital bone nuchal area height index value, the overall morpho-
In the 1940s W. E. Le Gros Clark argued that the logical pattern of these female specimens is extremely
small, horizontally oriented nuchal plane of the occipi- primitive.
tal bone of South African australopith crania was Figure 5 depicts the large, male A. afarensis cranium
compatible only with a humanlike poise of the head A.L. 444-2 in posterior view. Asterion in hominins
on the cervical vertebral column (Le Gros Clark usually lies close to the FH and the low position of
1947, p. 309; 1950, p. 241 – 243). He devised the the superior nuchal line relative to the biasterion line
‘nuchal area height index’ to express the much smaller is indicated in the figure. We draw attention to the dis-
degree to which the insertion area of the neck muscles tinction between Hadar crania that have high nuchal
extended superiorly (relative to the Frankfurt horizon- lines and steep nuchal planes (A.L. 822-1, A.L. 162-
tal (FH) baseline) as a percentage of maximum 28 and A.L. 439-1; the A.L. 288-1a, ‘Lucy’, occipital,
calvarial height in fossil and living hominins as com- too incomplete to orient with precision, bears these
pared with the great apes. In the African great apes same hallmarks), and those in which the nuchal lines
the height of the nuchal area constitutes (on average) are lower (closer to the biasterion line) and the
approximately 50 per cent of the calvarial height in nuchal plane much more horizontal (A.L. 333-45,
both male and female chimpanzees and 67 per cent A.L. 444-2), as in most later hominins. With one
in female gorillas (in male gorillas the index is more exception, this difference divides the sample by size,
than 100 per cent because the superior extension of which we take to indicate sex, with males showing
the enormous compound temporal/nuchal crest actu- the more derived morphology. The exception is A.L.
ally surpasses maximum vault height). Among the 439-1, a very large male occipital (comparable in size
australopiths, in contrast, the percentage averages to that of A.L. 444-2). Although this specimen bears
only about 10 per cent (with a total range of 23% to massive compound temporal/nuchal (T/N) crests that
þ14%, n ¼ 10), which is much closer to what is extend on each side from the middle of the nuchal
observed in modern humans (average ¼ 22%, i.e. line laterally to asterion, it is not fully mature judging
nuchal plane height is slightly below the FH; see from the open lambdoidal suture. The same mor-
table 1). phology is replicated in yet another even more
Phil. Trans. R. Soc. B (2010)
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A. afarensis cranial base W. H. Kimbel & Y. Rak 3369

fragmentary Hadar occipital, A.L. 444-1 (from the Table 2. Position and orientation of foramen magnum.
same locality as the complete, old adult A.L. 444-2 Index calculated as the projected length opisthion–
skull); this specimen, which consists of two non- opisthocranion/projected length glabella –opisthocranion.
articulating squamous fragments that span the Negative value for foramen orientation indicates
boundary between nuchal and occipital planes on oppo- anteroinferior orientation.
site sides, is from a large, thick-vaulted cranium and
FM
bears a weak compound T/N crest. The relatively
position FM
feeble expression of the compound crest, together with taxon/specimen index (%) orientation (8)
the completely patent and ‘puffy’ lambdodial sutural
surface, argues for a younger subadult growth stage of Australopithecus afarensis
this apparently male individual compared with A.L. A.L. 444-2 24 16
439-1. As in A.L. 439-1, however, the nuchal plane is A.L. 333-45 (recon.) 19 —
very steep, facing more posteriorly than inferiorly, A.L. 822-1 23 14
even making allowance for errors in orientation of the Australopithecus africanus
fragments. These two relatively young, large male indi- Sts. 5 19 20
viduals present a significant contrast with older adult Australopithecus boisei
males as represented by A.L. 333-45 and A.L. 444-2. OH 5 24 7
The expanded sample of Hadar skulls permits the KNM-ER 406 18 13
identification of a cross-sectional ontogenetic trans- KNM-ER 13 750 20 —
formation of male occipital morphology (from young Australopithecus aethiopicus
to old, A.L. 444-1!439-1!333-45!444-2). This KNM-WT 17 000 21 —
transformation entails increasing horizontality of the Homo sapiens (n ¼ 10) 31 28
nuchal plane, which results in greater flexion of the Pan troglodytes male (n ¼ 10) 12 18
occipital squama on the sagittal plane; increasing topo- Pan troglodytes female (n ¼ 10) 14 20
Gorilla gorilla male (n ¼ 10) 7 27
graphic flattening of the nuchal plane; lowering of the
Gorilla gorilla female (n ¼ 10) 13 30
nuchal crest, and related to these shifts, an alteration
of the compound T/N crest from a posterosuperior
extension of the nuchal plane to an inferior projection
of the occipital plane (see Kimbel et al. 2004, for com- horizontal projected length of the calvaria (g – op).1
parative observations and data). We do not, based on In our sample of African great apes, the mean index
presently available evidence, see the same transform- value ranges between 7 per cent (male gorillas, with
ation in female individuals of A. afarensis. All four their massive compound crests) and 14 per cent
specimens from which relevant information can be (female chimpanzees). In humans the more anterior
extracted are mature (A.L. 162-28, A.L. 822-1 and position of opisthion is conveyed by the much higher
KNM-ER 2602, probably A.L. 288-1a) and these mean index value in our sample of 31 per cent
clearly demonstrate the symplesiomorphic pattern (range ¼ 28 – 34%). Individual australopith values
associated with young males of the species. This simi- vary between 18 and 24 per cent, with the two
larity partly explains (along with an expansive A. afarensis specimens (A.L. 444-2 ¼ 24%, A.L.
posterior temporalis) why compound T/N crests are 822-1 ¼ 23%) falling at the high end of this range
so common in the smaller crania of this species (table 2). Weidenreich’s reported values for Asian
(Kimbel et al. 2004). Homo erectus crania yields an average of about 26 per
cent (range ¼ 24 – 28%).
The importance of these data on foramen magnum
(b) Position and orientation of the foramen position among fossil hominins is that neither hypoth-
magnum esized postural/locomotor differences (i.e. between the
The margins of the foramen magnum in A.L. 822-1 australopiths and H. erectus) nor absolute brain-size
are preserved on two fragments: one extends from differences (with H. erectus having endocranial
the basioccipital posterolaterally to include the right volumes 1.5 to 2.0 times larger than australopith
occipital condyle and adjacent jugular process; the values) has a large impact on the position of the fora-
other is a strip of nuchal plane bearing a short men on the cranial base. Rather, the major difference
(14 mm) segment of the margin just anterolateral to is between the quadrupedal apes and the bipedal
opisthion (although this fragment does not connect hominins. However, a different division applies to
to the main portion of the occipital squama, external the data on foramen magnum orientation (ba– o line
morphology constrains its placement to within a few relative to FH). In humans the foramen is forwardly
mm). Between these two pieces we can estimate the inclined (i.e. the plane of the foramen faces anteroin-
size and position of the foramen within a narrow feriorly) whereas in the great apes it is posteriorly
error range (+2 mm). inclined (posteroinferior orientation). In A. afarensis
In A. afarensis, as in all australopith species, the the reconstructed angle of the ba-o line is ca 148 in
foramen magnum, and with it the occipital condyles, A.L. 822-1 and ca 168 in A.L. 444-2, values that lie
resides in an anterior position on the cranial base. within the range for other australopith crania. The
Typically, this is assessed through indices expressing australopith range (table 2) is well below the range
the anteroposterior position of basion (ba) or opisthion for our sample of modern humans (the mean value
(o) in relation to cranial length. We use Weidenreich’s for which is ca 288; again, the foramen faces anteroin-
(1943) index relating the position of opisthion to the feriorly) but overlaps the low end of the range for

Phil. Trans. R. Soc. B (2010)

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3370 W. H. Kimbel & Y. Rak A. afarensis cranial base

Table 3. Measures of basi-occipital length. msp be bt bz

basi-occip. basi-occip. gorilla F

length lg/biorbital
taxon/specimen (mm) br * 100 chimpanzee M

Australopithecus afarensis AL 822-1

A.L. 444-2 20 21
A.L. 822-1 22 23 AL 444-2
A.L. 417-1 19 24
Australopithecus africanus Sts 5
Sts. 5 25 29
MLD 37/38 21 — KNM-ER 406
Stw 187 17 —
Australopithecus boisei KNM-WT 17 000
OH 5 20 20
KNM-ER 406 25 24
KNM-ER 407 21 —
Figure 6. Schematic of relative cranial base breadth in homi-
Australopithecus aethiopicus noids. Dashed vertical lines represent the biorbital breadth of
KNM-WT 17 000 25 27 A.L. 822-1, to which all specimens are size-adjusted. MSP,
Homo sapiens (n ¼ 10) 21 22 midsagittal plane; be, terminus of bi-entoglenoid breadth;
Pan troglodytes male (n ¼ 10) 28 29 bt, terminus of bi-articular tubercle breadth; bz, terminus
Pan troglodytes female (n ¼ 10) 26 28 of bizygomatic breadth. Heavy red line defines the breadth
Gorilla gorilla male (n ¼ 10) 37 33 of the articular eminence. Note in A.L. 822-1, chimpanzees
Gorilla gorilla female (n ¼ 10) 29 30 (males, n ¼ 10) and gorillas (females, n ¼ 10) the close
approximation of the entoglenoid processes, expressing a
narrow central cranial base.

Table 4. Cranial base breadth in hominoids.

position between modern apes and humans, but
bi-entogl. br/
bi-entoglenoid biorbital
closer to the former (chimpanzees, specifically).
taxon/specimen br (mm) br * 100 Whereas the anterior shift of basion and opisthion
accounts for the forward location of the foramen
Australopithecus afarensis magnum in australopiths and modern humans, the
A.L. 444-2 80 84 relative vertical positions of these landmarks (beneath
A.L. 333-45 (recon.) 78 89 the FH, for example) explain the differences in orien-
A.L. 822-1 57 62 tation of the foramen (Kimbel et al. 2004). Because
Australopithecus africanus the vertical position of basion is similar in apes and
Sts. 5 65 76 humans, differences in foramen orientation reduce to
MLD 37/38 62 — differences in the vertical position of opisthion. In
Australopithecus boisei humans, uniquely, opisthion sits much further below
OH 5 89 84 FH than basion (the foramen opens anteroinferiorly),
KNM-ER 406 85 89 which can be explained as a consequence of overall
KNM-ER 13 750 86 80 expansion and rotation of the occipital squama
KNM-ER 23 000 80 — with encephalization (e.g. Weidenreich 1941; Biegert
KNM-ER 407 65 —
1957). In the small-brained A. afarensis, although the
Australopithecus aethiopicus foramen magnum is far forward on the base, opisthion
KNM-WT 17 000 80 85 is elevated relative to basion and so the plane of the
Homo sapiens (n ¼ 10) 74 77
foramen inclines posteriorly, more similar to what is
Pan troglodytes male 61 67
(n ¼ 10) observed in the apes.
Pan troglodytes female 59 65 Occipital morphology in A. afarensis is consistent
(n ¼ 10) with these signs of affinity from the foramen
Gorilla gorilla male 72 63 magnum. As discussed above, the orientation of the
(n ¼ 10) nuchal plane, the height of the nuchal muscles’ inser-
Gorilla gorilla female 64 64 tion area, and the degree of sagittal flexion of the
(n ¼ 10) occipital squama range from symplesiomorphic (ape-
like) to more derived, but taken as a package convey
an intermediate position on the hominoid occipital
bone morphocline. At the derived end of the morpho-
chimpanzees (mean ¼ ca 198; gorilla means are about cline occipitals approach a quasi-human form in their
50% higher; see Kimbel et al. 2004, for details). Thus, relatively horizontal nuchal plane, low nuchal area
in contrast to the data on foramen magnum position, height index and strongly flexed squama, but they do
which align A. afarensis and other australopiths with not show the strongly rotated squama that in modern
modern humans, the data on orientation of the fora- humans confines the maximum height of the nuchal
men situate the australopiths in an intermediate area below the FH (on average) and drops opisthion
Phil. Trans. R. Soc. B (2010)
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
90
ER 13 750
85
80 ER 23 000, WT 17 000
333-45
75
bientoglenoid breadth
70
65 ER 407
MLD 37/38
60 X
58-22
55
50
25
Figure 7. Bivariate plot of palate breadth and cranial base (bi-entoglenoid) breadth in hominoids. Light brown data points,
male gorilla; dark brown, female gorilla; light blue, male chimpanzee; X, Australopithecus afarensis; þ, A. africanus; Z, A. boisei.
very far below basion, introducing a negative angle to
the foramen’s orientation. It bears noting that the pos-
ition of the foramen magnum, which is relatively
anterior in A. afarensis and close to the condition in
modern humans, is not linked to this impressive
range of variation in occipital bone morphology.
(c) Length and breadth of the cranial base
Along with the anterior position of the foramen
magnum, the shortened external length of the cranial
base is a derived feature in A.L. 822-1 shared with
modern humans. This can be judged from the length
of the basi-occipital fragment associated with this
fossil (22 mm) as well as that attributed to another
Hadar specimen, A.L. 417-1 (19 mm), which essen-
tially match the mean for modern humans both
absolutely and relative to biorbital breadth (table 3).
A shortened external base can be inferred for speci-
mens of A. afarensis in which the basi-occipital is
missing, such as the large (male) crania A.L. 333-45
and A.L. 444-2, from the anteroposterior distance
between the carotid foramen and foramen ovale
(which roughly approximates basi-occipital length) or
the length of the petrous elements (which frame the
basi-occipital area), both of which are shorter than in
gorillas and chimpanzees.
Phil. Trans. R. Soc. B (2010)
A. afarensis cranial base W. H. Kimbel & Y. Rak 3371
Z
OH 5
Z
ER 406
X
444-2
+
Sts 5
X
822-1
30 35 40 45 50
internal palate breadth at M2
Most other early hominins share the shortened
external anterior cranial base with A. afarensis (table 3).
Dean & Wood (1982), however, showed that the
A. africanus base is unusual in its somewhat elongated
anteroposterior dimensions compared with other
australopiths and early Homo. Specimen Sts 5 indeed
has absolutely and relatively long basi-occipital and
petrous elements compared with other hominins
(table 1), but it is the only A. africanus cranium in
which these dimensions can be judged relative to a
non-calvarial size standard (such as biorbital breadth
or palatal length). In absolute terms the basi-occipital
of MLD 37/38 and Stw 187 are as short as those of
A. afarensis, so it is unclear whether Sts 5 is typical
of A. africanus.
Relative to body size and skull size the modern
human cranial base is short, but also wide, whereas
the great apes exhibit the opposite proportions.2
Tobias (1967) noted that the mandibular fossa is
equally wide (mediolaterally) in gorillas and OH 5
(the type specimen of Australopithecus boisei), but
only in the latter does the fossa project laterally far
beyond the calvarial wall to anchor the temporal root
of the flaring zygomatic arch. In gorillas, he found,
the mandibular fossae, in spite of their great breadth,
are actually closer together on the cranial base and
so do not project nearly as far from the calvarial wall.
This difference is depicted graphically in figure 6,
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3372 W. H. Kimbel & Y. Rak A. afarensis cranial base

Table 5. Palate dimensions in fossil hominins. Palate depth breadths compared with clearly male crania (A.L.
is the midline height of the palatine process of the maxilla 333-45, A.L. 444-2). Biorbital breadth is not available
above the inner alveolar margin at M2. Palate breadth is for A.L. 58-22, but another way to assess the relative
the width across the internal alveolar crests at mid-M2. width of the central cranial base is by a simple index
Palate length is the direct distance between orale and expressing the bi-entoglenoid distance as a percentage
staphylion (reconstructed in some specimens). Relative
of the bi-articular tubercle distance. When this is
palatal breadth (Palatal Index) is calculated as palate
breadth/palate length * 100.
done, it can be seen that in spite of small fossa
breadths (which would increase the index), the bi-
palate palate palate palatal entoglenoid distance is relatively small in these two
taxon/specimen depth breadth length index specimens (ca 48%), compared with the larger
Hadar crania (ca 55%) and other early hominins,
Australopithecus afarensis including A. africanus (ca 54%, n ¼ 2).
A.L. 58-22 — 27.0 — —
A.L. 199-1 11.0 32.0 54.0 59.3
A.L. 200-1a 8.5 33.5 65.0 51.5 (d) The cranial base and palate shape
A.L. 417-1d 14.0 28.5 58.0 49.1 In their diagnosis of A. afarensis, Johanson et al. (1978,
A.L. 427-1 11.0 32.0 — —
A.L. 442-1 — 25.0 — —
p. 6) listed as a distinguishing feature of the adult cra-
A.L. 444-2 12.0 41.0 75.0 54.7 nium ‘palate shallow, especially anteriorly; dental
A.L. 486-1 11.2 33.0 — — arcade long, narrow and straight-sided’. Subsequent
A.L. 822-1 14.0 31.0 63.0 49.2 discovery and analysis have confirmed this symplesio-
Australopithecus africanus morphic feature set of the A. afarensis palate (Kimbel
Sts. 5 18.0 35.7 65.3 54.7 et al. 2004). However, two specimens found since
Sts. 53 — 32.0 54.0 59.3 1990 extend the range of variation in this species’ palatal
Stw. 73 14.5 30.0 58.0 51.7 form. In both A.L. 417-1 and A.L. 822-1 the palate
Australopithecus robustus is both very narrow and very deep: internal palate
SK 12 12.8 32.0 — — depth (both 14 mm at M2) is the greatest among
SK 46 12.2 35.0 — — seven measureable Hadar specimens, while relative
SK 48 15.5 — — — palate breadth (internal breadth at M2/length  100 ¼
SK 79 13.5 — — — ca 49%) is the lowest among five Hadar specimens
SKW 11 15.0 34.6 60.0 57.7 and, indeed, among 11 of 12 australopith specimens
Australopithecus boisei in our sample overall (table 5).
KNM-ER 405 22.0 38.0 75.0 50.7 The very narrow palate of the smaller Hadar crania
KNM-ER 406 20.0 37.4 70.0 53.4 is potentially related to the narrow cranial base in these
OH 5 21.0 38.2 79.1 48.3 A. afarensis individuals. Recall that the base (measured
KNM-CH 1 — 40.8 72.0 56.7 between the entoglenoid processes) of A.L. 822-1 is as
relatively narrow as in gorillas. Cranial base width
cannot be measured for A.L. 417-1, but in A.L.
58-22, which (as described in the previous section)
where it can be seen that many other australopiths has a cranial base width approximately as small as that
resemble the morphology Tobias (1967) described of A.L. 822-1, estimated palate breadth (ca 27 mm, at
for OH 5. A notable exception is A.L. 822-1, which, M2) is the second smallest in the A. afarensis sample
in relative terms (note that all specimens in the (palate length for A.L. 58-22 cannot be estimated).
figure are scaled to the biorbital breadth of this The relationship between the narrowness of the palate
Hadar cranium), has a very narrow cranial base. As and the narrowness of the cranial base would appear
measured across the entoglenoid processes (the recon- to hold, albeit on limited available evidence.
structed positions of which are validated by the This relationship is explored further in the context
bicondylar breadth of the specimen’s mandible), the of African great ape comparative data in figure 7.
cranial base of A.L. 822-1 is as narrow as average for Among the apes there is a strong correlation (r 2 ¼
our sample of female gorillas, and narrower than in 0.52, p , 0.0001) between absolute values of palate
any other of the figured australopith specimens, breadth and bi-entoglenoid breadth, which appears
including Sts 5 and the A.L. 444-2 cranium of A. afar- largely to be a function of strong size-dimorphism in
ensis, in which the mandibular fossae are spread far gorillas (figure 7). Using size-standardized variables
apart on the base. (with biorbital breadth as the standard), the corre-
Another Hadar specimen, A.L. 58-22, appears lation is much weaker (because male gorillas no
similar to A.L. 822-1 in its narrow cranial base. This longer stand out; r 2 ¼ 0.14, p , 0.017). However, in
specimen is a craniofacial fragment with part of the both cases the smaller A. afarensis individuals are the
right posterior maxilla, sphenoid and temporal bone; most apelike of the small fossil hominin sample in
the vomer establishes the midline (Kimbel et al. their combination of narrow palates and narrow cranial
1982). As with A.L. 822-1, the bi-entoglenoid dis- bases, with A. boisei and even A. africanus specimens
tance (60 mm) is small compared with the larger highly divergent (indeed, humanlike, though humans
Hadar crania, by at least 20 mm (table 4). This absol- were not included in our analysis) in their broader
ute difference may reflect sexual dimorphism in cranial cranial bases.
base dimensions in A. afarensis, as both of these Hadar Of considerable interest is the position of A.L.
specimens also have abbreviated mandibular fossa 444-2, the large male A. afarensis skull. Compared
Phil. Trans. R. Soc. B (2010)
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
A. afarensis cranial base
with the smaller specimens, it has a much broader
cranial base for its palate breadth than predicted
by either great ape regression, which hints at an
unusual—but perhaps not exceptional—pattern of
sexual dimorphism in A. afarensis. Note that there
are no small A. boisei specimens in the sample for
which both palate and cranial base breadths can be
measured (only OH 5 and KNM-ER 406 preserve
both dimensions). However, the bi-entoglenoid
breadth of KNM-ER 407, considered by consensus a
female A. boisei calvaria, is less than 10 mm wider
than that of the two A. afarensis females (see y-axis
in figure 7), and if we grant this individual a palate
breadth somewhere between, say, those of A.L.
822-1 and Sts 5 (ca 31 – 36 mm), then the presumptive
female-to-male trend in the cranial base versus
palate breadth relationship for A. boisei would be
very similar to that of A. afarensis. That is, compared
with extant African apes (and other anthropoid
species; M. Spencer 2010, personal communication),
males have a much wider cranial base for their palate
width than females (see also the suggestive position
of other large A. boisei and A. aethiopicus specimens
on the y-axis of figure 7). (Unfortunately, the fossil
record does not permit us to extract any more
information from the size-standardized data.) This
suggests a unique pattern of cranial sexual dimorphism
among australopith species.
4. DISCUSSION
The A.L. 822-1 skull focuses attention on several
aspects of adult cranial base morphology that were
not previously well understood for A. afarensis.
First, this Hadar specimen presents a particularly
primitive basicranial profile. Its relatively narrow cra-
nial base, high nuchal lines, and correspondingly
steep nuchal plane are more similar to African great
ape conditions compared with other australopiths so
far known. While other more fragmentary A. afarensis
specimens hint at relatively generalized occipital form,
A.L. 822-1 places this morphology within the context
of the entire skull for the first time.
Second, A.L. 822-1 points to a pattern of cranial
sexual dimorphism neither recognized previously
among the australopiths nor encountered among
extant hominoids. The apelike cranial base pro-
portions and nuchal area form are already presented
in derived conditions in larger A. afarensis specimens
usually considered to be males (A.L. 333-45, A.L.
444-2). In these crania the basicranium is wider
(absolutely and size-standardized) and the position of
the nuchal lines approximates FH, with a horizontal
nuchal plane, differences that raise the question of
whether species-level taxonomic distinction between
the two morphs is warranted. Two further points
argue otherwise. First, the combination of high
nuchal lines and a steep nuchal plane in two
large, immature occipital specimens (A.L. 439-1,
A.L. 444-1) suggests that this dimorphism in the
Hadar cranial sample has an ontogenetic basis, with
young males ‘passing through’ the final adult form of
the smaller females to reach mature male (and more
derived) morphology. Second, the adult cranial
Phil. Trans. R. Soc. B (2010)
W. H. Kimbel & Y. Rak 3373
sample of A. boisei hints at the same pattern of cranial
base breadth dimorphism, while the occipital of the
L338y-6 calotte (Shungura Formation, Member E),
interpreted by Rak & Howell (1978) as a immature
male of this species, has a very steep nuchal plane, as
is also observed in the young Hadar males. These
observations convince us that the variation in Hadar
occipital and cranial base form, though phylogeneti-
cally informative, is intraspecific. A similar case has
previously been made for the polymorphic lower
third premolar in A. afarensis (Kimbel et al. 2004,
2006).
Finally, the expanded cranial sample of A. afarensis
highlights the strongly mosaic nature of basicranial
evolution in the hominin clade. Evolutionary changes
in the cranial base and occipital squama that are
thought to unite early hominins with modern
humans (and which, for example, have raised suspi-
cions of pervasive homoplasy in the crania of robust
australopiths and Homo), were still not completed by
the time of A. afarensis, ca 3.5 – 3.0 Ma. Thus,
although an anteriorly located foramen magnum and
a short basioccipital segment are shared with extant
humans, the narrow cranial base, posteriorly inclined
foramen magnum, high nuchal lines and concomi-
tantly steep nuchal plane, are apelike characteristics
that are inferred to have been commonly, though not
universally, expressed in this taxon.
Upright posture and a large brain are the most com-
monly invoked influences on the cranial base
morphology of modern humans (see Lieberman et al.
2000, for a review). According to Le Gros Clark
(1947), Robinson (1958) and Olson (1981), among
others, the descent of the nuchal musculature and
the rotation of the nuchal plane to a horizontal pos-
ition beneath the brain case mirrors the adoption of
upright posture and bipedal locomotion in the homi-
nin clade. Biegert (1957; also Weidenreich 1941), in
contrast, argued that the architectural remodelling of
the hominin posterior calvaria was a by-product of cer-
ebral expansion, which introduced a strongly flexed
basicranial axis and a ‘rolling up’ of the braincase
that impelled the foramen magnum and occipital con-
dyles forward. After casting doubt on the oft-proposed
correlation among foramen magnum orientation,
occipital condyle position and mode of locomotion
in primates, Biegert (1963) pointed to the horizontal
nuchal plane and anterior foramen magnum of
A. africanus (Sts 5) as evidence of an initial phase of
encephalization in hominin evolution. Robinson
(1958), citing the case of the ‘short-faced squirrel
monkey’ (Saimiri ), noted that the orientation of the
nuchal plane (steep) and the position of the occipital
condyles and foramen magnum on the cranial base
(anterior) are not necessarily related, which recalls
the situation in A. afarensis. The review by Lieberman
et al. (2000) concluded that the orientation of the fora-
men magnum (as distinct from its anteroposterior
position) is unrelated to the posture of the head on
the vertebral column but, with cranial base flexion, is
primarily a reflection of brain size relative to cranial
base length.
The skulls of A. afarensis bear on these issues. This
species is demonstrably an upright biped with a mean
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3374 W. H. Kimbel & Y. Rak A. afarensis cranial base
endocranial volume (ca 450 cc) slightly larger than
that of Pan troglodytes, to which, among the living
hominoid taxa, it is probably closest in body size.
The marked variation in the height of the nuchal
muscle insertions and angulation of the nuchal plane
in A. afarensis would seem to negate a major role for
upright locomotion in dictating morphological vari-
ation in this region of the hominin skull. One caveat
is that we do not have a good idea about how the
head was held on the cervical vertebral column in
Australopithecus; while the anterior position of the
occipital condyles suggests a head posture more simi-
lar to that of modern humans than apes, the slightly
posterior orientation of the foramen magnum, the
strongly angled atlanto-occipital articular surfaces
(on A.L. 333-45, A.L. 822-1, and the A.L. 333-83
first cervical vertebra), and the long, straight and
robust spine of the lower cervical vertebra (C6, A.L.
333-106), may be signs of a mechanical environment
dissimilar to that of the modern human cranioverteb-
ral interface. We do not know the extent of cervical
lordosis in these early hominins, but it would not
surprise us to find a less lordotic cervical column in
A. afarensis than in modern humans.
Obviously, whether measured absolutely or relative
to estimated body mass, brain size in A. afarensis is
much closer to that of apes than modern humans.
This indicates that the humanlike anterior position of
the foramen magnum is largely, if not entirely, unre-
lated to overall brain size. Perhaps, though, relative
neocortical (cerebral) expansion is responsible for
the forward migration of the foramen. In this context,
the (by now) clear evidence of a relatively posterior
position of the lunate sulcus on earliest australopith
brain endocasts (Holloway et al. 2004) can be seen
as a sign of relative cerebral expansion, which, poster-
iorly, is manifested as a bulging of the occipital poles
over the cerebellar lobes, and, perhaps, a forward
‘rotation’ of the cranial base (similar to what Biegert
1963 hypothesized). In the A. afarensis brain endocast
the absolute and relative size of the cerebellar lobes
(and especially their anteroposterior length) is much
smaller than in African great apes, in which the cer-
ebral and cerebellar lobes protrude subequally
(Holloway & Yuan 2004). However, it is unclear to
what extent the form of the braincase beneath the
tentorium cerebelli would be affected morphogenetically
by enlargement of the cerebrum posteriorly; this is
an area in need of further research.
The ape-sized brain of A. afarensis rests on a base
with a much shorter basi-occipital segment than in
any great ape. As shown by Lieberman et al. (2000;
see also Spoor 1997; McCarthy 2001), brain size rela-
tive to cranial base length explains a fairly large
amount (but not all) of the observed variation in cra-
nial base angle across a wide spectrum of anthropoid
primates. We do not know the exact length of the
anterior cranial base (sella turcica to foramen
caecum) in A. afarensis, but evidence from fragmen-
tary specimens (i.e. A.L. 58-22, A.L. 417-1) and the
demonstrably short segment between basion and the
rear of the palate indicate a total cranial base length
less than an ape of comparable brain size. (The
index of relative encephalization 1, which expresses
Phil. Trans. R. Soc. B (2010)
the cube root of endocranial volume as a percentage
of cranial base length [ba-sella þ sella-fc], is roughly
0.94 in A.L. 822-1, which is smaller than values for
fossil and extant Homo but in the zone of overlap for
the small sample of australopiths and extant apes
measured from CT scans by Spoor 1997.) Similarly,
we can only estimate the (internal) flexion of the cra-
nial base in A. afarensis, using the preserved
morphology of A.L. 822-1 (which includes a marked
superior deflection of the external basioccipital surface
at basion) with support from the other more fragmen-
tary specimens mentioned above; for A.L. 822-1 the
angle (ba-se/se-fc; CBA1 of Lieberman et al. 2000) is
approximately 1428 (+58), which is some 15– 208
more flexion than great ape species’ means and close
to the modern human mean. This Hadar skull has a
more highly flexed cranial base than extant African
apes of similar relative brain size (details in prep-
aration; see also Spoor 1997; Lieberman et al. 2000,
for comparative data).
Although the influence of body posture on primate
cranial base form has been discounted by recent
research (see Lieberman et al. 2000), we see the
anterior position of the foramen magnum and occipital
condyles as the major cranial base distinction between
Australopithecus and Homo, on one hand, and the great
apes on the other. The fact that this distinction maps
onto primary locomotor differences speaks to upright
posture in hominins as an important factor in the
positional shifts of these cranial base structures. In
our view (see also Spoor 1997; Kirk & Russo 2010),
the adoption of upright posture (though not necessarily
striding bipedal locomotion per se) in hominins led to a
forward migration of the foramen magnum/occipital
condyles and a shortened cranial base.3 The combi-
nation of a small, ape-sized brain on a relatively short
base introduced the flexion of the basicranial axis.
Thus, despite their small brains, the anterior position
of the foramen magnum (basion) in Australopithecus
was associated with the relatively short, flexed cranial
base typical of modern humans by ca 3 Ma (figure 8).
Subsequent changes in the orientation of the foramen
magnum (anteroinferior-facing) in the Homo clade are
probably linked to an increase in endocranial volume
and the consequent descent of opisthion beneath the
braincase, as discussed above (see Kimbel et al. 2004
for details). The introduction of the cervical vertebral
lordosis may also play a role in this change, but the
fossil record is currently mute on the timing of the
initial appearance of this innovation.
If we consider the potential link between cranial
base configuration and facial orientation (e.g. Ross &
Ravosa 1993; Lieberman et al. 2000), the short,
flexed base may account for the relatively vertical mid-
facial segment in A. afarensis, which creates an overall
less prognathic facial profile than in chimpanzees and
gorillas (Kimbel et al. 2004: fig. 3.24, where midfacial
prognathism is measured as the angle between a line
connecting nasion or sellion to nasospinale and the
FH). In the great apes pronounced midfacial
prognathism—a dorsal deflection of the nasion-
nasospinale segment in relation to a weakly flexed
cranial base—results in an airorynch facial configur-
ation. The contrasting klinorynch condition is a
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010

A. afarensis cranial base W. H. Kimbel & Y. Rak 3375

A. afarensis, reveals a particularly generalized pattern

of morphology in occipital squama and cranial base.
With superiorly extended nuchal lines, a concomi-
na tantly steep nuchal plane, and a narrow cranial base,
this skull is notably more apelike than other australo-
fc
se pith crania, including those of larger, clearly male,
individuals of this species, which share derived states
157° of these characters with subsequent australopith
O
species and Homo. It throws into sharp relief the
ba morphology of previously known fragmentary cranial
specimens from the Hadar site, demonstrating that
ns
the generalized pattern is probably common in small
pr (female) individuals of this species. Qualitative data
on a cross-sectional cranial growth series contained
gorilla
within the Hadar sample suggest that some of the
variation in A. afarensis is indeed intraspecific because
young adult males resemble mature females more than
they do older males in their generalized occipital form.
na Although the inference is limited by the few data
fc available, these observations suggest for A. afarensis a
se pattern of cranial sexual dimorphism unknown
142° among extant hominoids, with adult males character-
ized by relatively wider cranial bases and more
O ns horizontal nuchal muscle origin surfaces than females.
ba At least for the cranial base width, this dimorphism
pr
may apply to A. boisei as well; no other australopith
taxon currently permits comparison.
Morphological variation in the cranial base of
A. afarensis is consistent with a mosaic pattern of
evolutionary change in this region of the skull. Early
australopiths were upright bipeds with small brains.
The anterior position of the foramen magnum and occi-
A.L. 822-1
pital condyles on a short (though not necessarily
broad), flexed cranial base—a derived character com-
plex linked plausibly to upright posture—is unrelated
to substantial variation in the morphology of the
nuchal region of the calvaria, which is often thought
to mirror postural differences. In species potentially
fc descendant from A. afarensis the nuchal region
se na became more uniformly humanlike in form and orien-
tation, the functional basis for which remains poorly
understood. A derived, relatively upright midfacial pro-
137° ns file, which likewise ties A. afarensis to later australopiths
ba and Homo, may be related to these cranial base modifi-
O pr cations and thus, indirectly, to upright posture itself.
H. sapiens
We thank the Authority for Research and Conservation of
Figure 8. Midsagittal craniograms of A.L. 822-1, female gor- Cultural Heritage and the National Museum of Ethiopia,
illa, and modern human, showing cranial base and midfacial Ethiopian Ministry of Culture and Tourism, and the Afar
angles. A.L. 822-1 anterior cranial base (sella-foramen Regional State government for permission to conduct the
caecum) reconstructed with additional information from field (Hadar) and laboratory (Addis Ababa) research. We
A.L. 417-1 and A.L. 58-22. See text for discussion. are grateful to the (US) National Science Foundation for
grants supporting the field and lab work. Thanks are due
Dr Mark Spencer for discussion and Mr Lucas Delezene
for help with collecting the comparative data.
hallmark of the human facial skeleton already mani-
fested, at least incipiently, in A. afarensis (figure 8).
The prognathic maxilla, with its strongly inclined
nasoalveolar clivus, would not be expected to be ENDNOTES
impacted as directly by cranial base form, and this 1
Weidenreich chose opisthion rather than basion for this purpose
remains the most apelike aspect of the A. afarensis face. probably because none of the Homo erectus crania he described
preserves the anterior margin of the foramen magnum.
2
Here, cranial base length is taken as the combined length of the
segments basion to sella turcica to foramen cecum. Width of the
5. CONCLUSIONS base is measured between the summits of the entoglenoid processes.
The A.L. 822-1 specimen, providing the first view 3
As noted by Schultz (1955), in ontogenetic context the hominin
of the complete small, presumptively female skull of foramen magnum does not migrate anteriorly; from the relatively

Phil. Trans. R. Soc. B (2010)

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3376 W. H. Kimbel & Y. Rak A. afarensis cranial base
anterior position common to all juvenile hominoids, the foramen
fails to shift posteriorly with growth of the cranium, as it does in
all great apes.
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Phil. Trans. R. Soc. B (2010) 365, 3377–3388

doi:10.1098/rstb.2010.0042

Hominin diversity in the Middle Pliocene

of eastern Africa: the maxilla of
KNM-WT 40000
Fred Spoor1,2,*, Meave G. Leakey3,4 and Louise N. Leakey3,5
1
Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz
6, 04103 Leipzig, Germany
2
Department of Cell and Developmental Biology, University College London, UK
3
Koobi Fora Research Project, Nairobi, Kenya
4
Department of Anatomical Sciences, and
5
Department of Anthropology, Stony Brook University, New York, USA
The 3.5-Myr-old hominin cranium KNM-WT 40000 from Lomekwi, west of Lake Turkana, has
been assigned to a new hominin genus and species, Kenyanthropus platyops, on the basis of a
unique combination of derived facial and primitive neurocranial features. Central to the diagnosis
of K. platyops is the morphology of the maxilla, characterized by a flat and relatively orthognathic
subnasal region, anteriorly placed zygomatic processes and small molars. To study this morphology
in more detail, we compare the maxillae of African Plio-Pleistocene hominin fossils and samples of
modern humans, chimpanzees and gorillas, using conventional and geometric morphometric
methods. Computed tomography scans and detailed preparation of the KNM-WT 40000 maxilla
enable comprehensive assessment of post-mortem changes, so that landmark data characterizing
the morphology can be corrected for distortion. Based on a substantially larger comparative
sample than previously available, the results of statistical analyses show that KNM-WT 40000 is
indeed significantly different from and falls outside the known range of variation of species of
Australopithecus and Paranthropus, contemporary Australopithecus afarensis in particular. These
results support the attribution of KNM-WT 40000 to a separate species and the notion that
hominin taxonomic diversity in Africa extends back well into the Middle Pliocene.
Keywords: human evolution; Pliocene; Africa; Kenyanthropus platyops; maxilla; geometric
morphometrics

1. INTRODUCTION these fossils is considered to be within the range of

Whether or not the Pliocene hominin fossil record
from Hadar (Ethiopia) and Laetoli (Tanzania) rep-
resents more than one species was the subject of
ongoing debate in the 1980s (see Boaz 1988 for a
review). Recovery of additional fossils and studies of
intraspecific variation and temporal trends have sub-
sequently resulted in a broad consensus supporting
the interpretation of a single, sexually dimorphic
species, Australopithecus afarensis (Lockwood et al.
1996, 2000; Kimbel et al. 2004; Kimbel & Delezene
2009). However, fossils found at two other sites have
reopened the debate of species diversity in the African
Middle Pliocene. A partial mandible and upper pre-
molar, discovered in 1994 in the Koro-Toro area of
Chad and approximately 3.5 Myr old, have been
assigned to a new species, Australopithecus bahrelghazali
(Brunet et al. 1995, 1996). This attribution has been
questioned as the limited morphology preserved by
* Author for correspondence (f.spoor@eva.mpg.de).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rstb.2010.0042 or via http://rstb.royalsocietypublishing.org.
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
variation of A. afarensis (White et al. 2000; Ward
et al. 2001; Kimbel 2007; Wood & Lonergan 2008).
However, a detailed analysis of symphyseal shape of
both the type specimen and a previously unpublished
second mandible supports a separate specific status
(Guy et al. 2008).
A second site providing possible evidence for
species diversity is Lomekwi, west of Lake Turkana
(Kenya). Fieldwork in the early 1980s and late 1990s
resulted in hominin discoveries dated between 3.5
and 3.2 Ma, including a well-preserved temporal
bone, 2 partial maxillae, 3 partial mandibles, 44
isolated teeth and a largely complete although dis-
torted cranium, KNM-WT 40000 (Brown et al.
2001; Leakey et al. 2001). Several of these specimens
were found to show a morphology markedly different
from that of contemporary A. afarensis (Leakey et al.
2001). Accordingly, the cranium and one fragmentary
maxilla were assigned to a new genus and species,
Kenyanthropus platyops, based on a unique combi-
nation of derived facial and primitive neurocranial
features (Leakey et al. 2001). A number of recent
studies and reviews have cautiously considered
K. platyops as a valid taxon (Strait & Grine 2004;
Kimbel 2007; Cobb 2008; Nevell & Wood 2008;

3377 This journal is q 2010 The Royal Society

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3378 F. Spoor et al. The maxilla of KNM-WT 40000
Wood & Lonergan 2008). On the other hand, White
(2003) questioned the taxon’s validity, and the
notion of Pliocene hominin diversity. In his view it
cannot be excluded that KNM-WT 40000 is an
early Kenyan variant of A. afarensis, given the distor-
tion of the specimen and the known cranial variation
in early hominin species and among modern apes
and humans.
Central to the diagnosis of K. platyops is the mor-
phology of the maxilla, characterized by a flat and
relatively orthognathic subnasal region, an anteriorly
placed zygomatic process and small molars. In the pre-
sent study, this morphology, as shown by KNM-WT
40000, is investigated in more detail. We made quan-
titative comparisons, using geometric morphometric
and univariate methods, with Plio-Pleistocene homi-
nin fossils from Ethiopia, Kenya, Tanzania and
South Africa and with samples of modern humans,
gorillas and chimpanzees. Such analyses are obviously
affected by the post-mortem distortion of KNM-WT
40000, the reason the initial description provided
limited metric comparisons only (Leakey et al. 2001).
The impact of the preservation of the maxilla was
therefore evaluated in detail using new evidence
based on additional preparation of the specimen and
computed tomography (CT). The information thus
obtained was used to adjust landmarks representing
the key morphological features. In statistical analyses
the morphology of the specimen is considered both
in its preserved form and corrected for distortion.
Using a substantially larger comparative sample
than available to Leakey et al. (2001), the present
study aims to assess two specific hypotheses.
1. KNM-WT 40000 does not differ significantly from
A. afarensis with respect to the morphological fea-
tures of the maxilla included in the differential
diagnosis of K. platyops (Leakey et al. 2001).
Rejection of this null hypothesis would provide
evidence for species diversity in eastern Africa at
around 3.5 Ma.
2. KNM-WT 40000 does not differ significantly from
species of Australopithecus and Paranthropus with
respect to the morphological features of the maxilla
included in the differential diagnosis of K. platyops
(Leakey et al. 2001). Rejection of this null
hypothesis would support the attribution of
KNM-WT 40000 to a separate species.
2. MATERIAL AND METHODS
In geometric morphometric shape analyses the KNM-
WT 40000 maxilla was compared with all available
hominin specimens attributed to Australopithecus and
Paranthropus that preserve the morphology concerned.
These are: Australopithecus anamensis (KNM-KP
29283), A. afarensis (A.L. 199-1, A.L. 200-1, A.L.
417-1, A.L. 427-1, A.L. 444-2 and A.L. 486-1),
Australopithecus africanus (MLD 9, Sts 52, Sts 71 and
Stw 498), Australopithecus garhi (BOU-VP-12/130),
Paranthropus aethiopicus (KNM-WT 17000), Paran-
thropus boisei (OH 5) and Paranthropus robustus
(SK 11, SK 12, SK 13, SK 46, SK 48, SK 83
and SKW 11). All are adults, with the exception of
Phil. Trans. R. Soc. B (2010)
A.L. 486-1, Sts 52, OH 5, SK 13 and SKW 11,
which are subadults (third molars not in occlusion).
The intraspecific variation in maxillary shape
among the fossils was examined by making compari-
sons with samples of modern humans and African
great apes. The modern human sample consists of
55 specimens (sex mostly unknown), representing
indigenous populations from all six widely inhabited
continents, housed at the Natural History Museum
(London) and at the Department of Cell and Develop-
mental Biology at University College London. The
African ape samples (all non-captive) include 50
specimens of the eastern lowland gorilla (Gorilla gorilla
gorilla; 26 males, 24 females) and 61 specimens of
chimpanzee (Pan troglodytes, all subspecies rep-
resented; 28 males, 33 females) from the collections
of the Powell Cotton Museum (Birchington), the
Royal College of Surgeons (London), the Natural
History Museum (London) and the Department of
Cell and Developmental Biology at University College
London. Specimens are adult and lack signs of
substantial pathology, of the alveolar process of the
maxilla in particular.
CT was used to examine internal morphology
and record surface landmarks of some of the fossil
specimens. KNM-WT 40000 was scanned with a
Siemens AR.SP medical scanner at the Diagnostic
Center, Nairobi (Kenya). Scans in sequential mode
were made in the transverse plane, parallel to the
postcanine alveolar margin, using a slice thickness
and increment of 1.0 mm. Images were reconstructed
with a SP90 kernel, extended CT-scale and a
0.17 mm pixel size. The tooth roots were segmented
by Kornelius Kupczik and the first author. New CT
data with improved spatial resolution (isotropic voxel
size 0.069 mm) were obtained more recently with the
portable BIR ACTIS 225/300 high-resolution
industrial CT scanner of the Department of Human
Evolution at the Max Planck Institute for Evolutionary
Anthropology (Leipzig, Germany), at the time
installed at the National Museums of Kenya in
Nairobi. Other CT data of hominin fossils used here
are from the digital archives of the National Museums
of Kenya, and the Department of Anthropology,
University of Vienna. Visualization of the CT datasets
was done using AMIRA 4.1.2 (Mercury Computer
Systems).
A set of maxillary landmarks was selected using
three criteria: (i) they should quantify the features
used in the differential diagnosis of K. platyops; (ii) it
should be possible to take these landmarks from the
KNM-WT 40000 maxilla and correct them for distor-
tion of the specimen; and (iii) the number of fossil
specimens used in the comparative sample should be
as large as possible. Optimizing all three criteria
resulted in the selection of five two-dimensional land-
marks, taken from the specimens projected in lateral
view: nasospinale (ns), prosthion (pr), the buccal
alveolar margin between the canine and third premolar
(pc), the buccal alveolar margin between the second
and third molar (m23) and the antero-inferior take-
off of the zygomatic process (azp), a point most
anterior, inferior and medial on the root of the process
(figure 1). These landmarks quantify the orientation of
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
The maxilla of KNM-WT 40000
(a)
ns azp
pr
pc m23
(b)
Figure 1. CT-based parallel-projected 3D reconstructions
comparing the maxillae in lateral view of (a) A.L. 200-1
(reversed right side of cast, Australopithecus afarensis) and
(b) KNM-WT 40000 (left side of original, Kenyanthropus
platyops). The five landmarks are shown, together with the
connecting wire frame used in figure 3 (see text for the
abbreviations of the landmarks). The broken surface of the
zygomatic process of KNM-WT 40000 facing laterally is
not visualized to emphasize the outline compared with the
equivalent morphology in A.L. 200-1. Scale bar, 10 mm.
the subnasal clivus in the midsagittal plane (ns-pr),
the anterior zygomatic process position along the post-
canine tooth row (azp relative to pc-m23) and the
degree of anterior projection and transverse flatness
of the subnasal clivus (pr – pc or sagittally projected
length of the canine and incisor alveolar margin).
The five landmarks were mostly recorded from digi-
tal images of the specimens in exact lateral view and
taken with a focal distance of 1 – 2 m to minimize par-
allax artefacts. Nasospinale and prosthion may not be
visible in this view and are indicated by markers (see
Spoor et al. 2005 for details of this method). The land-
marks of KNM-WT 40000, A.L. 444-2, Sts 52a,
Sts 71, KNM-WT 17000 and OH 5 were taken from
CT datasets, using AMIRA 4.1.2 (Mercury Computer
Systems) to obtain parallel-projected three dimen-
sional surface reconstructions in a lateral view and
sagittal sections to locate nasospinale and prosthion.
The left side of the extant specimens was used, the
mean of both sides of A.L. 200-1 and OH 5 and the
best preserved side of the other fossils (left for
KNM-WT 40000). All landmark coordinates were
recorded with IMAGEJ 1.42d (National Institutes of
Health, USA).
To examine the impact of the distortion of KNM-
WT 40000 on the landmark positions, additional
surface preparation was done of the anterior and
lateral aspects of the left maxilla. Small remnants of
the matrix on the bone surface were removed and
cracks fully exposed. Bone edges on either side of the
crack could thus be matched, identifying possible
Phil. Trans. R. Soc. B (2010)
F. Spoor et al. 3379
shifts along the crack. Moreover, the width of the
cracks along specific trajectories linking the five land-
marks (figure 2a,d ) were measured to the nearest
tenth of a millimetre with digital callipers, making
sure that the distance was taken between matching
edges. The midsagittal surface area above prosthion
is not well preserved, and the expansion of the subna-
sal clivus in the sagittal plane was examined more
laterally along a line from the I2/C interalveolar
septum to the left lower corner of the nasal aperture
(figure 2a). The crack widths were used to calculate
the percentage of surface expansion between the five
landmarks, and the x and y coordinates were adjusted
accordingly. Both preparation and measurements were
done under a binocular microscope, using acetone to
temporarily enhance the difference between bone
and matrix.
Generalized procrustes analyses of the landmark
coordinates and principal component analyses (PCAs)
of the output were performed with MORPHOLOGIKA
2.5 (O’Higgins & Jones 1998). With this software,
the maxillary shape variation associated with each prin-
cipal component (PC) can be explored visually by
morphing a wireframe of the five landmarks according
to the position on a bivariate plot of two PCs. F-tests
and t-tests of the individual PC scores, with sequential
Bonferroni correction for multiplicity (Rice 1989), were
done using PAST 1.93 (Hammer et al. 2001) and
MS EXCEL 2003. One-tailed distributions were used
in the t-tests when the hypotheses and the species
diagnosis of K. platyops specifically state the nature
of a possible difference (e.g. KNM-WT 40000 is
subnasally less prognathic than A. afarensis). Conse-
quently, two-tailed distributions were used only for
the comparison of PCs related to zygomatic process
position in KNM-WT 40000 and P. robustus, where
there is no prior prediction of the nature of the differ-
ence. KNM-WT 40000 was also compared with
species individually by combining all PCs obtained in
separate analyses of KNM-WT 40000 and each
species. The Mahalanobis’ distance of KNM-WT
40000 from the centroid of the species sample is
compared with the distances from that centroid of
the specimens in the sample (software written by
Paul O’Higgins, Hull York Medical School, UK).
All statistical analyses were done separately for
KNM-WT 40000 in its preserved form and corrected
for distortion.
A drawback of the landmark-based approach is that
it limits the number of specimens that can be included.
That is because each must preserve the full area
covered by the landmarks, whereas less complete
specimens may be informative regarding individual
diagnostic aspects of the K. platyops maxilla. When
interpreting the main shape analysis, two maxillary
features were therefore considered individually as
well, to assess consistency among a larger number of
fossils than those preserving all five landmark
locations. The subnasal clivus angle marks the orien-
tation in the sagittal plane of the segment
nasospinale to prosthion relative to the postcanine
alveolar margin, up to the M2/M3 septum. It was
measured using IMAGEJ from digital images or
CT-based visualizations of a specimen in a lateral
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3380 F. Spoor et al. The maxilla of KNM-WT 40000

(a) (b)

P3

ns

M2

pr
(c)
(e) M

(d)
6%

18%

20%

18%

16%

Figure 2. Distortion of KNM-WT 40000. (a) Anterior view, giving the midline (black line) to indicate the midface skewing,
left nasospinale (ns), prosthion (pr) and the trajectory used to calculate the height expansion of the subnasal area (white line).
(b) CT-based 3D reconstruction of the maxilla in superior view, showing the tooth roots inside the translucent bone. (c) A
high-resolution sagittal CT image through the buccal roots of the left P3 to M2 (orientation indicated by the black line
in (b)). The thin black lines mark a longer crack through the premolar roots. (d) Lateral view of the left maxilla, showing
the pattern of matrix-filled cracks highlighted by wetting with acetone. The five landmarks are shown as in figure 1. The tra-
jectories along which crack widths were measured are given by lines with associated percentages of expansion (black line refers
to the subnasal trajectory shown in (a)). (e) The right M2 crown (M, mesial; B, buccal), with black lines marking the endpoint
of cracks highlighted with acetone. The white lines indicate the match at the mesial end of the widest crack. The dark area on
the mesiolingual corner is a strong shadow of the enamel more distally, rather than damage to the dentine. Scale bars,
(a,b) 30 mm, (c,d ) 10 mm and (e) 3 mm.

view, where feasible estimating the postcanine alveolar
margin orientation if the exact position of landmarks
pc or m23 is not preserved. Furthermore, the anterior
position of the zygomatic root is considered relative
to the dental row, following Lockwood & Tobias
(1999, table 7). These features were recorded by the
authors from the original specimens, with additional
observations regarding zygomatic root position in
A. afarensis provided by William H. Kimbel (Arizona
Sate University, USA).
Finally, the crown size of the right M2 was assessed
on the basis of conventional mesiodistal and buccolin-
gual measurements, defined in two different ways
Phil. Trans. R. Soc. B (2010)
(Tobias 1967; White 1977). Full preparation of the
M2 crown had been done at the time of the first
announcement (Leakey et al. 2001), and measure-
ments of cracks affecting the length and width had
been taken at the time. Comparative data of M2
size in Plio-Pleistocene hominins were taken from the
literature, combined with our own measurements.
3. PRESERVATION OF THE MAXILLA
The facial parts of KNM-WT 40000 show post-
mortem distortion in the form of lateral skewing of
the nasal area and a network of matrix-filled surface
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The maxilla of KNM-WT 40000 F. Spoor et al. 3381

(a) SKW11* 0.15

0.10 Stw498
SK13*
Sts71
KP29283
WT17k 0.05
BOUVP12/130
MLD9
OH5* Sts52*
PC1
–0.1 0.1 AL486-1*
SK83 WT40k
SK12 AL200-1
–0.05 AL427-1

SK11 SK46
–0.10 AL199-1
AL417-1
AL444-2

PC2

(b) 0.06 WT40k

AL199-1
Stw498
SK12 AL200-1
0.02 SK13*
SKW11*

AL427-1 SK11
PC4 OH5*
–0.075 AL417-1 0.05
Sts71
KP29283 SK83 MLD9 Sts52*
AL444-2
AL486-1* SK46
BOUVP12/130
–0.04
WT17k

PC5

0.3
(c)

A. africanus 0.2
H. sapiens

P. troglodytes
WT40k
PC1
–0.6 –0.2

P. robustus G. gorilla
–0.2
A. afarensis
–0.3
PC2

Figure 3. Bivariate plots of PCs. (a) PC2 against PC1 and (b) PC5 against PC4 of the fossils samples. (c) PC2 against PC1 of
the combined fossil and extant samples. KNM-WT 40000 (black dot) is corrected for distortion. The prefix KNM- of the
Kenyan specimens is omitted, and an asterisk indicates subadults. Convex hulls are given for A. afarensis (solid line),
A. africanus (dash-dot line) and P. robustus (dashed line), as well as in (c), the 95% confidence ellipses of these taxa and the
extant species (solid line). The grey-shaded wire frames in (a,b) are defined in figure 1 and indicate the maxillary shapes
represented at the extremes of the PC axes. See the main text for the percentage of variance represented by each PC.

Phil. Trans. R. Soc. B (2010)

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3382 F. Spoor et al. The maxilla of KNM-WT 40000
cracks associated with clay-induced expansion mainly
affecting the alveolar and zygomatic processes
(Leakey et al. 2001; figure 2a,d ). Before assessing the
degree of expansion in the landmarked part of the
maxilla, it is worth considering whether this area
shows any evidence of substantial post-mortem shape
changes as well. A good indicator of structural integ-
rity of the alveolar process is the internal
preservation of the tooth roots. Those present, of the
left I1 to M2 and the right C to M3, are visualized in
a CT-based three dimensional reconstruction of the
maxilla in superior view (figure 2b). The roots are
well preserved, without distinct misalignments or dis-
tortion, and the dental arcade is symmetrical in
shape. The only exception is the largely exposed
right canine root which is in the correct position at
the alveolar margin, but the apex is tilted anteriorly.
A more detailed view of the internal preservation of
the left maxilla is provided by a high-resolution sagittal
CT image through the buccal roots of the left P3 to M2
(figure 2c). Several fine cracks through the roots can be
seen, and the mesiobuccal root canal of the M2 is
expanded, but this is not accompanied by substantial
displacement of the root parts on opposite sides
of the cracks. The mesiodistal distance between the
P4, M1 and M2 is increased by matrix expansion,
particularly of the alveolar space around the roots.
However, this is less so between the P3 and P4.
Overall, the internal CT evidence suggests a pattern
of expansion without substantial shape changes due
to skewing or other directional deformation. The
well-preserved state of the premolar root area is of
particular importance as it indicates that the overlying
anterior zygomatic process position is unlikely to have
been altered by the distortion. This is further con-
firmed by the absence of major shifts of surface bone
fragments between the premolar alveolar margin and
the anterior zygomatic root.
The percentages of bone expansion along the
measured trajectories vary from 16 per cent along the
postcanine alveolar margin to 20 per cent transversely
over the canine jugum (figure 2d). The one exception
is the area superior to the canine alveolus where the
expansion in transverse direction is only 6 per cent.
The right M2 crown is shown in figure 2e. The
widest crack runs from the mesial interstitial facet to
the distolingual corner, a second shorter one from
the central area of the main break to the lingual
crown margin and a third thin one from the central
area to the distal interstitial facet. Enamel and occlusal
dentine edges of the breaks provide good clues regard-
ing the match of the four parts they delineate. A refit of
the crown would require the two lingual parts to
be moved buccally, the triangular distolingual part to
be moved mesially and the mesiolingual part to be
moved slightly distally. Closing the cracks would
result in an estimated 1.2 mm reduction of the bucco-
lingual width of the crown. The mesiodistal length
along the crown axis (White 1977) is not affected
by the cracks, and has only been corrected for an esti-
mated 0.5 mm of mesial interstitial wear. However,
the maximum length (Tobias 1967) requires correction
for the 0.7 mm distal displacement of the triangular
distolingual part. The buccolingual width is not
Phil. Trans. R. Soc. B (2010)
affected by occlusal wear as it has not reached the
level of maximum bulging of the buccal and lingual
surfaces. The recently acquired high-resolution CT
scans will provide the opportunity to prepare a full
three dimensional virtual reconstruction of the right
M2 crown.
4. MORPHOMETRIC COMPARISONS
The PCA of the hominin fossil sample described here
uses the corrected landmark configuration of KNM-
WT 40000 (table 1). The first six PCs account for
99.9 per cent of the variation. Although PC3 – PC6
contribute less than 10 per cent each, these were still
assessed because KNM-WT 40000 could specifically
differ from the other fossils in morphology that is
less variable among the Australopithecus and Paranthro-
pus specimens which dominate the sample. PC1, PC2,
PC4 and PC5 were found to provide evidence in
relation to the hypotheses examined here, and these
are shown in bivariate plots (figure 3), with wireframes
marking the shapes represented at either end of each
axis. PC3 and PC6 will be briefly described as well.
PC1 (eigenvalue 0.0263; 72% of variance) rep-
resents the variation in anteroposterior position of
the anterior zygomatic process (landmark azp) and
the relative length and transverse flatness of the subna-
sal clivus (ns– pr and pr – pc, respectively). PC1
separates Australopithecus species, with a more poster-
iorly positioned zygomatic and a shorter and
transversely curved (projecting) subnasal clivus, from
Paranthropus species, with a more anteriorly positioned
zygomatic and a longer and transversely flat subnasal
clivus (figure 3a). Addressing hypothesis 1, the PC1
score of KNM-WT 40000 differs significantly from
that of A. afarensis (table 1), reflecting its more ante-
riorly placed zygomatic and a subnasal clivus that is
transversely flat. When compared with multiple species
(hypothesis 2), the difference between KNM-WT
40000 and A. afarensis is statistically significant, as is
the difference from A. africanus. The PC1 scores
suggest that KNM-WT 40000 is intermediate between
Australopithecus and Paranthropus with respect to this
particular morphology. However, the difference from
P. robustus is not statistically significant, with the suba-
dult SKW 11 having a score close to KNM-WT 40000.
PC2 (eigenvalue 0.0054; 15% of variance) rep-
resents both the inferosuperior and anteroposterior
position of the zygomatic process and the length of
subnasal clivus. This PC separates A. afarensis, with
a more inferoposteriorly positioned zygomatic and
longer subnasal clivus, from A. africanus, with a
more anterosuperiorly positioned zygomatic and
shorter clivus (figure 3a). KNM-WT 40000 and
A. garhi are intermediate, A. anamensis falls with
A. africanus, and Paranthropus specimens show the
full range of PC2-related morphological variation.
KNM-WT 40000 is not significantly different from
A. afarensis (hypothesis 1) or from other hominin
species more in general (hypothesis 2).
PC3 (eigenvalue 0.0029; 8% of variance) purely
represents the inferosuperior height of landmark azp,
the anterior zygomatic root position, above the postca-
nine alveolar margin. KNM-WT 40000 does not differ
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The maxilla of KNM-WT 40000 F. Spoor et al. 3383

Table 1. PCs of the maxillary shape analysis. The landmarks of KNM-WT 40000 are corrected for distortion. The sample
size (n), mean, minimum, maximum and standard deviation (s.d.) are given, and the comparisons of KNM-WT 40000 by
t-test list the probability ( p; one-tailed, except þtwo-tailed) and the significance (multiple comparisons after sequential
Bonferroni correction). n.s., not significant; *p , 0.05; **p , 0.01.

PC1 PC2 PC4 PC5

KNM-WT 40000 20.068 20.003 0.049 0.065

A. anamensis n¼1 0.167 0.064 20.045 20.009
A. afarensis n 6 6 6 6
mean 0.1285 20.0742 20.0012 0.0014
min. 0.053 20.129 20.024 20.030
max. 0.198 20.001 0.018 0.038
s.d. 0.0623 0.0498 0.0136 0.0262
A. garhi n¼1 0.178 0.029 20.011 20.027
A. africanus n 4 4 4 4
mean 0.1065 0.0558 0.0076 20.0004
min. 0.064 0.025 20.046 20.015
max. 0.152 0.092 0.043 0.030
s.d. 0.0401 0.0316 0.0382 0.0208
P. aethiopicus n¼1 20.152 0.068 20.010 20.040
P. robustus n 6 6 6 6
mean 20.1879 0.0073 20.0040 0.0014
min. 20.259 20.070 20.087 20.024
max. 20.070 0.142 0.048 0.019
s.d. 0.0654 0.0855 0.0488 0.0169
P. boisei n¼1 20.194 0.020 0.018 20.005
comparison with A. afarensis
p 0.016 0.120 0.010 0.037
sign. * n.s. ** *
comparison with Australopithecus and Paranthropus
A. afarensis p 0.016 0.120 0.010 0.037
sign. * n.s. * *
A. africanus p 0.015 0.098 0.204 0.034
sign. * n.s. n.s. n.s.
P. robustus p 0.151þ 0.919þ 0.182 0.009
sign. n.s. n.s. n.s. *

significantly from A. afarensis, A. africanus or
P. robustus, and this morphology does not relate to
the hypotheses.
PC4 (eigenvalue 0.0011; 3% of variance) represents
the subnasal clivus orientation associated with vari-
ations in the midline area only, as shown by the
angle of ns– pr to the entire alveolar margin (pr – pc –
m23; figure 3b). KNM-WT 40000 has the highest
score in the sample and is significantly less prognathic
than A. afarensis (table 1). When compared with mul-
tiple species, this difference from A. afarensis is
statistically significant as well, but differences from
A. africanus and P. robustus are not.
PC5 (eigenvalue 0.0006; 2% of variance) represents
the subnasal clivus orientation associated with vari-
ations of the entire subnasal area. The midline clivus
(ns– pr) and the canine – incisor alveolar margin (pr –
pc) jointly vary in orientation relative to the postcanine
alveolar margin (pc – m23; figure 3b). KNM-WT
40000 is by far the most orthognathic in the sample,
and the difference from A. afarensis is statistically sig-
nificant (table 1, figure 3b). When compared with
multiple species, KNM-WT 40000 is significantly
different from A. afarensis and P. robustus.
PC4 and PC5 jointly contribute to an overall pat-
tern of differences in subnasal prognathism in the
fossil sample (figure 3b). KNM-WT 40000 is the
most orthognathic, whereas the P. aethiopicus specimen
KNM-WT 17000, the A. garhi type BOU-VP-12/130
and the A. anamensis specimen KNM-KP 29283
are the most prognathic. The other species of
Australopithecus and Paranthropus do not differ notably.
PC6 (eigenvalue 0.0003; 1% of variance) represents
the angle and length proportions between the alveolar
margins of the anterior (canine – incisor) and postca-
nine teeth. There is no separation between taxa, and
KNM-WT 40000 does not differ significantly from
A. afarensis, A. africanus and P. robustus.
Using the landmark configuration of KNM-WT
40000 as preserved rather than corrected for distortion
results in PC scores that are only marginally different
from those reported in table 1. Significance levels of
the t-tests are the same as for the corrected landmarks,
except for multiple species comparisons of PC5 with
A. afarensis and A africanus (electronic supplementary
material, S1). When excluding the five subadult speci-
mens from the fossil samples, KNM-WT 40000 differs
significantly from A. afarensis for PC1, 4 and 5, as

Phil. Trans. R. Soc. B (2010)

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3384 F. Spoor et al. The maxilla of KNM-WT 40000

Table 2. Mahalanobis’ distance test comparing KNM-WT Table 3. Interspecific comparisons of the standard deviations
40000 using all PCs combined. D 2, squared Mahalanobis’ of PC1 and PC2 obtained in the maxillary shape analysis,
distance of KNM-WT 40000 from centroid of species giving F and probability ( p) values. The differences are not
sample; SDU, standard deviation unit of Mahalanobis’ statistically significant after sequential Bonferroni correction.
distances within the sample; d.f., degrees of freedom; p,
probability that KNM-WT 40000 belongs to the species. PC1 PC2
For sample sizes less than six, the probability is not
calculated (n/a) because estimates of the variance are F p-value F p-value
insufficiently reliable.
A. afarensis –H. sapiens 1.010 0.865 1.441 0.450
D2 SDU d.f. p-value A. afarensis –P. troglodytes 1.083 0.758 1.192 0.648
A. afarensis –G. gorilla 1.371 0.503 1.368 0.505
KNM-WT 40000 (corrected) A. africanus –H. sapiens 1.570 0.811 2.233 0.560
A. afarensis 21.065 4.589 6 ,0.0025 A. africanus –P. troglodytes 1.435 0.885 2.698 0.451
A. africanus 37.084 6.089 4 n/a A. africanus –G. gorilla 1.134 0.914 2.351 0.529
P. robustus 13.284 3.644 6 ,0.05
P. robustus–H. sapiens 1.023 0.827 2.954 0.040
KNM-WT 40000 (as preserved) P. robustus–P. troglodytes 1.119 0.720 2.445 0.088
A. afarensis 18.909 4.348 6 ,0.005 P. robustus–G. gorilla 1.416 0.470 2.805 0.053
A. africanus 36.609 6.050 4 n/a
P. robustus 13.738 3.706 6 ,0.05
KNM-WT 40000 (corrected), adults only 40000 than in A. afarensis (table 4). When compared
A. afarensis 33.088 5.752 5 n/a with multiple species of Australopithecus and Paranthro-
A. africanus 28.397 5.328 3 n/a pus, its mesiodistal length is only significantly smaller
P. robustus 20.390 4.515 4 n/a than in P. boisei, but its buccolingual width is smaller
than in all species other than A. anamensis.

before, but for PC2 as well (electronic supplementary

material, S2). When compared with multiple species,
KNM-WT 40000 differs significantly from A. afarensis
for PC4 and from P. robustus for PC1.
Results of Mahalanobis’ distance tests comparing
KNM-WT 40000 with A. afarensis, A. africanus and
P. robustus individually, and using all PCs combined,
are given in table 2. Differences from A. afarensis
and P. robustus are statistically significant, whereas the
A. africanus sample is too small for a probability to
be calculated.
A PCA of the fossil hominins combined with
modern humans, chimpanzees and gorillas shows
how the main aspects of variation of the fossil samples,
as reflected by PC1 and PC2 (48% and 19% of the
variance), compare with those shown by larger
samples of extant species. A bivariate plot of PC2
against PC1 shows that the areas of observed variation
(convex hulls) of A. afarensis and P. robustus are not
substantially different from those of the extant species,
whereas A. africanus, with fewer specimens in the
sample, appears somewhat less variable (figure 3c).
With samples sizes of 50 or more, 95% confidence
ellipses of the extant species have a close fit with the
observed variation, but for the small fossil samples
the ellipses are large. Importantly, F-tests indicate
that the standard deviations of PC1 and PC2
obtained for the fossil taxa are not significantly differ-
ent from those of the extant species (table 3).
The M2 crown size of KNM-WT 40000 falls below
the currently known range of variation of all hominin
species included in the comparisons (table 4). Its
mesiodistal length is the same as the minimum
known for A. anamensis, but the particular specimen
has a larger buccolingual width than KNM-WT
40000 (KNM-ER 30200: 13.2 as opposed to 12.4).
Statistically, both the mesiodistal length and buccolin-
gual width are significantly smaller in KNM-WT
Phil. Trans. R. Soc. B (2010)
5. DISCUSSION
The taxonomic diagnosis of K. platyops and initial
description of its type specimen KNM-WT 40000
were mainly based on qualitative comparisons
(Leakey et al. 2001). Here we analyse the maxilla of
KNM-WT 40000 quantitatively and test the specific
hypotheses that the specimen is not different from
the contemporary taxon A. afarensis and, more
broadly, that it is not different from species of Austra-
lopithecus and Paranthropus. Based on the analyses of
maxillary shape and M2 crown size, both hypotheses
can be rejected. These findings thus support the
notion that there was hominin species diversity in the
Middle Pleistocene and corroborate the validity of
K. platyops as a separate species. It is worth pointing
out that the observed differences are substantial,
given that statistical significance is obtained for small
samples, with Bonferroni corrections when comparing
KNM-WT 40000 with multiple species. Moreover,
comparisons of the A. afarensis, A. africanus and
P. robustus samples used here with larger samples of
modern humans, chimpanzees and gorillas indicate
that these fossils show representative levels of intraspe-
cific morphological variation. Hence, the observed
differences from KNM-WT 40000 are unlikely to be
an artefact of under-sampled variation in the three
fossil species.
The observation by Leakey et al. (2001) that the M2
crown size of KNM-WT 40000 is smaller than the
known range of variation shown by species of Australo-
pithecus and Paranthropus is upheld here based on the
largest sample currently available. The difference is
most distinct for the buccolingual width. This is the
more reliable measure in KNM-WT 40000 as it is
not affected by interstitial or occlusal wear, and the
crack expanding the width is well defined and can be
corrected for with confidence.
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The maxilla of KNM-WT 40000 F. Spoor et al. 3385

Table 4. Mesiodistal (MD) length and buccolingual (BL) width of the M 2, and the subnasal clivus (ns-pr) angle to the
postcanine alveolar margin. The sample size (n), mean, minimum, maximum and standard deviation (s.d.) are given.
Comparisons by t-test of KNM-WT 40000 with hominin species list the probability ( p, one-tailed) and significance (n.s.,
not significant; multiple comparisons with sequential Bonferroni correction). MD1 and BL1 defined after White (1977),
MD2 and BL2 after Tobias (1967). The subnasal clivus angle was measured among adult and subadult specimens (M 2 in
full occlusion) listed in the electronic supplementary material, S3. *p , 0.05; **p , 0.01; ***p , 0.001.

M 2 size
subnasal
MD1 MD2 BL1 BL2 source angle

KNM-WT 11.4 11.9 12.4 12.8 Leakey et al. (2001), this study 47
40000
A. anamensis n 8 — 8 — Ward et al. (2001), White et al. (2000) 1
mean 12.88 14.50 27
min. 11.4 12.9
max. 14.3 16.7
s.d. 1.04 1.19
A. afarensis n 12 — 13 — Kimbel & Delezene (2009) 6
mean 13.00 14.80 34.6
min. 12.1 13.4 29
max. 14.1 15.8 39
s.d. 0.60 0.60 3.5
A garhi n¼1 14.4 — 17.7 — Asfaw et al. (1999) 27
A. africanus n — 24 — 28 Moggi-Cecchi et al. (2006), J. Moggi-Cecchi 9
mean 14.12 15.95 (2006, personal communication), this study 34.2
min. 12.6 13.5 30
max. 16.6 17.9 37
s.d. 1.09 1.23 1.9
P. aethiopicus n¼1 — — — — 31
P. robustus n — 24 — 24 J. Moggi-Cecchi (2006, personal communication), 8
mean 14.00 15.73 this study 36.8
min. 11.6 14.0 32
max. 15.7 16.9 39
s.d. 0.99 0.94 4.1
P. boisei n — 6 — 6 Tobias (1967), Leakey & Walker (1988), Wood 2
mean 15.84 18.18 (1991), this study 35.9
min. 14.7 16.6 33
max. 17.2 21.0 39
s.d. 1.03 1.55
comparison with A. afarensis
p 0.013 0.001 0.011
sign. * ** *
comparison with Australopithecus and Paranthropus
A. anamensis p 0.111 0.073
sign. n.s. n.s.
A. afarensis p 0.013 0.001 0.011
sign. n.s. ** *
A. africanus p 0.029 0.010 0.000
sign. n.s. * ***
P. robustus p 0.024 0.003 0.024
sign. n.s. * *
P. boisei p 0.008 0.012
sign. * *

The geometric morphometric shape analysis of the
maxilla shows that zygomatic process position together
with subnasal clivus length and transverse flatness
account for most of the variance in the hominin
fossil sample (PC1 and PC2 combined, 86%,
figure 3a). PC1 associates a more anteriorly positioned
zygomatic process with a transversely flatter and
longer subnasal clivus, along a gradient of genera:
Paranthropus, Kenyanthropus (i.e. KNM-WT 40000)
and Australopithecus. In contrast, PC2 associates a
more anteriorly positioned zygomatic process with a
shorter subnasal clivus and separates A. afarensis
from A. africanus only. There is no evidence of
intraspecific differences within Paranthropus regarding
PC1 and PC2, as KNM-WT 17000 and OH 5 fall
in the middle of the range of P. robustus.
Apart from zygomatic root position and transverse
subnasal flatness, subnasal prognathism is a third

Phil. Trans. R. Soc. B (2010)

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3386 F. Spoor et al. The maxilla of KNM-WT 40000

Table 5. Anterior position of the zygomatic process along the dental row. Accession codes CH, ER, KP and WT lack the
prefix KNM-.

P3 P3/P4 P4 P4/M1 M1

A. anamensis KP 29283
A. afarensis A.L. 442-1 A.L. 58-22 A.L. 199-1
A.L. 200-1a A.L. 333-2
A.L. 333-1 A.L. 413-1
A.L. 427-1 A.L. 417-1d
A.L. 444-2 A.L. 822-1
A.L. 486-1a
A.L. 651-1
A. garhi BOU-VP-12/130
A. africanus Sts 52a MLD 6 MLD 9 Sts 5
MLD 45 TM 1511
Sts 17 TM 1512
Sts 52a TM 1514
Sts 53 Sts 63
Sts 71 Sts 3009
Stw Stw 13
252a,b Stw
Stw 391 183a,b
Stw 505 Stw 498
K. platyops WT 40000
WT 38350
P. aethiopicus WT 17000
P. robustus SK 13a TM 1517 DNH 7
SK 47a SK 48 SK 11
SK 821 SK 52a SK 12
SK 79 SK 29
SK 83 SK 46
SKW 11a SK 79
SKW 12
P. boisei KGA 10-525 KGA 10-525
CH 1Ba ER 405
ER 732 ER 406
WT 17400a OH 5
a
Immature specimen.
b
Listed as A. africanus, but affinities uncertain (Lockwood & Tobias 2002).

prominent aspect of maxillary shape characterizing
KNM-WT 40000. It is also expressed by two separate
patterns of variation (PC4 and PC5; figure 3b), which
differ depending on whether the clivus orientation
varies in the midline only (PC4), or involves the
entire subnasal area, from canine jugum to canine
jugum bilaterally (PC5). As most specimens in
the sample (P. robustus, P. boisei, A. afarensis and
A. africanus) tend to show similar levels of prognath-
ism, this morphology does account for only 5 per
cent of the variance in the total sample. However, it
does single out the orthognathic morphology of
KNM-WT 40000 and to a lesser extent the more prog-
nathic shape in A. anamensis, A. garhi and P. aethiopicus.
This pattern illustrates that in interspecific comparisons
the higher PCs associated with small amounts of
overall variance can provide highly relevant information
regarding individual specimens, because the distribution
of the variance depends on the sample composition.
In all, the analyses confirm the occurrence of three
different facial patterns among the early hominins con-
sidered here. Australopithecus is characterized by a
prognathic, transversely curved subnasal area com-
bined with posteriorly positioned zygomatics
(figure 1a), Paranthropus by a prognathic, transversely
Phil. Trans. R. Soc. B (2010)
flat subnasal area with anteriorly positioned zygo-
matics and Kenyanthropus by a more orthognatic,
transversely flat subnasal area with anteriorly
positioned zygomatics (figure 1b).
Two of the facial features, the degree of midline
subnasal prognathism and the position of the zygo-
matic process, can be quantified individually in a
larger number of early hominin specimens than
could be included in the geometric morphometric
analyses. It can thus be assessed whether the
evidence from larger samples is consistent with the
landmark-based results. The subnasal angle, which
combines the shape variation associated with PC4
and PC5, is larger in KNM-WT 40000 (478) than in
any of the Australopithecus and Paranthropus specimens
that could be measured (27– 398; table 4, electronic
supplementary material, S3). Those differences that
can be tested, from A. afarensis, A. africanus and
P. robustus, are statistically significant. The anterior
zygomatic root positions of early hominins, associated
with PC1 and PC2, are summarized in table 5.
The position in KNM-WT 40000 at the level of the
P3/P4 interalveolar septum is commonly found in
Paranthropus as well. On the other hand, it falls outside
the range of variation of Australopithecus, with the
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
The maxilla of KNM-WT 40000
exception of the left side of the subadult specimen Sts
52. Importantly, in A. afarensis, the position is always
more posterior, in one instance at the distal half of
P4, and more commonly at the P4/M1 septum or M1.
Hence, these univariate observations do fully confirm
the characterization of K. platyops as subnasally orthog-
nathic combined with anteriorly positioned zygomatics.
The A. afarensis specimen most similar in geological
age to KNM-WT 40000 is the Garusi 1 maxilla
(Laetoli approx. 3.6 Ma). It is too fragmentary to be
included in the PCA, or even to allow the quantification
of subnasal clivus orientation or zygomatic process pos-
ition. However, it is possible to make some inferences
about its morphology that are relevant here. There is
no evidence of the zygomatic root in the premolar
area, and the anterior position must thus have been at
P4/M1 or more posteriorly. Subnasally, Garusi 1 is
very prognathic, has rounded nasal margins around
the canine alveoli and lacks a clear nasal sill. In the
latter characters, it differs from the A. afarensis Hadar
sample and is more similar to A. anamensis (Kimbel
et al. 2006; Kimbel 2007), and in all these aspects,
Garusi 1 contrasts strongly with KNM-WT 40000.
KNM-WT 40000 is poorly preserved, and Leakey
et al. (2001) reported on the specimen by extracting
meaningful information from selected areas after care-
fully mapping the post-mortem distortion. Bone
expansion associated with clay-filled cracks is fre-
quently encountered among fossils found in the
Turkana Basin and has been routinely recognized as
a phenomenon affecting a specimen’s morphology
(e.g. the descriptions in Wood 1991). Naming it
expanding matrix distortion, White (2003) states to
have ‘formalized’ this taphonomic process, defining
five stages. He assigned KNM-WT 40000 to stage 4,
but as no definition of these stages has been published,
it is not possible to evaluate this classification. It is
worth pointing out that some areas of the cranium,
such as parts of the left temporal bone, show very
little distortion, whereas others, such as the cranial
vault, are highly affected. Thus, characterizing the
specimen by a single stage has little value.
The analyses presented here show that the distor-
tion has had little impact on the characters of
maxillary shape relevant to the diagnosis of K. platyops.
The preservation of the tooth roots and the integrity of
the dental arcade indicate that distinct directional
shape changes, such as skewing or compression, did
not occur in the lower part of the left maxilla. Expan-
sion cracks did cause a size increase of about 18 per
cent, but this occurred mostly at a similar rate across
the area, thus having little effect on shape. In all,
there is no indication that the position of the zygomatic
root or the subnasal clivus shape were modified sub-
stantially, particularly in a way that would mimic
normal morphological differences between species.
The only striking contrast in expansion rate was
found between the area above (6%) and over the left
canine jugum (20%). This difference is consistent
with the CT-based observation that internal expansion
is strongest in the alveolar space around the roots, a
phenomenon that is understandable as it becomes
readily filled with clay, unlike trabecular bone not
open to the outside. Moreover, positioned at the
Phil. Trans. R. Soc. B (2010)
F. Spoor et al. 3387
corner of the dental arcade, the canine alveolus has
more thin overlying bone than other teeth, making
the jugum particularly vulnerable to cracking.
Apart from the zygomatic process position, sub-
nasal clivus morphology and a small upper molar
size Leakey et al. (2001) also lists similarly sized I1
and I2 roots and upper premolars that are three-
rooted as features characterizing the maxilla of
K. platyops. These have not been considered here,
but warrant further study. The unusual incisor root
proportions (figure 2b) and their spatial relationship
to the transversely flat, orthognathic subnasal area is
of particular interest, and using high-resolution CT
this can now be examined in more detail.
The partial maxilla KNM-WT 38350 shares with
KNM-WT 40000 the anterior zygomatic root posi-
tion, three-rooted premolars and a small molar size
and was therefore designated as the paratype of
K. platyops (Leakey et al. 2001). However, it is too frag-
mentary a specimen to enable a full comparison with
the unique facial morphology of KNM-WT 40000.
The partial mandible KT12/H1, the holotype of the
broadly contemporary species A. bahrelghazali, is
characterized by a sagittally and transversely flat
anterior corpus, said to reflect a more orthognathic
face (Brunet et al. 1996). If correct, this would
increase the likelihood that KNM-WT 40000 and
KT12/H1 are conspecific. However, the association
between subnasal and symphyseal shapes is not well
understood (Spoor et al. 2005), and how K. platyops
relates to A. bahrelghazali remains unclear. Thus,
although there is good evidence, presented here and
elsewhere (Leakey et al. 2001; Guy et al. 2008), of
hominin species diversity in the Middle Pliocene of
Africa, additional fossils will be required to reveal the
full nature and interrelationships of the lineages
present at that time.
We thank Alan Walker and Chris Stringer for inviting us to
contribute this work and the National Museums of Kenya,
the National Museum of Ethiopia, the Transvaal Museum
(South Africa), Department of Anatomy, Witwatersrand
University (South Africa), the Institute of Human Origins
(USA) and the museums listed in §2 for access to
specimens in their care. We are grateful to Berhane Asfaw,
Michel Brunet, Ron Clarke, Nick Conard, Chris Dean,
Heidi Fouri, Philipp Gunz, John Harrison, Jean Jacques
Hublin, Louise Humphrey, Paula Jenkins, Don Johanson,
Andre Keyser, Bill Kimbel, Rob Kruszynski, Kornelius
Kupczik, the late Charlie Lockwood, Emma Mbua, Jacopo
Moggi-Cecchi, Sam Muteti, Paul O’Higgins, Matt Skinner,
Gen Suwa, Heiko Temming, Brian Villmoare, Tim White
and Andreas Winzer for help with various aspects of this
study. Financial support was provided by the Leakey
Foundation, the National Geographic Society and the Max
Planck Society.
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Phil. Trans. R. Soc. B (2010) 365, 3389–3396

doi:10.1098/rstb.2010.0059

Stable isotopes in fossil hominin tooth

enamel suggest a fundamental dietary shift
in the Pliocene
Julia A. Lee-Thorp1,*, Matt Sponheimer2, Benjamin H. Passey3,
Darryl J. de Ruiter4 and Thure E. Cerling5
1
Research Laboratory for Archaeology, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK
2
Department of Anthropology, University of Colorado at Boulder, 233 UCB, Boulder, CO 80309, USA
3
Department of Earth and Planetary Sciences, Johns Hopkins University, Baltimore, MD 21218, USA
4
Department of Anthropology, Texas A&M University, College Station, TX 77843, USA
5
Department of Geology and Geophysics, University of Utah, Salt Lake City, UT 84112, USA
Accumulating isotopic evidence from fossil hominin tooth enamel has provided unexpected
insights into early hominin dietary ecology. Among the South African australopiths, these data
demonstrate significant contributions to the diet of carbon originally fixed by C4 photosynthesis,
consisting of C4 tropical/savannah grasses and certain sedges, and/or animals eating C4 foods.
Moreover, high-resolution analysis of tooth enamel reveals strong intra-tooth variability in many
cases, suggesting seasonal-scale dietary shifts. This pattern is quite unlike that seen in any
great apes, even ‘savannah’ chimpanzees. The overall proportions of C4 input persisted for well
over a million years, even while environments shifted from relatively closed (ca 3 Ma) to open
conditions after ca 1.8 Ma. Data from East Africa suggest a more extreme scenario, where results
for Paranthropus boisei indicate a diet dominated (approx. 80%) by C4 plants, in spite of indi-
cations from their powerful ‘nutcracker’ morphology for diets of hard objects. We argue that
such evidence for engagement with C4 food resources may mark a fundamental transition in
the evolution of hominin lineages, and that the pattern had antecedents prior to the emergence
of Australopithecus africanus. Since new isotopic evidence from Aramis suggests that it was not pre-
sent in Ardipithecus ramidus at 4.4 Ma, we suggest that the origins lie in the period between 3 and
4 Myr ago.
Keywords: carbon isotopes; enamel; C4 resources; australopiths

1. INTRODUCTION folivorous hominid diet to include roots, bulbs and

Diet is a fundamental feature of a species’ biology,
strongly influencing basic body size and morphology,
life-history strategies for survival of the young in par-
ticular, social organization and the manner of its
adaptations to its environment. Consequently, the
nature of ancestral diets remains one of the most
active topics of research in human evolution. Many
years after Dart first puzzled over how the newly dis-
covered ‘man-like apes’ (in reference to the Taung
child and its kind) had survived in Taung’s xeric,
open, Kalahari environment, so alien to all the other
forest-loving great apes (Dart 1925, 1926), we are
still actively debating these issues today (e.g. White
et al. 2009a). Dart could not have comprehended, at
that time, the full scale of environmental shifts that
occurred in Africa in the past several millions years, or
indeed the depth of time encompassed. But he made
some surprisingly prescient suggestions, including the
likely expansion of the conventional frugivorous and
* Author for correspondence (j.a.lee-thorp@bradford.ac.uk).
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
animal foods such as insects, scorpions, lizards, bird’s
eggs and the young of small antelope (Dart 1926).
Effectively, it was a pre-statement of the ‘Dietary
Breadth’ hypothesis. These debates have continued
apace, but although our understanding of the nature
of environments and preferred habitats has advanced
substantially, the fossil record has grown and more
sophisticated methods have been applied to study mor-
phology and the biomechanics of food processing, our
comprehension of the important dietary shifts that
must have occurred during the early emergence of
hominins in the Pliocene is still uncertain. Such chal-
lenges have encouraged the development of new
methods for examining dietary ecology.
In an earlier Royal Society meeting on human evol-
ution almost 30 years ago, Alan Walker set out a series
of what he considered to be the more promising emer-
ging avenues in early hominin dietary research (Walker
1981). Among other candidates, Walker suggested the
inspection of tooth microwear, and carbon isotope and
trace element analysis of fossil bones (Walker 1981,
p. 58). It was evident at the 2009 meeting that the
first two methods have undergone considerable devel-
opment and progress since that time, in opening new

3389 This journal is q 2010 The Royal Society

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3390 J. A. Lee-Thorp et al. Isotopes and hominin diets
windows on hominin dietary ecology. Walker’s
predictions followed closely on a flurry of pioneering
studies in the late 1970s that began to explore the sys-
tematics of these three approaches. In the case of
stable isotopes, studies demonstrated the direct
relationship between carbon isotopes in the diet
and in animal tissues (DeNiro & Epstein 1978a),
others that these distinctions held for wild grazers
and browsers (DeNiro & Epstein 1978b; Vogel 1978)
and finally that it provided a new approach for
addressing an archaeological question about the
introduction of maize agriculture (van der Merwe &
Vogel 1978). Other studies hinted that these methods
might be extended to fossils at greater time depth
if based on the mineral rather than the organic
phase of bone (e.g. Ericson et al. 1981; Sullivan &
Krueger 1981).
At that stage, almost all chemical studies were based
on bone collagen or bone mineral (a biological apa-
tite), but the latter is an extremely unstable
structure, which is vulnerable to diagenesis. It was
not until the potential of the more crystalline, stable
enamel phase was explored and demonstrated
(Lee-Thorp & van der Merwe 1987) that the full
potential of the method to older fossils could be
realized. Following earlier work (Parker & Toots
1980; Elias et al. 1982), the potential of trace
elements, especially strontium to calcium ratios (Sr/
Ca), as trophic indicators in fossil foodwebs was
explored extensively (Sillen 1988, 1992), but these
efforts have largely stalled. This may be a reflection
of the former strong focus on fossil bone, with its
attendant problems of diagenesis. A single, broader
enamel-based study in the South African hominin
sites was unable to replicate the trophic patterns
seen earlier for Paranthropus robustus (Sponheimer &
Lee-Thorp 2006); instead, it was suggested that
Sr/Ca and Ba/Ca, in combination, may be more
informative about plant resources. That suggestion
awaits further exploration, and trace elemental analysis
will not be discussed further here.
Our main purposes in this paper are to review the
evidence for the shift to incorporate C4 resources in
early hominin diets, to present new data for temporal
variability in C4 consumption in the earlier South
African australopith, Australopithecus africanus, which
is comparable to that of P. robustus (Sponheimer et al.
2006b), and to make some predictions about the
origins and inferences of such an adaptation.
2. ISOTOPIC EVIDENCE FOR C4 IN HOMININ
DIETS
The primary distinction in application of stable carbon
isotopes to hominin diets is the difference in 13C/12C
(expressed as d13C)1 between C3 and C4 plants. In
the African environments they typically occupied,
where the growing (wet) season is warm, all carbon
dietary sources from trees, bushes, shrubs and forbs
are distinctly lower in d13C compared with those
from tropical grasses and some sedges. The primary
exception is in tropical forest ecosystems where C3
subcanopy (shaded) plants are even more depleted in
13
C (i.e. lower d13C), while vegetation in clearings
Phil. Trans. R. Soc. B (2010)
and in the canopy (including fruits) is slightly less
depleted (van der Merwe & Medina 1989; Cerling
et al. 2004). Dietary d13C values are reflected in all tis-
sues, including enamel, so that fossil enamel d13C
values provide opportunities to test hypotheses about
the dietary habits of extinct animals (e.g. Lee-Thorp
et al. 1989; Cerling et al. 1997).
Most published isotope hominin dietary research
has so far focused on the South African hominins
(Lee-Thorp et al. 1994; Sponheimer & Lee-Thorp
1999; Sponheimer et al. 2005, 2006b; Lee-Thorp &
Sponheimer 2006), although this situation is begin-
ning to change. Comparisons between the two South
African australopiths were also a starting point for
the development of occlusal enamel microwear com-
parisons (Grine 1981, 1986). This and subsequent
studies using less subjective, more quantifiable
methods (Scott et al. 2005) suggested that, in spite
of significant overlap, P. robustus microwear showed
subtly more complexity or pitting in occlusal enamel
wear compared with Australopithecus africanus. There-
fore, the inference is that the former included a
higher proportion of harder food items that required
more processing and caused more pitting and fewer
directional scratches (Grine 1986). These results
were thought to be consistent with the widely held
view that Paranthropus was a specialist vegetarian
(Grine 1986). The microwear distinctions are quite
subtle and may also be influenced by differences in
enamel prism orientation between the two taxa
(Macho & Shimizu 2009).
Nevertheless, the microwear findings provide a
useful framework for hypothesis-testing using stable
isotopes since the data essentially suggest diets that
would be classed as C3 (i.e. hard fruits and nuts).
The prediction would be that A. africanus and
P. robustus should be indistinguishable in their d13C
values from C3 feeders, such as browsers and frugi-
vores. The results, however, flatly contradict this
prediction. Analysis of more than 40 hominin speci-
mens from the sites Makapansgat, Sterkfontein,
Kromdraai and Swartkrans, spanning a period of
about 3 – 1.5 Ma, demonstrate that d13C values of
both australopiths are indistinguishable from each
other, but distinct from that of coexisting C3 consu-
mers (figure 1). Surprisingly, the proportions of C4
in enamel, on average, remain relatively constant in
spite of the passage of time and marked shifts in
environments, from relatively closed to far more
open landscapes, by about 1.8 Ma (Vrba 1985; Reed
1997; Lee-Thorp et al. 2007).
On average, both taxa obtained 25 – 35% of their
carbon from C4 sources. These resources must have
been obtained either directly from grasses or sedges,
or indirectly from animals that ate these plants.
Since few of the fine scratches characterizing
consumption of grass are present in their microwear
(Grine 1986; Scott et al. 2005), it was deduced
that direct consumption of grass blades was less
plausible (although not ruled out) (Lee-Thorp &
Sponheimer 2006). C4 sedges, grass rhizomes and
the proposed consumption of grass-eating termites
(and other small animal foods) may be implicated
(Sponheimer et al. 2005; Yeakel et al. 2007), but
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Makapansgat M3
Sterkfontein M4
Swartkrans M1
–14 –12 –10 –8 –6 –4 –2 0 2
δ13C‰
Figure 1. Data for all the South African hominins are sum-
marized as means d13C (black boxes) and standard
deviations compared with means and standard deviations
for the browsing and grazing fauna. The sites are given in
sequence from oldest (top) to youngest (bottom). Maka-
pansgat Member 3 is about 2.7–3 Ma, Sterkfontein
Member 4 is usually considered to be about 2.2 –2.5 Ma
and Swartkrans Member 1 is younger than 2 Ma. These
ages based on biostratigraphy are imprecise, but sufficient
for our purposes. More precise chronometric studies based
on Pb/U isotopes have recently been completed (R. Pickering
2009, personal communication), but do not change the over-
all sequence. All the hominin data show significant C4
contributions compared with C3 feeders, in spite of large
shifts, from closed to open, in the environments (Reed
1997). Adapted from Lee-Thorp & Sponheimer (2006).
when examined individually, none of these resources
offers a completely satisfactory solution. For instance,
it has been shown that in this part of southern Africa
the proportion of sedges following the C4 pathway
is modest (Stock et al. 2004), and likewise few
termite species seem to be C4 specialists (Sponheimer
et al. 2005). The most plausible explanation is that
they utilized C4 resources quite broadly, including
both C4 plant and animal resources. Although the
results say little about the rest of the diet (i.e.
the major C3 portion), they hint that neither of
these australopiths were plant specialists.
These results were also unexpected because extant
great apes consume minimal or no C4 resources even
when they live in relatively open habitats. Several
studies have shown that even ‘savannah’ chimpanzees,
who live in the more open parts of the Pan range, con-
sume few, if any, C4 resources (Schoeninger et al.
1999; Sponheimer et al. 2006a). Most forest-dwelling
chimpanzees and gorillas reveal distinct low d13C
values, indicative of the use of resources located in
shaded understorey vegetation (Carter 2001; Cerling
et al. 2004; Sponheimer et al. 2009; J. A. Lee-Thorp,
Y. Warren & G. A. Macho 2009, unpublished
data). It is this engagement with C4 resources,
which were becoming increasingly available in the
Plio-Pleistocene, that indicates a fundamental niche
difference between the australopiths and extant apes.
Phil. Trans. R. Soc. B (2010)
Isotopes and hominin diets J. A. Lee-Thorp et al. 3391
3. VARIABILITY BETWEEN AND WITHIN
INDIVIDUALS
The foregoing discussion relies on broad averages,
and we now turn to examine patterns in individuals.
Where sufficient australopith d13C values exist
within any one site, or members within that site,
the data are quite variable, which suggests a degree
of dietary opportunism and flexibility. This obser-
vation leads to the question of whether hominins
shifted their diets on annual or even seasonal time
scales, and whether the C4 contributions observed
in bulk tooth enamel measurements mask short-term
dietary variability.
Tooth enamel is an incremental tissue that can be
sampled to investigate temporal changes in both
climate and diet using stable isotope analysis.
4 Developments in laser ablation techniques now
permit high-resolution sequential sampling of enamel
crowns, with minimal visible damage (Passey &
Cerling 2006). However, the sequential chronological
resolution that can be attained, no matter how small
the sample spot, is severely constrained by overprinting
during maturation of the enamel. Enamel maturation
occurs for many months, even years, after primary
mineralization during prism formation (Suga 1982;
Balasse 2002). Recovery of primary dietary signals
has been successfully accomplished using a forward
and inverse model only in continuously growing
teeth and where the growth and enamel maturation
parameters are well characterized (Passey et al.
2005). The patterns of enamel maturation in modern
human tooth crowns are poorly understood, and
those of early hominins even less so. However, it is evi-
dent that the nature of crown formation and enamel
maturation inevitably produces a mixture of isotope
signals, from both the initial primary mineralization
and the maturation periods, so that there will be
dampening or overprinting of the original signals.
Nevertheless, three statements can be made with
certainty: (i) the isotope profile from crown to root
preserves an ordered time series extending from earlier
(crown) to later (root) in time, (ii) the mimimum time
duration of any single spot-sample within a tooth is
equivalent to the ‘maturation time’, or time required
for enamel to cure into its fully mineralized form
(probably months in primates), and (iii) the total time
duration of an isotopic profile across a tooth is the
sum of the crown enamel deposition time (for example,
as recorded by perikymata) and the maturation time of
the last enamel increment deposited.
Notwithstanding the constraints imposed by matu-
ration patterns and by lower analytical precision,
laser ablation has been applied to sample the external
surface along the growth trajectory of four P. robustus
tooth crowns (Sponheimer et al. 2006b) (figure 2b).
The results showed that d13C values, and the pattern
or temporal change, differed between individuals
and, most startling, showed differences of up to 5‰
within a given P. robustus tooth. Given that the signal
is attenuated or even scrambled as described above,
these data still suggest a very large shift from a diet
dominated by C3 to a diet dominated by C4 resources
in certain individuals. Variability is observed at several
time scales—intra- and inter-annual.
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3392 J. A. Lee-Thorp et al. Isotopes and hominin diets

(a) 0 (b)

–2

–4
δ13C

–6

–8

–10

–12
0 2 4 6 8 10 12 14 0 2 4 6 8 10 12 14 16 18
scan number scan number

Figure 2. High-resolution laser ablation d13C sequences for (a) A. africanus and (b) P. robustus plotted against sample (scan)
number. Sample increments were approximately 0.3 mm. The Paranthropus data are from Sponheimer et al. (2006b), where the
data were plotted according to a time-sequence model based on perikymata counts. In this case, we avoided the application of a
time sequence based on perikymata because the lengthy maturation time introduces not only a longer time period but also
more uncertainty. (a) Open diamonds, STS 2518 max RM3; filled circles, STS 31 max RM3; filled triangles, STS 2253
mand RM1. (b) Open diamonds, SKW 6427 M; filled circles, SKW 5939 M; filled triangles, SK 24606 RM2 or 3; squares
with crosses, SK 24606 RM3.

Four A. africanus molar crowns from Sterkfontein
Member 4 were analysed using the same methods.
The results for one tooth were omitted because of con-
cerns about the interference of glue on the surface,
observed as puffs of gas during ablation. Although
the age of Member 4 is uncertain, biostratigraphic
evidence indicates that it is considerably older
than Swartkrans, and with several taxa—including
A. africanus—in common with the older site of
Makapansgat (Vrba 1985). As was the case for the
P. robustus crowns, all teeth are lightly to moderately
worn molars. The tooth assignments are shown in
figure 2, although some in figure 2b were too fragmen-
tary to allow determination other than that they are
molars.
The analytical methods for the A. africanus molars
followed exactly those reported in Sponheimer et al.
(2006b). Each tooth was cleaned mechanically and
chemically (with acetone), and then thoroughly dried
in a low-temperature oven. Samples were purged
with helium inside the laser chamber for several min-
utes or hours as required for the rate of CO2
outgassing to fall below appropriate levels. Small
amounts (10– 30 nmol) of CO2 were generated using
a CO2 laser (10.6 mm) operating at 5 – 15 W and
8.5 ms pulse duration in a He atmosphere. The CO2
was cryogenically purified and ‘focused’ prior to intro-
duction to a continuous-flow GC-IRMS (MAT 252).
Systematic isotope fractionation and fractionation
associated with laser ablation production of CO2
were monitored by analyses of injected aliquots of
CO2 and by analysis of a suite of internal tooth
enamel standards, both calibrated against NBS-19
gas (d13C ¼ 1.95‰). The laser-carbonate isotope frac-
tionation (1*LASER-carb) for fossil herbivore samples
from several South African hominin sites was – 1.3 +
1.5‰ (1s).
Enamel was sampled at ca 0.3 mm intervals,
encompassing about four perikymata for each laser
ablation track (or scan) and the space between
tracks. The length of each sampling trajectory varied
Phil. Trans. R. Soc. B (2010)
depending on the available tooth surface, with between
nine and 12 scans for the three reported molars. Based
on a periodicity of 7 days per striae of Retzius
(observed externally as perikymata) as calculated in
Lacruz et al. (2006), the period of primary mineraliz-
ation in the sampled area is over a year for two
specimens (STS 2253 and STS 31) and just under a
year for the third (STS 2518). However, as discussed
above, the time represented in the isotope profile is
much longer when enamel maturation is taken into
account, and additionally the measured values
represent an attenuated signal of higher amplitude.
Variability in the proportions of C3 and C4
resources between and within individuals is on a simi-
lar scale for A. africanus compared with P. robustus
(figure 2). At least one individual, STS 2518, indicates
a more or less uniform C3 resource base, while
another, STS 31, shows values varying by over 6‰
from a C3 to a predominantly C4 resource base. As
emphasized above, it is difficult to ascertain the precise
time scales over which this variation occurred. How-
ever, given that the enamel underlying the sampling
arrays mineralized and matured over a period of over
a year in each case, the differences between individuals
cannot be ascribed to sampling of a single season in
one case and multiple seasons in another.
The results suggest that C4 resources formed an
important but highly variable component of hominin
diets, extending at least as far back as A. africanus at
Sterkfontein. There is no reason to believe that the
dietary ecology of A. africanus at the earlier site of
Makapansgat Member 3 would be significantly
different.
4. ORIGINS AND TIME DEPTH OF THE C4
PATTERN IN HOMININ DIETS
Few analyses have been performed on eastern African
material to allow us to definitively address the question
of the origins of engagement with C4 resources. Clues
from several sources may hint at an origin associated
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Isotopes and hominin diets
with the emergence of the genus Australopithecus, but
at present there are no data to address the period
prior to emergence of A. africanus.
Recently published d13C data for two Paranthropus
boisei individuals from Olduvai revealed a strong
dependence on C4 resources (van der Merwe et al.
2008). This was unexpected since the similarity of
the ‘nutcracker’ dental and masticatory complex to
that of South African P. robustus led to the expectation
of a broadly similar dietary adaptation. Such high d13C
values cannot be explained by consumption of C4
animal foods alone since they would require a highly
unlikely dietary scenario that included almost exclu-
sive consumption of the flesh of grazing (C4)
animals. The results demand an alternative expla-
nation. The authors suggested that P. boisei, or at
least these two individuals, probably specialized in
exploitation of C4 sedges, which are far more abun-
dant in East African wetlands than they are in South
Africa (van der Merwe et al. 2008). Additionally, a
recent microwear study of P. boisei occlusal enamel
showed little evidence for the pitting associated with
hard object feeding (Ungar et al. 2008). These data
seem inconsistent with their strongly developed masti-
catory complex, widely considered to be an adaptation
for the consumption of hard foods. However, their
diets were clearly abrasive when the degree of wear is
considered (Tobias 1967). In combination, the high
C4 resource consumption and the lack of a hard-
object microwear pattern may require that we rethink
the functional significance of the australopith
masticatory package.
Interestingly, microwear patterns for Australopithe-
cus afarensis and Australopithecus anamensis also lack
evidence for hard-object feeding (Ungar 2004; Grine
et al. 2006), but rather resemble patterns seen in
apes, especially gorillas. These results could also be
considered as inconsistent with an evolutionary trajec-
tory for larger molars and thicker enamel, which seem
to suggest adaptation to increasingly more xeric habi-
tats (Grine et al. 2006). However, other evidence
points in a similar direction. It has been argued that
the biomechanical masticatory complex of both
A. anamensis (Macho et al. 2005) and A. afarensis
(Rak et al. 2007) is more gorilla-like. Furthermore,
modern humans and gorillas share life-history charac-
teristics including non-seasonal breeding (Knott
2005), which in turn carries implications for a pattern
of seasonal resource exploitation that ensures maxi-
mum infant survival. No isotope data exist for these
older australopiths that would allow us to test whether
C4 exploitation formed part of an increasingly seasonal
foraging round as suggested by Macho et al. (2003).
If they did engage with such resources, it will be
important to understand the seasonal variation.
While no isotopic data yet exist for A. anamensis and
A. afarensis, recently published data for Aramis suggest
that Ardipithecus ramidus, at 4.4 Ma, included few,
if any, C4 resources in the diet (White et al.
2009b). Rather their isotopic composition most closely
resembles that of savannah chimpanzees which avoid
C4 resources, and contrasts with that observed in
A. africanus at Makapansgat (figure 3). Although the
authors lay stress on the woody nature of the Aramis
Phil. Trans. R. Soc. B (2010)
J. A. Lee-Thorp et al. 3393
Aramis 4.4 Ma
hyaenids
Makapansgat ca 2.8–3 Ma
hyaenids
–14 –12 –10 –8 –6 –4 –2 0 2 4
δ13C‰
Figure 3. A summary comparison of the hominin data for
Aramis (above), and Makapansgat (below), plotted as
means (black boxes) and standard deviations with mean
values for C3 and C4 feeders shown for comparison. Data
for carnivores (hyaenids) are also shown (white boxes; n ¼
2 for Makapansgat), because they are effectively integrators
for the values of all the fauna they consume. These data
are shifted towards values more enriched in 13C in Aramis,
suggesting more open, C4 elements in the environment com-
pared with Makapansgat, where the faunal assemblage
consists largely of C3 feeders. In spite of this difference, Ar.
ramidus remains relatively depleted in 13C, quite unlike the
patterns for A. africanus seen at Makapansgat. Data for
Aramis are from White et al. (2009b), and for Makapansgat
are from Sponheimer (1999).
environment, the d13C values for the fauna, taken
together, show that a good deal of C4 grassy vegetation
was present in the environs. Therefore, the important
point is not that ‘Ar. ramidus was a denizen of wood-
land’ (White et al. 2009a), but that Ar. ramidus
focused almost exclusively on C3 resources while
avoiding nearby C4 resources, which were present. In
contrast, the Makapansgat hominins clearly had
moved to exploit C4 resources (figure 3), in spite of
the relatively closed nature of that environment
(Reed 1997). The Aramis data would certainly suggest
that, if an engagement with C4 foods marked a funda-
mental shift in hominin evolution as we have argued,
then such a shift occurred post Ar. ramidus, or
elsewhere.
Further evidence for a possible ecological shift
between Aramis and Makapansgat may reside in a
comparison of the combined d13C and d18O data
(figure 4). The d18O composition of enamel provides
a potential source of information about dietary ecology
because, in addition to the influences of hydrology and
isotopic composition of precipitation, an animal’s d18O
value is affected by dietary ecology, drinking behaviour
and thermophysiology (Bocherens et al. 1996; Kohn
1996; Kohn et al. 1996; Sponheimer & Lee-Thorp
2001). It has been shown that suids, some primates
and in particular all faunivores have relatively low
d18O compared with herbivores (Lee-Thorp &
Sponheimer 2005). The reasons are not yet clear and
almost certainly differ for these groups. In the case
of suids, it may reflect reliance on underground storage
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3394 J. A. Lee-Thorp et al. Isotopes and hominin diets

(a) 8
Kuseracolobus
6
Pliopapio
Deinotherium
4 Giraffidae
Tragelaphini
2 Neotragini
δ18OVPDB

Simatherium
0 Eurygnathohippus
Aepyceros
–2 Nyanzachoerus
Kolpochoerus
–4 Hyaenidae
Ardipithecus
–6

–8

(b) 8

6
Cercopithecoides
4 Parapapio
Diceros
2 Giraffids
δ18OVPDB

Tragelaphini
0 Neotragini
Simatherium
–2 Hipparion
Aepyceros
–4 Suidae
Hyaenidae
–6 Australopithecus

–8
–16 –14 –12 –10 –8 –6 –4 –2 0 2 4
δ13C‰

Figure 4. Bivariate d13C and d18O comparisons of similar taxa in (a) Aramis and (b) Makapansgat shown as means and
standard deviations. Several significant differences are observed. On average, d18O values for Makapansgat fauna are about
2‰ lower than at Aramis, which is consistent with their relative geographical positions and associated values for hydrology.
However, the Aramis data are more variable, with some exceptional and unusually low values for Deinotherium in particular.
Australopithecus africanus data are relatively enriched in 13C and depleted in 18O, and occupy the same isotopic ‘space’ as the
hyaenids, quite unlike Ar. ramidus. The other primate species are also more enriched in 13C, unlike Aramis, but the impala
(Aepyceros) has higher d13C values at Aramis. Although impalas are generally considered to be mixed feeders, a recent
study showed high d13C and almost exclusive grazing habits for Aepyceros in the nutritious grasslands of Rwanda (Copeland
et al. 2009). The data for Nyanzochoerus at Aramis are remarkably similar to those for the Suidae at Makapansgat, suggesting
a similar ecological niche. Data for Aramis are from White et al. (2009b) and for Makapansgat from Sponheimer (1999).

organs, and for faunivores, a high proportion of dietary
lipids and proteins, or a very heavy reliance on drink-
ing water. Australopith d18O data from Makapansgat
overlap with those of carnivores in the same strata
(figure 4). Similarly low d18O values—compared with
other taxa in the Aramis faunal assemblage—are not
observed for Ar. ramidus. Whatever the underlying
contributors to the lower d18O values for hominins at
Makapansgat (and we do not imply that they are
necessarily the same), these observations call for
further study and explanation.
5. CONCLUSIONS
Carbon isotope data have demonstrated that australo-
piths in South Africa increased their dietary breadth by
Phil. Trans. R. Soc. B (2010)
consuming C4 resources, while in East African P. boisei,
this involvement might rather be regarded as a special-
ization. The exact nature of these C4 resources
remains unclear, and cannot be deduced from the
d13C values alone, but they most plausibly included
various C4 resources, in varying proportions. Among
the South African australopiths at least, consumption
of C4 resources varied strongly between individuals
and within individuals, in both A. africanus and
P. robustus. The australopith pattern is quite unlike
that seen in modern chimpanzees, and indeed in
early Pliocene Ar. ramidus, and we argue that it rep-
resented a fundamental shift in dietary ecology that
increased dietary breadth. Additionally, the exact
foods that contributed to the observed C4 signals in
australopith enamel are not clear. We cannot yet
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Isotopes and hominin diets
pinpoint when the shift occurred because no published
data yet exist for A. anamensis and A. afarensis, but cer-
tainly further research should target the period
between 4 and 3 Ma.
We thank Alan Walker and Chris Stringer for organizing the
Royal Society Symposium on the ‘First four million years of
human evolution’, the Royal Society for sponsoring the
meeting, Debbie Guatelli-Steinberg for her work on the
perikymata and many colleagues for their assistance and
helpful discussions over the course of many years spent
exploring the fascinating discipline of isotope ecology.
ENDNOTE
1 van Schaik), pp. 351 –378. Cambridge, UK: Cambridge
By convention, 13C/12C ratios are expressed in the delta (d)
notation relative to the PDB standard, as follows: d13C (‰) ¼
(Rsample/Rstandard 2 1)1000, where R ¼ 13C/12C, and similarly,
18
O/16O ratios are expressed as d18O relative to PDB or SMOW
(we use PDB in this paper).
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Phil. Trans. R. Soc. B (2010) 365, 3397–3410

doi:10.1098/rstb.2010.0052

Review

Retrieving chronological age from dental

remains of early fossil hominins to
reconstruct human growth in the past
M. Christopher Dean*
Department of Cell and Developmental Biology, University College London, Gower Street,
London WC1E 6BT, UK
A chronology of dental development in Pan troglodytes is arguably the best available model with
which to compare and contrast reconstructed dental chronologies of the earliest fossil hominins.
Establishing a time scale for growth is a requirement for being able to make further comparative
observations about timing and rate during both dento-skeletal growth and brain growth. The absol-
ute timing of anterior tooth crown and root formation appears not to reflect the period of somatic
growth. In contrast, the molar dentition best reflects changes to the total growth period. Earlier
initiation of molar mineralization, shorter crown formation times, less root length formed at gingival
emergence into functional occlusion are cumulatively expressed as earlier ages at molar eruption.
Things that are similar in modern humans and Pan, such as the total length of time taken
to form individual teeth, raise expectations that these would also have been the same in fossil
hominins. The best evidence there is from the youngest fossil hominin specimens suggests a close
resemblance to the model for Pan but also hints that Gorilla may be a better developmental
model for some. A mosaic of great ape-like features currently best describes the timing of early
hominin dental development.
Keywords: hominin evolution; dental development; incremental markings; tooth root growth;
enamel; dentine

1. BACKGROUND Smith (1989) has shown that certain key marker

The lives of all living organisms can be divided into
stages. This allows comparisons to be made between
them. There are many reasons for studying the stage
or period of growth in primates in a comparative con-
text, which include identifying those ontogenetic
changes shared by all primates and those that are
unique to modern humans (Schultz 1937). Relative
comparisons of the stages of skeletal or dental
growth have proved to be a useful way of defining simi-
larities and differences between both living and fossil
primates. When chronological age is known, then the
length of the phases of growth as well as the rates of
growth of individuals can be compared. Dental devel-
opment is just one measure of biological maturity, but
is arguably the most stable, and it occurs over an unu-
sually long period of time from before birth to
maturity. Besides enabling us to discover things
about the evolutionary history of our own growth
period, studies of comparative dental development
provide us with an opportunity for investigating the
biological processes that govern tooth formation from
the initial mineralization of teeth to the completion
of their roots (Swindler 1985).
*ucgacrd@ucl.ac.uk
One contribution of 14 to a Discussion Meeting Issue ‘The first four
million years of human evolution’.
3397
events during dental development actually correlate
better with important variables that describe life-
history variation than any of these life-history variables
do with each other. Because of this, some tentative
inferences can be made about the way fossil primates
lived their lives compared with living primates that
go beyond simple relative dento-skeletal comparisons.
A powerful aspect of dental biology is that tooth tissues
preserve an incremental record of their growth, which
remains literally embodied within the microstructure
of enamel and dentine. This offers an opportunity to
reconstruct the period of maturation in fossil primates
and compare them in real time with living primates.
Even if it may never be possible to retrieve information
about many life-history variables from the fossil
record, it should be possible to reconstruct a time
scale for growth in the past.
2. INCREMENTAL GROWTH OF ENAMEL
AND DENTINE
The cells that form enamel and dentine (ameloblasts
and odontoblasts) secrete their matrix in a rhythmic
manner (Bromage 1991; Smith 2006; Bromage et al.
2009). A circadian rhythm in cell function is expressed
as a daily slowing of secretion during enamel and den-
tine formation and is still manifest in the enamel and
dentine microstructure of fully formed teeth as a
This journal is # 2010 The Royal Society
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3398 M. C. Dean Review. Dental development in early hominins
(a) (b)
Figure 1. Scanning electron micrograph showing perikymata
on the upper lateral incisor of MLD 11 (Au. africanus) from
Makapansgat, South Africa (a). Their spacing becomes
closer towards the cervix. Two or three regions of enamel
hypoplasia are evident indicating periods of slowed enamel
growth during tooth formation. (b) Transmitted polarized
light micrograph of enamel incremental markings seen in a
longitudinal ground section of a probable second molar frag-
ment (Ward et al. 2001) attributed to Au. anamensis (KNM-
ER 30748) from Allia Bay, Kenya. Coarse oblique long
period incremental markings (approx. 35 mm apart) run
from bottom left to top right and emerge at the surface
within perikymata troughs. Along prisms, that run left to
right in this image, are short period daily increments
marked by fine cross striations approximately 5 mm apart.
In this specimen, there are seven daily increments between
adjacent long period striae.
daily incremental marking (Boyde 1976, 1979, 1989,
1990a; Shinoda 1984). Thin sections of teeth pre-
pared for histological analysis, or even polished or
naturally fractured surfaces of fossil teeth that are suit-
able for examination with various kinds of microscopy
(figure 1) can be used to reveal these markings in
enamel and dentine (Boyde 1989, 1990b; Dean
2000, 2006; Lacruz et al. 2006, 2008). Counts of
daily incremental markings in the teeth of individuals
with known dates of birth and death match very closely
with the number of days of life (Antoine et al. 2009).
The daily increments of enamel secretion in great
ape and fossil hominin teeth cumulate at a faster rate
than they do in modern human tooth enamel (Dean
et al. 2001). Enamel measuring 200 mm thick over
the cusp of a great ape tooth, takes on average between
55 and 65 days to form, whereas in modern humans
this takes 70 – 80 days (Dean et al. 2001; Dean 2009;
Smith et al. 2006). Daily rates of dentine formation,
however, are more similar in great apes and humans
and take between 80 and 100 days to form 200 mm
close to the root surface (Dean 2009, in press).
Another, but longer period rhythm, that also slows
dental hard tissue formation in a regular way is super-
imposed upon this daily rhythm (figure 1). In modern
humans this coarser more prominent marking usually
occurs every 7, 8, 9 or 10 days with a modal value of
8 days (Smith et al. 2006). Long-period incremental
markings are aligned along the original mineralizing
tissue front in both enamel and dentine. The slope
of these incremental markings, with respect to the
Phil. Trans. R. Soc. B (2010)
junction between enamel and dentine, provides a way
of estimating past rates of differentiation of new
secretory cells during tooth formation (Boyde 1963,
1964, 1990b; Shellis 1984; Dean 1985; Risnes 1986).
The rate of increase in both tooth crown height and
root height can be reconstructed by dividing incre-
ments of tooth crown length along the enamel
dentine junction (EDJ), or cement dentine junction
(CDJ) by the time intervals taken to form them
(Boyde 1963; Risnes 1986; Dean 2006, 2009). In
figure 2, consecutive 200 mm-thick increments of
enamel and dentine have been used to plot increasing
tooth height against time from the dentine horn to a
point as close to completion of the root as possible
(Dean 2009).
The number of daily increments between long-
period markings appears always to be the same in
each of the teeth of an individual but it varies between
individuals. In large samples of individuals there are
also outliers with a long-period rhythm of 6 or 11 or
even perhaps 12 days. We now know that these long-
period markings (first described by Anders Retzius
(1837) and, therefore, also referred to as Retzius
lines) occur in the enamel of other primates including
early fossil hominins (figure 1). Of 29 australopiths
examined so far, 17 (59%) showed a mean periodicity
of 7 days and of seven early Homo specimens examined
so far, two had long-period lines 7 days apart, four
were 8 days apart and one was 9 days apart (Lacruz
et al. 2008). Fossil teeth, however, are precious and
it is only rarely possible to employ partially destructive
techniques to retrieve data about their growth. Never-
theless, long-period markings also create a furrow or
trough on the external surface of permanent tooth
enamel. These so-called perikymata (waves around
the tooth) first defined by Preiswerk (1895) in ungu-
late enamel are well preserved on many early
hominin teeth and they can be counted with scanning
electron microscopy (figure 1) or even in oblique-
reflected light. They can be used to estimate enamel
formation times in fossil teeth since counts of periky-
mata are equivalent to counts of long-period striae
within the tooth but their periodicity may not be
known unless the internal structure of the enamel
can be visualized.
3. CONSTRUCTING A COMPARATIVE MODEL
FOR EARLY HOMININ MATURATION
Recent evidence about DNA sequence analysis and
from molecular biology suggests that modern
humans and chimpanzees are more closely related to
each other than to any other living ape (Goodman
et al. 1994; Ruvolo 1994; Bradley 2008). It is, there-
fore, not an unreasonable assumption that the last
common ancestor of the Pan – Homo clade had a life
history more like that of modern chimpanzees than
modern humans (Robson & Wood 2008). It is none-
theless equally likely that among the species of early
hominins there were many different life-history strat-
egies that spanned what we know today about life
history in modern orangutans, chimpanzees, bonobos
and gorillas. One key question that we can then ask
is whether there is any evidence among early hominins
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Review. Dental development in early hominins M. C. Dean 3399

(a) 25 000 (b)

tooth height along EDJ (mm)

20 000

15 000

10 000

5000

0 2 4 6 8 10 12 14 16 18 0 2 4 6 8 10 12 14 16 18
tooth formation time (years) tooth formation time (years)
Figure 2. Plots of M1, M2 and M3 formation time (years) against increasing tooth height (mm) along the mesiobuccal (pro-
toconid) EDJ (red open circles), continued along the CDJ (open blue circles) for (a) Pan troglodytes and (b) modern human
molars. The mean length (+1 s.d.) of mesiobuccal root formed at gingival emergence in free-living Pan specimens given in
Kelley et al. (2009), M1, 4.2 mm; M2, 5.2 mm; M3, 6.8 mm has been used to generate a likely range of root lengths (and
thereby corresponding ages) where molars in Pan might have emerged into the mouth (yellow filled circles). Arrows denote
the median ages of gingival emergence. The rates of crown and root growth, as well as the total tooth formation times in
modern humans and Pan, are similar but earlier initiation times compress Pan molar development into approximately 12
years rather than approximately 18 years. Distance curves for a single Gorilla M1, a short M1 fragment of KNM-ER
30749 and a longer M2 fragment of KNM-ER 30748 (both attributed to Au. anamensis, Ward et al. 2001) are superimposed
over the Pan M1 and M2 molars (filled black circles, crown; filled blue circles, root). Rates of root extension in Gorilla and
Au. anamensis are faster than in Pan.

for a period of maturation that differs from that known
today for modern chimpanzees. Another feasible ques-
tion is whether there is evidence among the various
species of early hominins for any differences between
them in the timing of dental development that might
point to the presence of different life-history strategies
existing together during the first four million years of
human evolution. If this were so it might point to inter-
esting links with climate change or diet. To answer
these questions requires a detailed knowledge of the
chronology of dental development in modern great
apes and an assessment of how early fossil hominins
do or do not compare with this. Since this is realisti-
cally only presently possible for Pan troglodytes, it
makes sense to try and construct a model that brings
together everything that is known about the timing of
dental development in P. troglodytes and use this to
examine the timing of dental development in early
hominins.
4. THE CHRONOLOGY OF DENTAL
DEVELOPMENT IN PAN TROGLODYTES
Early studies of dental development in great apes were
made on single individuals or on samples of animals
brought to zoos or acquired for comparative skeletal
collections (Keith 1899; Schultz 1924, 1935, 1940;
Zuckerman 1928; Krogman 1930; Bennejeant 1940;
Clements & Zuckerman 1953). Few of the living ani-
mals studied were actually born in captivity and so
their chronological age was rarely known. While
some early studies identified differences in the
sequence of dental eruption between great apes and
humans and also noted earlier ages for the eruption
of certain teeth, others found no differences in the
timing of dental development between great apes and
Phil. Trans. R. Soc. B (2010)
modern humans (Zuckerman 1928). In recent years
many issues have been clarified through studies on
samples of captive animals of known chronological
age. Parallel histological studies of enamel and dentine
growth in great apes have also helped to build a better
picture of the chronology of dental development in a
comparative context. What follows is a synthesis of
those studies.1
(a) Permanent tooth eruption times in Pan
In two classic longitudinal studies on chimpanzee
dental emergence, Nissen & Riesen (1945, 1964) pre-
sented the first reliable data for ages of gingival
emergence (eruption) in captive chimpanzees. They
showed that the deciduous dentition was fully emerged
into functional occlusion by approximately one year of
age (Nissen & Riesen 1945) and that for eight males
and seven females combined (Nissen & Riesen
1964), the mean ages of emergence for M1 were 3.3
years (range, 2.6 – 3.8); M2, 6.7 years (range, 5.6 –
7.8); and M3, 10.8 years (range, 9.0 – 13.6). All of
these molar eruption ages are much earlier than
those known for modern humans. Interestingly, how-
ever, the equivalent data for incisors and canines are
indistinguishable from those known for modern
humans. Mean gingival emergence ages for those
teeth are, respectively, I1: 5.7 years (range, 4.5 – 7.0);
I2: 6.4 years (range, 5.0 – 8.3); C: 9.0 years (range,
7.6 – 10.1). Kuykendall et al. (1992) in a study of 22
male and 36 female laboratory born and raised chim-
panzees aged between 1 and 10 years observed
median emergence times for permanent teeth that
were rarely more than a month or two different from
the data of Nissen & Riesen (1964). One exception
was the permanent canine that in both the mandible
and maxilla erupted a year earlier at approximately
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3400 M. C. Dean Review. Dental development in early hominins
8 years (range 6.5 – 8.7). Unfortunately, the age sample
of Kuykendall et al. (1992) did not extend to individ-
uals with emerging M3s, but the general consistency
for dental emergence ages between these samples of
laboratory-raised chimpanzees is remarkable. How-
ever, these data are not so closely reflected by those
derived from a much smaller sample of free-living
chimpanzees of known chronological age originally
described by Zihlman et al. (2004) but subsequently
revisited by Smith et al. (2009, 2010).
(b) Environmental effects on dental development
in great apes
An important issue that is still not well understood is
the effect on great ape dental development of being
born and raised in captivity and perhaps more signifi-
cantly, the effect of being nursed and raised by the
mother in captivity or being hand-nursed and bottle-
fed by humans. Zihlman et al. (2004, 2007) have pre-
sented a range of data for free-living chimpanzees that
demonstrate a slower rate of behavioural, somatic and
dental development than for captive animals. They
place M1 emergence at approximately 4 years, M2
between 6 and 8 years, canine emergence between
10 and 11 years and M3 emergence at approximately
12.5 years. Smith et al. (2006) have also illustrated a
wild-born chimpanzee aged 4.4 years (fig. 6 in Smith
et al. 2006), where M1 is still far from functional
occlusion. Phillips-Conroy & Jolly (1988) and
Kahumbu & Ely (1991) also recorded later eruption
times in free-living than in captive baboons. Even if
the degree of difference is both population- and
sample size-sensitive, some degree of difference is cer-
tainly real. Kelley et al. (2009) used the extrinsic
staining on newly emerged cusps of molar teeth to
indicate gingival emergence in wild-collected great
ape skulls. In figure 2, the mean lengths for mesiobuc-
cal roots (+1 s.d.) measured at gingival emergence in
that study are plotted individually onto each Pan molar
root (M1, n ¼ 14; M2, n ¼ 10; M3, n ¼ 8). The age
ranges generated for these root lengths have been
used to simulate a likely range and median age of
attainment for gingival emergence in the predomi-
nantly wild-collected Pan specimens represented in
figure 3. The results are a close match with those of
Zihlman et al. (2004) for M1 and to some extent for
M2 with simulated median age of attainment of M1
at approximately 4.0 years, M2 at approximately 7.0
years and M3 at approximately 10 years. Interestingly,
they also fall close to the 32.6, 59.4 and 86 per cent of
the total time to complete dental development that
Swindler (1985) calculated for modern human molar
eruption times, assuming that this total time is
approximately 12 years in P. troglodytes. However,
with the exception of M1, these simulated median
ages of attainment for molar gingival emergence still
fall within the ranges reported for captive chimpan-
zees. Kelley & Schwartz (2009) have drawn attention
to the wide range of ages likely for gingival emergence
in free-living great apes but Smith et al. (2010) have
suggested that ages for gingival emergence may be
influenced more by free-living or captive rearing than
crown or root formation are.
Phil. Trans. R. Soc. B (2010)
M1
M1
M1
M1
M1
M2
M2
M2
M2
M2
M3
M3
M3
M3
M3
100
80
percentile
60
40
20
0
2 3 4 5 6 7 8 9 10 11 12
age at tooth eruption (years)
Figure 3. Predicted median ages of attainment (50th percen-
tile) for molar gingival emergence ages in Pan (M1, 4.1
years; M2, 6.9 years; M3, 10.1 years). These are derived
from the times corresponding to root lengths formed at gin-
gival emergence shown as yellow filled circles in figure 2. The
interquartile age ranges (vertical lines) of attainment were
simulated by using 1 s.d. of root formed at gingival emer-
gence. The median values are represented by central
vertical lines. A spread of initiation times over a lower age
range, which in reality seems likely, would, reduce these
estimates slightly.
What lies behind this difference is likely to be multi-
factorial but certainly to a large extent nutritional.
Lippert (1977) showed that captive hand-reared
infant apes double their birth weight by three
months, whereas mother-nursed infants do not do so
until six months. This difference persists until at
least 21 months and probably continues as a trend
into adulthood (Nissen & Riesen 1945; Fooden &
Izor 1983). Nissen & Riesen (1945), Marzke et al.
(1996) and Winkler et al. (1991) have all noted
advanced deciduous tooth emergence ages between
mother-nursed and formula-fed infant great apes.
Marzke et al. (1996) specifically made the point that
data from mother-nursed captive animals are likely to
be more directly relevant to free-living conditions
than data for hand-reared great apes. The available
data for great ape dental development needs, there-
fore, to be considered carefully in this light if a
model for dental development in fossil hominins is to
be realistic.
(c) Tooth initiation times, sequences
and overlaps
Swindler (1985), Anemone et al. (1991), Anemone &
Watts (1992), Kuykendall (1996) and Reid et al.
(1998) have all noted that the times for initial mineral-
ization of the permanent incisors and canines in
Pan are very similar to those described for humans
(Kronfeld 1935) and that the sequence of minerali-
zation is identical. Lower permanent incisors initiate
at approximately 3 –4 m after birth and canines at
4– 5 m although both earlier and later times have
been recorded (Kronfeld 1935; Anemone et al. 1991;
Kuykendall 1996; Winkler 1996; Schwartz et al.
2006). Winkler (1995) demonstrated that direct obser-
vations of tooth germs can pick up earlier initiation
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Review. Dental development in early hominins
times than radiography as Hess et al. (1932) and
Beynon et al. (1998) also observed. Reid et al. (1998)
have nonetheless noted generally similar initiation
times in Pan from histological studies for lower I1
(range, 1.8–5.6 m), lower I2 (range, 2.3–8.5 m) lower
canines (range, 4.6–6.9 m) as well as for P3 and P4
initiation (range, 1.1–1.95 years) something also
observed by Anemone et al. (1991) and Kuykendall
(1996) to between 1.4 and 1.8 years in Pan.
Understanding the differences in dental development
that exist between great apes that take approximately
12 years to grow up and modern humans that take
approximately 18 years to grow up is fundamental to
our being able to interpret juvenile fossil hominin
material. It is molar development that reflects these
somatic growth differences most closely. While the
sequence of molar initiation is also always identical in
great apes and humans (M1, M2, M3), the timing of
molar initiation has been much debated. Molar for-
mation is drawn out in modern humans between birth
and approximately 18 years. Initiation of M1 around
birth is followed by M2 initiation at approximately 3
years and M3 initiation at approximately 8 years with
each molar then taking about 10 years to form.
Dean & Wood (1981) suggested that molar
initiation times were compressed together in great
apes (M1 close to birth, M2 at 2.5 years and M3 at
5 years) and that total molar formation times were
shorter, with M3 root formation completing between
11 and 12 years. Certainly, studies of dissected M1
germs in great apes have usually, but not always,
demonstrated three or four mineralizing cusps at
birth (Oka & Kraus 1969; Tarrant & Swindler 1972;
Moxham & Berkovitz 1974; Winkler 1996). Schwartz
et al. (2006) have described an extreme case of M1
initiation in a captive hand-raised gorilla as early as
90 days before birth. However, Anemone et al.
(1991) and Anemone (1995) in the first longitudinal
radiographic studies of dental development in captive
P. troglodytes, showed that for 16 individuals, the pro-
posal of Dean & Wood (1981) for M2 and M3
initiation in Pan was incorrect. They demonstrated
even earlier initiation times for M2 at 1.5 years and
M3 at 3.5 – 4.0 years.
Subsequently, Kuykendall (1996) in an extensive
cross-sectional radiographic study imaged stages of
tooth formation in 118 captive chimps and reported
even younger median ages of molar initiation: M2,
1.3 years (range, 1.15– 1.48) and M3, 3.2 years
(range, 3.0 – 4.6). Despite the supposed advantage of
picking up initial mineralization of tooth germs earlier
in histological studies, Reid et al. (1998) estimated M2
initiation in Pan at between 1.7 and 1.9 years and M3
initiation between 3.6 and 3.8 years. In figure 2, for
consistency, and because for isolated teeth initiation
times can never be known, histological estimates for
molar initiation times have been used and fixed at
the average age for molar tooth types estimated in
Reid et al. (1998): M1, birth; M2, 1.75 years; M3,
3.69 years.
The issue of early molar initiation in great apes has
become confused with observations about the degree
of overlap in crown formation periods between
sequential molars. Overlap of crown formation periods
Phil. Trans. R. Soc. B (2010)
M. C. Dean 3401
has as much to do with how long or short the crown
formation period of the earlier forming molar is as it
has to do with the early or late initiation of the sub-
sequent forming molar. Smith et al. (2006) noted the
potential effect earlier or later molar initiation might
have on eruption timing and highlighted the need to
document the degree of molar overlap in free-living
versus captive animals and in hand-reared versus
mother-nursed animals. Indeed in figure 2, a spread
of molar initiation times towards earlier ages would
reduce the simulated estimates for median emergence
times in figure 3. Winkler et al. (1996) studied a much
larger originally free-living sample of 89 orangutans
and concluded that sequential molars in orangutans
had usually begun to mineralize by the time a previous
molar had reached crown completion but that variabil-
ity was too high to consistently predict that crown
initiation had always commenced prior to crown com-
pletion of a preceding molar. Smith et al. (2006) in a
histological study of Pan molars from the same individ-
uals again noted variability in the degree of molar
overlap but that more often than not this was consider-
able. The effects of captive rearing, therefore, cannot
yet be resolved.
(d) Total tooth and root formation times
Kuykendall (1996) made the important observation
that the overall duration of crown and root formation
in chimpanzee permanent incisors and canines is com-
parable with that in modern humans. Some of the best
summary data for mean age at entering a formation
stage for modern humans (Liversidge 2009) places
apex closure for mandibular I1 (8.04 years), I2 (8.69
years), canines (12.2 years) and M1 (9.38 years) at
very close to the recorded ranges reported for Pan
(Anemone et al. 1991; Anemone 1995; Kuykendall
1996). The median values and ranges of ages for
root apex completion in Pan are: I1, 9.55 years
(range, 7.99– 10.75); I2, 9.69 years (range 8.35 –
10.75); C, approximately 12 years.
When initiation times are taken into account, total
molar formation times in Pan appear to come close to
those for modern human molars (approx. 10 years).
Data for 30 observations of mean M1 apex closure
(M1, 8.14 years, range 6.47 – 10.75 years) given in
Kuykendall (1996) and data for M2 and M3 from
Anemone et al. (1991) and Anemone (1995) also
suggest overlap in total M2 and M3 formation times
with modern humans (M2, 6.5 – 9.8 years; M3, 11 –
13 years). Kuykendall (1996), however, concluded
that, unlike incisors and canines, total molar formation
times in Pan were in fact slightly shorter than those
known for modern humans but since no longitudinal
studies exist with sufficient samples of older
animals this remains speculative. Nevertheless, the
wide range of ages reported for molar apex closure
in great apes is noteworthy. Beynon et al. (1991) illus-
trated a gorilla with an open M1 apex at approximately
6 years with a little more root growth to come (see also
the additional gorilla M1 in figure 2) and Schwartz
et al. (2006) yet another gorilla at the same stage but
aged only 3.2 years. These data suggest that total
molar formation times in Gorilla may be shorter than
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3402 M. C. Dean Review. Dental development in early hominins

n=2 n=2
5.5
5.8 5.2
5.5
4.8
5.1
4.2
4.6
3.5
4.0
2.8
3.4
2.3
2.9
2.5 1.8
1.0 1.4
2.1
1.8 1.0
1.5
1.5 0.7
2.2
1.0 0.7
0.8
2.9 1.0
1.4 1.1
1.2
1.8 1.4
3.7 1.5
2.4 1.8
1.9
4.4
3.0 2.3
2.4
5.1 2.9 2.9
3.6
4.2 3.4 3.4
5.8
4.1 4.0
4.9
6.5 4.6 4.4
5.5
5.0 4.7
7.0 6.1 5.4
7.3 6.5
male n = 10 female n = 8 n=7 n=6

Figure 4. Anterior crown formation times in Pan troglodytes. Crown heights are divided into deciles and an average chronologi-
cal age of attainment for each decile of height has been calculated from estimates of enamel formation time made from counts
of daily cross striations and long period striae in longitudinal ground sections of teeth. (Data from Reid et al. 1998, 2000;
Schwartz & Dean 2001; Schwartz et al. 2001.)

those reported for Pan but sample size and these data
for captive animals may be misleading.
(e) Crown formation times
Perhaps, the most debated aspect of great ape dental
development is the time taken to form enamel, or
crown formation time. The reason for this is that it
bears heavily on whether early fossil hominins can be
judged ‘ape-like’ or ‘human-like’ with respect to this
formation time. However, enamel formation time
may be defined differently in radiographic studies
and histological studies of tooth development
(Beynon et al. 1998; Kuykendall 2001) and an added
complication is that in histological studies, different
enamel formation times are often estimated for each
cusp of a molar tooth (Smith et al. 2006). For these
reasons and others many comparisons of enamel
formation times between modern humans and
great apes have often been either unconvincing or
incomparable (Kuykendall 2001).
With the exception of lower canines (Schwartz &
Dean 2001; Schwartz et al. 2001), the data for anterior
crown formation times in great apes is very poor.
Figure 4 summarizes what is known for a few
specimens of Pan with data taken from Reid et al.
(1998, 2000), Schwartz & Dean (2001) and Schwartz
et al. (2001). However, the data for one or two speci-
mens of Gorilla published by Beynon et al. (1991)
and Schwartz et al. (2006) suggest crown formation
times for incisors may sometimes be as short as 2.7
years suggesting that Pan may be atypical in this
sense. Once again this raises the question of potentially
advanced dental development in captive animals or
perhaps of significant differences between Pan and
Gorilla that are currently unappreciated and in
addition, whether a Pan-like model for dental develop-
ment is actually the most appropriate for early
hominins.
Knowing something about anterior crown formation
times allows us to link periodic linear hypoplastic band-
ing patterns on anterior teeth that are common in many
Pan and Gorilla specimens collected from locations in
West Africa (Gabon, Cameroon) with two rainy seasons
each year (Skinner & Hopwood 2003). Besides being
generally under the weather in colder wetter conditions,
chimpanzees in particular are more susceptible to
increased intestinal parasite loads (Lilly et al. 2002)
since damp soil and sporadic forest floor flooding
present prefect conditions for eggs, protozoa and

Phil. Trans. R. Soc. B (2010)

 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
40
crown and root extension rate
35
30
25
(mm d–1)
20
15
10
5
0 rates should begin to fall off at the time of initial func-
–1 0 1 2 3
tooth formation time (years)
Figure 5. Extension rates for the same sample of Pan M1s
shown in figure 2. Rates are high in the cusps of the crown
but then quickly fall to values between 4 and 8 mm d21
(see also Dean 2009). These data for 14 teeth are each
aligned (arrow) around the mean age (3.8 years) of peak
height velocity (PHV) for this sample, which displaces the
initiation and completion of tooth formation to earlier or
later ages but highlights the root spurt more clearly. The
mean chronological age and range of ages at which PHV
occurs during early root formation (3.01– 4.65 years, s.d.
0.48) broadly mirrors those ages reported for gingival
emergence in Pan M1s.
helminths to flourish. Seasonal fluctuations such as this
increase the likelihood of individuals succumbing to any
number of conditions that are known to underlie linear
enamel hypoplasias (particularly prolonged bouts of
diarrhoea or dysentery) and are a likely explanation
for many wild-collected great ape permanent canines
having, for example, 15 or so faint bands on canine
crowns that took close to 7.5 years to form enamel.
The data presented in figure 2 for molar crown
(protoconid) formation times in Pan are for slightly
bigger sample sizes than previous studies (but compar-
able to those of Smith et al. 2006, 2010) although they
are not based on counts or error-prone periodicities of
long period incremental markings but only on counts
of daily increments close to the EDJ: M1, 2.3 years
(range 1.78 – 2.66); M2, 2.38 years (range 1.72–
3.19); M3, 2.71 years (range 2.19 – 3.34). Mean
values for modern human (protoconid) formation
times (Reid & Dean 2005) are greater than these:
M1 (3.1 years), M2 (3.2 years) and M3 (3.27 years)
but there is overlap in the ranges (for example, see
Reid & Dean 2005 and Mahoney 2008) such that an
individual molar tooth could not always be attributed
to Pan or Homo on the basis of molar crown formation
time alone.
(f) Rates of root formation and the timing
of gingival emergence
All hominoid teeth show a pattern of change in exten-
sion rate that is dominated by an initial high rate in the
cusps of the crown but which then quickly reduces to a
more constant rate in the lateral enamel (Dean 2009).
The transition from cervical enamel formation to
cervical root formation in hominoid teeth appears to
occur without any abrupt change to the rate of
growth in tooth length (figure 5). In many teeth, but
Phil. Trans. R. Soc. B (2010)
Review. Dental development in early hominins M. C. Dean 3403
not all, the root extension rate then rises to a peak
and falls off again. In very long tooth root, there may
again be a rise in root extension rate towards apex
completion. In the small sample of Pan, M1 mesiobuc-
cal roots plotted in figure 5, the mean age at which this
early peak in root extension rate occurs (3.8 years,
range ¼ 3.01 – 4.65 years, s.d. 0.48) is close to that
reported for gingival emergence. While this apparent
signature for gingival emergence is unlikely to be a
simple epigenetic reflection of tooth movement
through the bone, it is intuitive that root extension
4 5 6 7 8 9 tional occlusion. When the data for extension rates are
aligned around this early mean peak height velocity
(PHV) rather than plotted with respect to initiation
at birth, this small rise in root extension rate is more
easily seen and not smoothed out (figure 5). For this
sample of Pan M1s, PHV is 8.7 mm d21 (range 6.1 –
10.2 mm d21). The expression of this peak in early
root growth becomes weaker distally in M2s and
M3s but is still there although it occurs later into
root formation. PHV in this sample of M2s was
6.7 mm d21 and occurred at 4.7 years (range 3.4 – 6.4
years, s.d. 0.85) into tooth formation.
(g) Summary points about dental development
in P. troglodytes
The sequence and times of initiation as well as total
tooth formation times of incisors and canines are
little different from modern humans. The ages of gin-
gival emergence of incisors and canines are also little
different. Anterior crown formation times (with the
exception of male canines crowns which take longer
to form) are only slightly longer than average
modern human crown formation times. It is the
initiation times and eruption times of the molar denti-
tion in modern humans that are drawn out to later ages
with prolongation of the growth period. The greatest
shift in timing appears to be in eruption times, which
can be observed both at later stages of root formation
in modern humans as well as at later ages than in Pan.
This is most marked in M3 that initiates approximately
4.5 years later in modern humans than in Pan and
which erupts into functional occlusion approximately
8 years later at close to 18 years of age. Average total
molar tooth formation times in Pan are shorter than
those in modern humans, but it only seems by between
one and two years, and while molar crown formation
times are also shorter on average, this is only by six
to nine months with overlapping ranges. It appears
(figure 2) that there is little or no difference in the
rate of growth in height of the molar crowns or roots
between Pan and modern humans. Besides these com-
parisons of timing in tooth formation, it may well be
that great ape teeth contain information about seasonal-
ity and perhaps even about their own eruptive history.
5. THE EVIDENCE FOR A CHRONOLOGY OF
DENTAL DEVELOPMENT IN FOSSIL HOMININS
(a) Molar eruption times
Bromage & Dean (1985) estimated the age at death of
four early hominin specimens with M1 just prior to or
at functional occlusion (Sts 24, Australopithecus
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3404 M. C. Dean Review. Dental development in early hominins
africanus; LH 2, Au. afarensis; SK 62 and SK 63, Para-
nthropus robustus) to be 3.2 – 3.5 years on the basis of
perikymata counts on lower permanent incisors. Sub-
sequently, a histological study of SK 63 (Dean et al.
1993) placed gingival emergence nearer to 4 years.
More recently, Lacruz et al. (2005) estimated M1
emergence into occlusion and age at death of the
Taung child (Au. africanus) to be between 3.73 and
3.93 years on the basis of M1 enamel formation
times and length of mesial root formed (5 – 6 mm:
Conroy & Vannier 1991a,b).
The only evidence for the status of the developing
dentition in Australopithecus of any species around
the age of M2 eruption comes from scans and radio-
graphs of MLD 2 and Stw 327, both of which are
described as having M2s recently in functional occlu-
sion (Skinner & Sperber 1982; Conroy & Vannier
1991a). While the M3 crypt of MLD 2 is only partially
preserved, CT scans of Stw 327 show a completed M3
crown (Conroy & Vannier 1991a). Skinner & Sperber
(1982) have drawn attention to the permanent canines
of MLD 2, which are still deep in their crypts and that
on CT scans (Conroy & Vannier 1991a) have less root
length formed than crown length. However, no histo-
logical age estimates are possible for either of these
specimens. But if the timing of canine root length
formed could be shown to match that known for
Pan, then the standards defined by Kuykendall
(1996) would provide a median age estimate of 7.6
years for MLD 2 (range 6.10– 8.75)—but this is
speculative. This age range, however, spans the range
of histological estimates for age at death of KNM-
WT 15000 (attributed to Homo erectus at 1.5 Ma),
where M2s were also just in functional occlusion and
where the one preserved upper M3 crown was also
just complete (Dean & Smith 2009).
(b) Molar initiation times
The approximately 3-year-old infant hominin dated to
3.3 Ma from Dikika, Ethiopia (Dik-1-1), and attribu-
ted to Au. afarensis had M1 crown complete with just
1.6 mm of mesiobuccal root formation (Alemseged
et al. 2006). The occlusal surface of the M2 crown
had already formed. This is clear evidence for early
initiation of M2 and of overlap in molar enamel for-
mation. KNM-ER 1477, a juvenile P. boisei mandible
roughly the same chronological age, preserves the
mesial portion of what may have been a well-formed
M2 crypt. However, this is the only other potential evi-
dence in any early hominin specimen that M2 may
already have been mineralizing at the time of M1
crown completion. The mineralizing P4 in this speci-
men would be expected to match M2 but this
cannot be known. A number of juvenile P. boisei or
P. robustus specimens exist with M1 at or close to
crown completion (Skinner & Sperber 1982; Dean
1987; Conroy & Vannier 1991b; Lacruz 2006). Relative
to this stage of M1 formation several of the P. robustus
specimens (SK 438, SK 64, SK 3978) appear to
show delayed premolar formation when compared
with the P. boisei specimens (KNM-ER 1477, KNM-
ER 1820) and one explanation for this might be shorter
M1 crown formation times in P. robustus.
Phil. Trans. R. Soc. B (2010)
Unlike Pan no evidence exists to show early
initiation of M3 in fossil hominins. Stw 151, from
the late Member 4 breccia deposit at Sterkfontein, is
described as a specimen with a dentition ‘not fully dis-
tinct from that of Au. africanus but with a cranial
morphology more derived in some characters’
(Moggi-Cecchi et al. 1998). While there is a small
mandibular M3 crypt in Stw 151, it is still too small
to have accommodated a mineralizing tooth germ,
which must, therefore, have initiated after M2 crown
completion. Another specimen (SK 63, attributed to
P. robustus) contains M2 crowns that are not quite
completed but at this stage, only incipient M3 crypt
depressions in the root of the ascending mandibular
rami are present. Certainly, M3 initiation could not
have occurred prior to M2 crown completion in this
specimen.
(c) Total tooth formation times
The evidence for total anterior tooth formation times
in early hominins is lacking but what there is suggests
little difference from Pan. Median ages for combined
sexes in Pan for lower incisors at the same develop-
mental stage (Kuykendall 1996) would estimate age
at death of Stw 151 at 4.95 years (range 4.61 – 5.22).
This is very close to the histological estimate of
5.2 – 5.3 years for this specimen (Moggi-Cecchi et al.
1998). There is then no evidence to suggest that the
timing of root formation in this early hominin was
different from that observed in Pan. Both standards
for lower lateral incisors in modern humans (8.0
years, s.d. 0.99; Liversidge 2009) and Pan (8.04
years, inter-quartile range 7.66– 8.86; Kuykendall
1996) also each give median age at death estimates
that match histological estimates for the H. erectus
youth from Nariokotome (7.6 – 8.8 years, Dean &
Smith 2009). Again this suggests that there is no evi-
dence for any change in total incisor tooth formation
times in early hominins, but histological evidence for
ages of hominin specimens with near completed
canine roots are needed to show that this also holds
true for canines.
Stw 151 is aged histologically to between 5.2 and
5.3 years at death (Moggi-Cecchi et al. 1998). It had
M1s with one or more incomplete root apex at the
time M2, premolar and canine crowns had just com-
pleted enamel formation. This age implies that root
apex closure of M1 was at the earliest end of the age
range reported for Pan and occurred close to M2
crown completion. The end of M2 crown completion
in KNM-WT 15000 (H. erectus) was also estimated
to have completed between 4.2 and 4.9 years on the
basis of perikymata counts (Dean & Smith 2009).
Other early hominin specimens from Laetoli, LH 3
and LH 6 (attributed to Au. afarensis) consist only of
isolated teeth (White 1977). However, in both speci-
mens, the upper M1 is at a similar stage of root apex
formation as Stw 151 and each have permanent
canine and premolar crowns close to or just com-
pleted. Close correspondence of the canine crown
perikymata counts (Stw 151 ¼ 140 and LH 6 ¼ 134)
suggests that LH 6 was close in age with the same pat-
tern of tooth formation and the same early age for
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Review. Dental development in early hominins
M1 root completion. No M2s are preserved for
comparison in either of these specimens from Laetoli.
While speculative, a tooth fragment from Allia Bay,
Kenya, attributed to Au. anamensis (KNM-ER 30748)
may contain information about molar eruption in early
hominins. It is plotted in figure 2 as an M2, since it has
an enamel formation time (2.7 years) beyond the range
of the Pan M1s sampled here (see also Ward et al.
2001). It contains a marked early root spurt of
9.8 mm d21 at 4.2 years into tooth formation that is
within the M2 range for Pan (3.44 – 6.38 years). If
M2 initiation in Au. anamensis was close to 1.75
years, as in Pan, and if early root PHV actually reflects
the eruptive process, then this would place functional
occlusion of this tooth towards the lower end of the
range reported for M2 in Pan (5.6 – 7.8 years)
(Nissen & Riesen 1964).
A number of chronologically older hominin speci-
mens exists with incomplete M3 roots. KNM-ER
1802 has a left M3 with just one wear facet on the pro-
toconid and a ca 9 mm long mesial root impression in
the alveolar bone for the right M3. Sts 52 (attributed
to Au. africanus), OH5 and KNM-WT 17400 both
attributed to P. boisei, are specimens closer to dental
maturity but there is no histological evidence at all
to estimate their chronological age, only a hint from
periapical radiographs of the upper canine of OH5
that this root apex may have been recently completed
by age at death (Skinner & Sperber 1982).
(d) Crown formation times
Perikymata counts on hominin incisors and canines,
especially those attributed to Paranthropus, all point
to anterior crown formation times having been shorter
than those known for modern humans and for Pan
(Dean et al. 1993, 2001; Dean & Reid 2001). One
lower canine tooth attributed to Au. africanus
(Sts 50) has 170 perikymata suggesting a crown for-
mation time of around four years or more (Dean &
Reid 2001) but in general the anterior teeth with the
greatest crown formation times appear to be those of
Au. anamensis and Au. afarensis. Here, canine enamel
formation times come closest to those known for
modern humans. Suwa et al. (2009a) counted 193
perikymata on the upper canine of ARA-VP-6/1 (the
holotype of Ardipithecus ramidus and a probable
male). This suggests that canine crown formation
took between 4.3 and 4.8 years in this specimen
(Suwa et al. 2009a) and so was potentially within the
range recorded for female Gorilla and Pongo, but
below the range so far recorded for female Pan canines
(Schwartz & Dean 2001). The several clear regularly
spaced hypoplastic bands illustrated on this specimen
in Suwa et al. (2009b) are reminiscent of what are
likely to be seasonally related cycles of poor growth on
living great ape canines (Skinner & Hopwood 2003).
If there were eight or nine such bands on ARA-VP-6/
1 and on other Ar. ramidus canines, this would strongly
suggest that Ar. ramidus existed in a seasonal environ-
ment with two colder wetter seasons per year.
At least seven juvenile specimens attributed to
P. boisei (KNM-ER 1477, KNM-ER 812, KNM-ER
1820, OH 30) or P. robustus (KB 5223, SK 64,
Phil. Trans. R. Soc. B (2010)
M. C. Dean 3405
SK 3978) have M1 at or close to crown completion (-
Skinner & Sperber 1982; Dean 1987; Conroy &
Vannier 1991b; Lacruz 2006). Some have been aged
on the basis of perikymata counts on anterior tooth
germs at between 2.5 and 3.0 years of age at death
(Dean 1987) but with some root formation. This fits
well with a histologically derived estimate of 2.4
years for M1 crown formation time in SK 63 (P. robus-
tus) from Swartkrans, South Africa (Dean et al. 1993).
Lacruz & Ramirez Rozzi (2010) have made histologi-
cal estimates of metaconid as well as total crown
formation times of two Au. afarensis molar fragments
(AL 333-52 and AL 336-1) at between 2.2 and 2.4
years. Beynon & Wood (1987) calculated a range of
molar crown formation times of 2.12 – 2.59 years in
P. boisei, while Ramirez Rozzi (1993, 1995) found
ranges of 1.93– 2.49 years for P. aethiopicus but a
greater range for enamel formation times of
P. boisei molars of all types (2.67 – 3.43 years). In
P. robustus from Kromdraai, Lacruz (2006) calculated
protoconid formation times at between 1.98 and
2.38 years and metaconid time to be near identical
(1.92 –2.37 years) but Lacruz et al. (2006) reported
protocone formation times in two Au. africanus
molars to be greater than this (M1, 2.74 years and
M2, 3.0 – 3.2 years). These latter two crown for-
mation times are very close to mean modern
human values. In general, molar crown formation
times in early hominins are less than those in
modern humans and more similar to those of Pan
but there is considerable overlap in the ranges and
still insufficient data to compare sample mean
values statistically.
(e) Summary points about dental development
in early hominins
The cumulative rates of enamel formation follow a
similar trajectory in both Pan and early hominins (irre-
spective of enamel thickness and crown formation
times) that is faster than that in modern humans
(Dean et al. 2001; Lacruz et al. 2008). Estimates for
gingival emergence times for M1 in several early homi-
nin specimens all fall within the range expected for
Pan, and in fact are all earlier than the time proposed
for free-born, free-living chimpanzees. There is, how-
ever, no direct evidence at all for ages of M2 and
M3 eruption among the earliest hominins. The evi-
dence for molar initiation times provides only one
example (Dikika: Dik-1-1) where there is clear early
M2 initiation with respect to M1 and there is no evi-
dence at all for M3 initiation occurring prior to
completion of M2 enamel formation in any early
hominin specimen. Total molar tooth formation
times have only been estimated in three hominin speci-
mens, and appear to fall closest to the earlier ages
known for Pan. In contrast, those of incisors appear
similar to those observed in Pan. Anterior crown for-
mation times are almost always consistently less than
those known for Pan with the shortest crown formation
times occurring in Paranthropus. Enamel (crown)
formation times in molars are generally within the
ranges known for Pan molars (but occasionally also
fall well within modern human ranges).
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
3406 M. C. Dean Review. Dental development in early hominins
6. DISCUSSION
Constructing a chronology for dental development in
P. troglodytes as a comparative model for early hominins
is useful for a number of reasons. First, it highlights the
processes whereby dental development is likely to have
kept pace with prolongation of the period of general
growth during hominid evolution. These seem to be
confined to the sequence of molar development and
to have involved shifts in the timing of initial mineral-
ization, slightly faster crown formation rates and
particularly, earlier times of tooth emergence into
functional occlusion. The cumulative effects of each
of these are most fully expressed in molar emergence
times, which appear to be the clearest measure of com-
parative development than any one of the components
that contribute to it. Estimates of M1 emergence times
in fossil hominins, as well as observations of early
molar initiation, and in some cases shorter crown for-
mation times, resemble Pan more closely than modern
humans. However, too few specimens exist to provide
clear evidence for early initiation or earlier gingival
emergence times of M2 or M3 among australopith
specimens, although the evidence for this is a little
better in early Homo (Dean et al. 2001; Dean &
Smith 2009). The model reveals, however, that the
key indicators of a Pan-like dental maturation pattern
would include early M3 initiation with respect to M2
crown formation time and a lesser proportion of root
formed at gingival emergence in all molar tooth
types than in modern humans.
A second point to emerge from the model for Pan is
that some things appear to be little different between
Pan and Homo and, it follows, might not be expected
to differ in early hominins. Total anterior tooth for-
mation times, and maybe also those for molars, fall
within the same range, all be it a broad range. Few
radiographic studies of molar development in Pan
have included older animals and few of the individual
plots in figure 2 extend all the way to root apex closure
and moreover, it is the distobuccal root (not the mesio-
buccal root shown in figure 2) in both Pan and Gorilla
that on radiographs completes formation last (Dean &
Wood 2003). It is highly likely, therefore, that future
studies will show total molar formation times to be
equal in Pan and Homo. In this respect, the evidence
for at least three individual australopith specimens
suggests that total M1 and M2 formation time may
have been at the low end of the range reconstructed
for Pan. The plot of M2 (figure 2) attributed to Au.
anamensis (KNM-ER 30748) has a crown formation
time at the upper limit of the M2 range for Pan
(2.66 years) but a total tooth formation time of only
5.5 years (but with a little root still to form) and a
faster rate of root formation generally than in Pan
that might prove to be more typical of Gorilla. Shorter
anterior crown formation times in many australopiths
and earlier times for root completion might also turn
out to fit a Gorilla model better than a Pan model.
This mosaic of great ape-like dental development
among australopiths is perhaps what one ought to
expect given the gorilla-like anatomy of the scapula
of Dikika, Dik-1-1 (Alemseged et al. 2006) and the
gorilla-like mandibular morphology of Au. afarensis
mandibles (Rak et al. 2007).
Phil. Trans. R. Soc. B (2010)
A third observation about the chronological model
of dental development in Pan compared with that in
early hominins is that anterior tooth growth does not
appear to reflect general somatic growth. While total
anterior tooth formation times appear to be little
different, anterior crown formation times in australo-
piths are very variable but always shorter than in Pan
(Dean & Reid 2001; Dean et al. 2001). In this respect,
the comparative chronological model for anterior
tooth crown formation times in Pan differs completely
from that reconstructed for australopiths. Crown for-
mation time does not relate in any simple way to
crown height (Dean 2009) within a tooth type. For
example, there is nothing to distinguish the enamel
formation times of smaller P. robustus canines from
taller canines of H. erectus (Dean et al. 1993, 2001).
The fact that both enamel thickness and anterior
tooth crown height, characters that can be broadly
linked to dietary specialization, are not tightly linked
to the time taken to form crowns is interesting. If in
fact total anterior tooth formation times are relatively
more stable than anterior tooth morphology appears
to be, then perhaps crown formation times might be
a better candidate for exploring phylogenetic related-
ness among closely related species of early hominins
than tooth morphology. An interesting case in point
worth further consideration is the short time taken to
form the reduced canine crown heights of Ar. ramidus
(Suwa et al. 2009a).
All observations made so far on fossil and living
apes and on early hominins indicate that M1 eruption
times would have fallen within the simulated ranges for
free-living Pan shown in figure 3 and none appear to
fall within the ranges known for modern humans.
Interestingly, all predictions so far for M1 emergence
in fossil apes (Kelley 1997, 2002; Kelley & Smith
2003; Dean 2006) actually fall below the simulated
median age of attainment for M1 emergence predicted
in figure 3 as indeed do most estimates for early homi-
nins. This raises questions about how different great
ape dental development in the Late Miocene might
have been to that known today for modern P. troglodytes
and how good a model modern Pan is for comparisons
with the earliest hominins. It also highlights the need
to reconstruct a chronology for dental development
in Gorilla to place that for Pan in a better modern com-
parative perspective. It remains a real possibility that
the chronological dental development in the earliest
hominins was more similar to that in modern Gorilla
than to modern Pan. Were this the case it would
raise very interesting issues about early hominin life-
history strategies of the kind discussed by Kelley &
Schwartz (2009). The issue of advanced dental matur-
ity in captive hand-reared great apes suggests that even
M1 emergence times of approximately 4.5 years pre-
dicted for H. erectus (Dean et al. 2001; Dean &
Smith 2009) would still fall comfortably within the
simulated range for wild-born chimpanzees (figure 3)
as has been suggested by Zihlman et al. (2004) but
predictions for M2 and M3 eruption of approximately
8 and approximately 14 years, respectively, in
H. erectus would not.
No convincing evidence exists for any differences in
the chronology of molar development and emergence
 Downloaded from rstb.royalsocietypublishing.org on October 24, 2010
Review. Dental development in early hominins
between early hominin taxa, but estimates of chrono-
logical age in specimens around 2.5 years and
younger make it clear that tooth wear was excessive
in some infant and juvenile late australopiths. Even
thicker deciduous dental enamel was insufficient to
compensate for this, resulting in extensive islands of
dentine exposure on deciduous teeth very early in
development (Aiello et al. 1991). Moggi-Cecchi et al.
(2010) describe an infant P. robustus hemi-mandible
from Drimolen (DNH-44) with an unworn erupting
Rdm2 where islands of dentine are exposed on the
Rdc and on four out of five cusps of the Rdm1, argu-
ably within a year or so of birth. The obvious
inference that some early hominin juveniles were
taking considerable quantities of supplementary
foods at a very early age cannot, at the moment, be
extended to assuming they were also weaned early
and that interbirth intervals were relatively short in
these later australopiths, although this is one interpret-
ation of those observations (Aiello et al. 1991; Dean
2006). Once again, there is the tantalizing suggestion
that a Gorilla-like life-history model may be a better
match for some, but not all, early hominins. Many
life-history variables in Gorilla such as age at weaning
(reviewed in Aiello et al. 1991) age at first reproduction
and interbirth interval (Watts 1991; Robson & Wood
2008; Kelley & Schwartz 2009) are reported to be
earlier than in Pan and Pongo (Wich et al. 2004).
However, a firm link with these variables and earlier
dental development remains illusive (Kelley &
Schwartz 2009; Humphrey 2010). In the future,
combined studies of tooth microstructure that put a
chronological time scale to more sophisticated
models of changing infant diets may shed more light
on early life-history events such as these during the
first four million years of human evolution (Humphrey
et al. 2008; Humphrey 2010).
I thank Alan Walker and Chris Stringer for inviting me to
contribute to this discussion meeting. Much of the
research underpinning this paper has been supported by
the Leverhulme Trust and the Royal Society through
grants to me. I thank Don Reid and Gary Schwartz for
helping with the construction of figure 4 and I am
especially grateful to Louise Humphrey, Jay Kelley, Helen
Liversidge and Holly Smith for discussions that have
helped develop some of the ideas set out here.
ENDNOTE
1
For consistency and clarity, ages given in the literature are cited here
as follows: Prenatal and postnatal ages up to 1 month are given in
days, those between 1 month and 1 year in months and those greater
than this in years.
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Phil. Trans. R. Soc. B | vol. 365 no. 1556 pp. 3263–3410 | 27 Oct 2010
ISSN 0962-8436

volume 365

27 October 2010 number 1556

volume 365 . number 1556 . pages 3263–3410
pages 3263–3410
The first four million years of human
evolution In this Issue

Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer The first four million years of human evolution
Introduction Papers of a Discussion Meeting issue organized and edited by Alan Walker and Chris Stringer
The first four million years of human evolution 3265
A. Walker & C. Stringer
Articles
In search of the last common ancestor: new findings on wild chimpanzees 3267
W. C. McGrew
More reliable estimates of divergence times in Pan using complete mtDNA sequences
and accounting for population structure 3277
A. C. Stone, F. U. Battistuzzi, L. S. Kubatko, G. H. Perry Jr, E. Trudeau, H. Lin & S. Kumar
Spinopelvic pathways to bipedality: why no hominids ever relied on a bent-hip–bent-knee gait 3289
C. O. Lovejoy & M. A. McCollum
Arboreality, terrestriality and bipedalism 3301
R. H. Crompton, W. I. Sellers & S. K. S. Thorpe
Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction 3315
M. Brunet

The first four million years of human evolution

Phylogeny of early Australopithecus: new fossil evidence from the Woranso-Mille (central Afar, Ethiopia) 3323
Y. Haile-Selassie
Anterior dental evolution in the Australopithecus anamensis–afarensis lineage 3333
C. V. Ward, J. M. Plavcan & F. K. Manthi
Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis 3345
P. S. Ungar, R. S. Scott, F. E. Grine & M. F. Teaford
An enlarged postcranial sample confirms Australopithecus afarensis dimorphism was similar
to modern humans 3355
P. L. Reno, M. A. McCollum, R. S. Meindl & C. O. Lovejoy
The cranial base of Australopithecus afarensis: new insights from the female skull 3365
W. H. Kimbel & Y. Rak
Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000 3377
F. Spoor, M. G. Leakey & L. N. Leakey
Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene 3389
J. A. Lee-Thorp, M. Sponheimer, B. H. Passey, D. J. de Ruiter & T. E. Cerling
Retrieving chronological age from dental remains of early fossil hominins to reconstruct human
growth in the past 3397
M. C. Dean

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