, 69 (2009);
et al.Gen Suwa,
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on October 12, 2009
VOL 326 2 OCTOBER 2009
Paleobiological Implications of the
Ardipithecus ramidus Dentition
Gen Suwa, Reiko T. Kono, Scott W. Simpson, Berhane Asfaw, C. Owen Lovejoy, Tim D. White
enamel thickness, and isotopic composition of teeth
provide a wealth of information about phylogeny, diet,
and social behavior. Ardipithecus ramidus was origi-
nally defined in 1994 primarily on the basis of recov-
ered teeth, but the sample size was small, limiting
comparison to other primate fossils. We now have over
145 teeth, including canines from up to 21 individuals.
The expanded sample now provides new information
regarding Ar. ramidus and, using comparisons with
teeth of other hominids, extant apes, and monkeys,
new perspectives on early hominid evolution as well.
In apes and monkeys, the male’s upper canine tooth
usually bears a projecting, daggerlike crown that is
continuously sharpened (honed) by wear against a
specialized lower premolar tooth (together these form
the C/P3complex). The canine tooth is used as a slic-
ing weapon in intra- and intergroup social conflicts.
Modern humans have small, stublike canines which
function more like incisors.
All known modern and fossil apes have (or had) a honing C/P3com-
plex. In most species, this is more developed in males than females (in
a few species, females have male-like large canines, either for territo-
rial defense or for specialized feeding). The relatively large number of
Ar. ramidusteeth, in combination with Ethiopian Ar. kadabba, Kenyan
Orrorin, and Chadian Sahelanthropus [currently the earliest known
hominids at about 6 million years ago (Ma)], provide insight into the
ancestral ape C/P3complex and its evolution in early hominids.
In basal dimensions, the canines of Ar. ramidus are roughly as
large as those of female chimpanzees and male bonobos, but their
crown heights are shorter (see figure). The Ar. ramidussample is now
large enough to assure us that males are represented. This means that
male and female canines were not only similar in size, but that the
male canine had been dramatically “feminized” in shape. The crown
of the upper canine in Ar. ramiduswas altered from the pointed shape
seen in apes to a less-threatening diamond shape in both males and
females. There is no evidence of honing. The lower canines of Ar.
ramidus are less modified from the inferred female ape condition
than the uppers. The hominid canines from about 6 Ma are similar in
size to those of Ar. ramidus, but (especially) the older upper canines
appear slightly more primitive. This suggests that male canine size
and prominence were dramatically reduced by ~6 to 4.4 Ma from an
ancestral ape with a honing C/P3complex and a moderate degree of
male and female canine size difference.
eeth are highly resilient to degradation and
therefore are the most abundant specimens in
the primate fossil record. The size, shape,
In modern monkeys and apes, the upper canine is important in
male agonistic behavior, so its subdued shape in early hominids and
Ar. ramidus suggests that sexual selection played a primary role in
canine reduction. Thus, fundamental reproductive and social behav-
ioral changes probably occurred in hominids long before they had
enlarged brains and began to use stone tools.
Thick enamel suggests that an animal’s food intake was abrasive;
for example, from terrestrial feeding. Thin enamel is consistent with
a diet of softer and less abrasive foods, such as arboreal ripe fruits. We
measured the enamel properties of more than 30 Ar. ramidus teeth.
Its molar enamel is intermediate in thickness between that of chim-
panzees and Australopithecus or Homo. Chimpanzees have thin
enamel at the chewing surface of their molars, whereas a broad con-
cave basin flanked by spiky cusps facilitates crushing fruits and
shredding leaves. Ar. ramidus does not share this pattern, implying a
diet different from that of chimpanzees. Lack of thick enamel indi-
cates that Ar. ramidus was not as adapted to heavy chewing and/or
eating abrasive foods as were later Australopithecus or even Homo.
The combined evidence from the isotopic content of the enamel, den-
tal wear, and molar structure indicates that the earliest hominid diet
was one of generalized omnivory and frugivory and therefore dif-
fered from that of Australopithecus and living African apes.
Dentitions from human (left), Ar. ramidus (middle), and chimpanzee (right), all males.
Below are corresponding samples of the maxillary first molar in each. Red, thicker enamel
(~2 mm); blue, thinner enamel (~0.5 mm). Contour lines map the topography of the crown
and chewing surfaces.
When citing, please refer to the full paper, available at DOI 10.1126/science.1175824.
on October 12, 2009
Paleobiological Implications of the
Ardipithecus ramidus Dentition
Gen Suwa,1* Reiko T. Kono,2Scott W. Simpson,3Berhane Asfaw,4
C. Owen Lovejoy,5Tim D. White6
The Middle Awash Ardipithecus ramidus sample comprises over 145 teeth, including associated
maxillary and mandibular sets. These help reveal the earliest stages of human evolution.
Ar. ramidus lacks the postcanine megadontia of Australopithecus. Its molars have thinner
enamel and are functionally less durable than those of Australopithecus but lack the derived Pan
pattern of thin occlusal enamel associated with ripe-fruit frugivory. The Ar. ramidus dental
morphology and wear pattern are consistent with a partially terrestrial, omnivorous/frugivorous
niche. Analyses show that the ARA-VP-6/500 skeleton is female and that Ar. ramidus was nearly
monomorphic in canine size and shape. The canine/lower third premolar complex indicates a
reduction of canine size and honing capacity early in hominid evolution, possibly driven by
selection targeted on the male upper canine.
vide crucial evidence on variation, phylogenetic
relationships, development, and dietary adapta-
tions. Furthermore, because canines function as
weapons in interindividual aggression in most
anthropoid species, they additionally inform as-
pects of social structure and behavior.
We have now recovered and analyzed a sam-
ple of 145 non-antimeric tooth crowns compris-
ing 62 cataloged dentition-bearing specimens of
Ardipithecus ramidus from the Lower Aramis
Member of the Sagantole Formation, about five
times more than previously reported (1, 2) (Fig.
1 and table S1). All permanent tooth positions
are represented, with a minimum of 14 individ-
uals for both the upper canine and upper second
molar (M2) positions. Excluding antimeres, 101
teeth have measurable crown diameters. In ad-
dition, seven Ar. ramidus specimens with teeth
have been described from Gona (3). These are
broadly comparable to their Aramis counterparts
in size, proportions, and morphology but slight-
ly extend the smaller end of the species range in
some mandibular crown diameters.
The major morphological characteristics of
the Ar. ramidus dentition have been outlined
in previous studies of Aramis and Gona fos-
ossilized teeth typically represent the most
abundant and best preserved remains of
hominids and other primates. They pro-
sils (1, 3, 4). Comparisons of Ar. ramidus with
Late Miocene hominids (Ar. kadabba, Orrorin
tugenensis, and Sahelanthropus tchadensis) have
identified slight but distinct differences, partic-
ularly in the canine (4–6). Other subtle features
of incisors and postcanine teeth have been noted
as phylogenetic or taxonomic distinctions (5–10).
However, the most recent and comprehensive
evaluation of the available Late Miocene mate-
rials concluded that these differences are minor
compared with extant ape (and later hominid)
genus-level variation and that both Ar. ramidus
and Ar. kadabba dentitions exhibit phenetic
similarities with early Australopithecus (4).
The expanded Ar. ramidus sample of the
present study allows a more definitive phylo-
genetic placement of Ar. ramidus relative to the
more primitive Ar. kadabba and the more derived
Au. anamensis and Au. afarensis (11). Here, we
focus on the paleobiological aspects of the Ar.
ramidus dentition, including variation, size, and
scaling, probable dietary niche, and canine/lower
third premolar (C/P3) complex evolution and its
behavioral implications. We also address the
alleged phylogenetic importance (7) of enamel
thickness in Ar. ramidus (1). This is now made
possible by the more comprehensive dental col-
lection that includes key associated dental sets.
Crown size, proportions, and variation.
The Ar. ramidus dentition is approximately
chimpanzee-sized (fig. S1 and tables S2 to S4).
Mean canine size is comparable to that of fe-
male Pan troglodytes, although the incisors are
smaller. Upper and lower first molars (M1s)
are P. troglodytes–sized but tend to be bucco-
lingually broader (figs. S1 to S3). The second and
third molars (M2s and M3s) are both absolutely
and relatively larger (figs. S1 and S4 to S6).
Postcanine size and proportions of Ar. ramidus
are similar to those of Ar. kadabba and other
~6.0-million-year-old forms (O. tugenensis and
S. tchadensis) (4–10), as well as to many Mio-
cene hominoids (although Miocene ape lower
molars tend to be buccolingually narrower)
Variation within the Aramis dental sample
is low. In modern anthropoids, the coefficient
of variation (CV) is lowest in M1 and M2, with
single-sex and mixed-sex values usually rang-
ing from about 3.5 to 6.5 (12–14). At Aramis,
Ar. ramidus upper and lower M1s and M2s are
less variable (CVs ranging from 2.5 to 5.6)
than those of Australopithecus afarensis and Au.
anamensis (table S2). However, these Australo-
pithecus samples represent multiple sites and
span a much greater time than the Aramis fos-
sils (11). The low variation seen in Aramis Ar.
ramidus probably reflects spatially and tempo-
rally restricted sampling and low postcanine
sexual dimorphism as in Pan (15) (table S5).
The Aramis postcanine dentition is also mor-
phologically more homogenous than known
Australopithecus species samples. For example,
the six relatively well-preserved M1s (Fig. 1)
differ little in features otherwise known to vary
widely within hominid and modern hominoid
species (16, 17), including Carabelli’s expres-
sion, occlusal crest development, and hypocone
lingual bulge. This suggests that the Aramis Ar.
ramidus collection samples regional demes or
local populations with persistent idiosyncratic
tendencies. The ubiquitous occurrence of single
rooted lower fourth premolars (P4) (now seen in
eight non-antimeric Aramis P4s) suggests in-
creased frequency of otherwise rare variants from
genetic drift, absent substantial selection for
larger and/or more complicated root systems
(18). Because this anatomy is shared with Gona
Ar. ramidus (3), it appears characteristic of this
Morphology and evolution of the C/P3com-
plex. The C/P3complex of anthropoids has be-
havioral and evolutionary importance because
canine size and function are directly linked to
male reproductive success (19). Therefore, clar-
ifying the tempo and mode of the evolution of
the C/P3 complex, from hominid emergence
through its early evolution, is important.
Not counting antimeres, 23 upper and lower
canines from 21 Ar. ramidus individuals are now
known from Aramis. Three more have been de-
scribed from Gona (3), and seven from the ~6.0-
million-year-old Ar. kadabba, O. tugenensis, and
S. tchadensis (4–10). There are no examples of a
distinctly large male morphotype in any of these
collections (Fig. 1 and figs. S7 and S8), suggest-
ing that canine sexual dimorphism was minimal
in Mio-Pliocene hominids. In basal crown di-
mensions, Ar. ramidus canine/postcanine size
ratios overlap extensively with those of modern
and Miocene female apes (fig. S9). Absolute
and relative canine heights are also comparable
to those of modern female apes, although canine
height appears exaggerated in P. troglodytes
[Fig. 1; figs. S8, S10, and S11; and supporting
online material (SOM) text S1].
1The University Museum, the University of Tokyo, Hongo,
Bunkyo-ku, Tokyo, 113-0033 Japan.2Department of Anthro-
Shinjuku-ku, Tokyo, 169-0073 Japan.3Department of Anat-
omy, Case Western Reserve University School of Medicine,
Cleveland, OH 44106–4930, USA.4Rift Valley Research Ser-
vice, Post Office Box 5717, Addis Ababa, Ethiopia.5Depart-
ment of Anthropology, Division of Biomedical Sciences, Kent
State University, Kent, OH 44240–0001, USA.6Human Evo-
lution Research Center and Department of Integrative Biol-
ogy, 3101 VLSB, University of California Berkeley, Berkeley,
CA 94720, USA.
*To whom correspondence should be addressed. E-mail:
2 OCTOBER 2009VOL 326
on October 12, 2009
Canine shape of Ar. ramidus is either com-
parable to female apes or more derived toward
Australopithecus (11) (Fig. 1 and figs. S12 and
S13). The upper canine (UC) is clearly derived
in Ar. ramidus, because it has a diamond-shaped
lateral crown profile with elevated and/or flar-
ing crown shoulders (n = 5 from Aramis and
n = 1 from Gona) [this study and (3, 4, 6)].
However, the lower canine (LC) retained much
more of the morphology of the female ape con-
dition (4, 5) (Fig. 1, figs. S11 to S13, and SOM
text S1). A hominid-like incisiform LC mor-
phology (high mesial shoulder, developed distal
crest terminating at a distinct distal tubercle) is
seen in some female apes (e.g., Ouranopithecus
and P. paniscus), whereas the LCs of Ar. kadabba
and Ar. ramidus tend to be conservative, exhibit-
ing a strong distolingual ridge and faint distal
crest, typical of the interlocking ape C/P3com-
plex (4) (Fig. 1 and SOM text S1).
The Ar. ramidus P3is represented by seven ob-
servable crowns, ranging from obliquely elongate
to transversely broad (1) (fig. S14). The Ar. ramidus
P3is relatively smaller than that of Pan and typ-
ically not as asymmetric or elongate in occlusal
view (figs. S15 and S16). In these respects, the
Ar. ramidus P3is comparable to those of Au.
anamensis and Au. afarensis. However, Ar.
ramidus is more primitive than Australopithe-
cus in retaining a proportionately higher P3
crown (fig. S16). It appears that there was a
decrease of P3size from the ancestral ape to
Ar. ramidus conditions, but this reduction was
greater in basal crown dimensions than in crown
height (SOM text S1).
In Ar. ramidus, the combined effect of (i) re-
duced canine size and projection and (ii) reduced
size and mesiobuccal extension of the P3results
in the absence of upper canine honing (defined
as distolingual wear of the UC against the mesio-
buccal P3face, cutting into the lingual UC crown
face and resulting in a sharpened distolabial enamel
edge). Instead, apical wear in Ar. ramidus com-
mences early and thereafter expands as wear
progresses. None of the known UCs or P3s ex-
hibits evidence of honing (fig. S14). However,
both upper and lower canines project beyond
the postcanine occlusal plane before heavy wear,
resulting in steep and beveled wear slopes, as
also seen in examples of Au. afarensis and Au.
anamensis (1, 4, 20).
Two Ar. ramidus specimens provide asso-
ciated maxillary and mandibular dentitions with
minimal canine wear. One is almost certainly
female (ARA-VP-6/500), and the other is a
probable male (ARA-VP-1/300) (see below).
Both individuals possess a UC with a shorter
crown height than the associated LC (>10%
difference in ARA-VP-1/300) (21). In contrast in
most anthropoid species, the UC is greater in
height than the LC (fig. S17), a condition ex-
aggerated in males of dimorphic species (over
50% in some papionins). Although less extreme
in extant great apes (22), the UC still exceeds
LC crown height by up to ~20% (fig. S18). In
modest samples of modern great ape canines
with little to no wear, we found no instances of
LC height exceeding that of the UC (25 males
and 27 females). This pattern of relative UC and
LC height in Ar. ramidus appears unique among
anthropoids and indicates differential reduction
Upper Canine Maximum Diameter
6 Ma hominids
Upper Canine Labial Crown Height
6 Ma hominids
Fig. 1. RepresentativeexamplesoftheAramisArdipithecusramidusdentition.(A)Occlusalviewmicro-CT–
based alignment of ARA-VP-1/300: top, maxillary dentition; bottom, mandibular dentition. The better-
preserved side was scanned andmirror-imagedto form these composites. (B) ARA-VP-1/300in buccal view:
top, right maxillary dentition (mirrored); bottom, left mandibular dentition. (C) Comparison of canine
P. troglodytes (cast), female P. troglodytes (cast), Ar. kadabba ASK-VP-3/400, Ar. ramidus ARA-VP-6/1, Au.
lower canines with hominid-likefeatures: left, P. paniscus(cast);right,OuranopithecusmacedoniensisRLP-55
(cast). The Ar. ramidus upper canine is highly derived, with a diamond-shaped crown with elevated crown
shoulders. The lower canine tends to retain aspects of primitive ape features. Further details are given in
the SOM figures and SOM text S1. (D) M1morphology (micro-CT–based renderings) showing relatively
little morphological variation among the Aramis individuals. Top row left, ARA-VP-1/300 (mirrored);right,
ARA-VP-1/1818. Middle row left, ARA-VP-1/3288; right, ARA-VP-6/500. Bottom row left, ARA-VP-6/502
(mirrored); right, KUS-VP-2/154. (E and F) Box plot of upper canine maximum diameter and labial height (in
mm). Ar. ramidus includes Aramis and published Gona materials (2). The ~6-million-year-old hominids are
represented by Ar. kadabba (ASK-VP-3/400) and O. tugenensis (BAR 1425'00) (7). Symbols give central 50%
range (box), range (vertical line) and outliers. See SOM figures and text S1 for additional plots and details.
VOL 3262 OCTOBER 2009
on October 12, 2009
of the UC in hominids. The UC < LC height
relation is retained in modern humans.
Morphological changes in the series Ar.
kadabba–Ar. ramidus–early Australopithecus
support the hypothesis of selection-induced UC
reduction. As detailed above, the UC is clearly
derived in Ar. ramidus, whereas the LC tends
to retain the primitive female apelike condition.
Au. anamensis, geologically younger than Ar.
ramidus but older than Au. afarensis, exhibits a
polymorphic condition represented by both prim-
itive and advanced LC morphologies (4, 20)
(SOM text S1). The more incisiform morphol-
ogy becomes universal in Au. afarensis and later
hominids. Furthermore, compared with both male
and female apes, Ar. ramidus exhibits a small
UC crown (both basal diameter and height) rela-
tive to apico-cervical root length, more so than
the LC (figs. S19 and S20). This observation
provides further support to the interpretation that
the UC crown was differentially reduced (SOM
A broader comparison of Ar. ramidus with
extant and Miocene apes illuminates aspects of
C/P3complex evolution. Compared with cerco-
pithecoids, hominoids tend to have smaller P3s
with less extensive honing (fig. S15). Compared
with other modern and Miocene apes, both spe-
cies of Pan appear to show P3reduction. The P3
of Ar. ramidus is even smaller, suggesting further
reduction of the C/P3complex from an ancestral
ape condition. At first sight, the comparatively
small P3size in Pan appears paradoxical, be-
cause among the modern great apes both male
and female P. troglodytes have relatively large
and tall canines (figs. S9 and S10 and SOM text
S1). However, this apparent paradox is removed
by a broader perspective on tooth and body size
proportions. Both Pan species share with atelines
and Presbytis (sensu stricto) small postcanine size
relative to body size (Fig. 2, figs. S21 and S22,
and SOM text S2), low postcanine dimorphism,
and low to moderate canine size dimorphism
(figs. S23 to S25). Conversely, papionins exhibit
the opposite condition: large postcanines, large
canines, and extreme dimorphism. We therefore
hypothesize that the basal Pan condition was
characterized by a somewhat reduced C/P3com-
plex as part of a generally small dentition relative
to body size and that the canines were second-
arily enhanced leading to modern P. troglodytes.
The ARA-VP-6/500 skeleton and sexual di-
morphism. Of the 21 individuals with canines,
ARA-VP-6/500 has UC and LC that are strik-
ingly small; its UC ranks either 12th or 13th (of
13), and its LC ranks seventh (of eight) in size
(table S6). However, postcranially, ARA-VP-6/
500 isa large individual with an estimated body
weight of ~50 kg (23). Was ARA-VP-6/500 a
small-canined male or a large-bodied female?
We began our evaluation of ARA-VP-6/500
(24) by estimating the degree of dimorphism in
the Ar. ramidus canine (SOM text S3). Even in
modern humans, the canine is metrically the most
dimorphic tooth. Mean basal crown diameter of
human male canines is about 4 to 9% larger than
that in females (table S5). Our analysis indicates
that Ar. ramidus was probably only marginally
more dimorphic than modern humans (tables S6
to S9 and SOM text S3), with a probable range of
10 to 15% dimorphism (in canine mean crown
diameter). This is substantially less dimorphic than
modern great apes, whose male canines (mean
crown diameter) are larger than those of females
by 19 to 47%.
On the basis of the above dimorphism esti-
mate, the probability of a male having canines
as small as those of ARA-VP-6/500 can be eval-
uated by bootstrapping (2). Assuming 12% di-
morphism in mean canine size (table S8), the
probability that ARA-VP-6/500 is a male is
<0.03 (if the UC is ranked 12th of 13) or <0.005
(if ranked 13th) (table S9 and SOM text S4). We
conclude that ARA-VP-6/500 is a large-bodied
female, a conclusion also corroborated by cranial
anatomy (25). This shows that skeletal size dimor-
phism in Ar. ramidus must have been slight (11),
as is the case in both species of Pan (26, 27).
The ARA-VP-6/500 skeleton and dimorphism
estimates allow us to place the Ar. ramidus den-
tition within a broader comparative framework.
Scaling analyses (2) show that the UC of Ar.
ramidus was relatively small in both sexes (fig.
S22 and SOM text S2). In particular, male UC
height of Ar. ramidus is estimated to be close to
that of female P. paniscus and Brachyteles and
to be much lower than that of male P. paniscus
(which has the least projecting male canine among
extant catarrhines) (Fig. 2).
Canine development and function. In cerco-
pithecoids with highly dimorphic canines, canine
eruption is typically delayed in males, beginning
after the age of eruption in females (28) and ap-
parently corresponding with species-specific pat-
terns of body size growth spurts (29–31). Once
male canine eruption is initiated, it then proceeds
at a higher rate than in females, but it can still last
for several years depending on species (31). As a
consequence, males attain full canine eruption as
they approach or achieve adult body size, both
of which are necessary for reproductive suc-
Sexually distinct patterns of canine eruption
in relation to body size growth have yet to be
well documented in modern great apes but ap-
pear to broadly share the cercopithecoid pattern
described above (28, 32–34). Initiation of canine
eruption in P. troglodytes differs by about 1.5 to
2 years between the sexes (35). In males of both
P. troglodytes and P. paniscus, full canine erup-
tion appears to coincide broadly with M3 erup-
tion (observations of skeletal materials), with
polymorphism in the eruption sequence of the
two teeth. By contrast in females of both spe-
cies, full canine eruption is attained before M3
Fig. 2. Size and scaling of the
Ardipithecus ramidus dentition.
Natural log-log scatter diagram
of relative upper canine height
(y axis) against relative post-
canine length (x axis): left, fe-
males; right, males. Both axes
represent size free variables
(residuals) derived from scaling
tooth size against body size
across a wide range of anthro-
poids (2). A value of zero rep-
resents the average female
catarrhine condition. Positive
and negative residuals repre-
sent relatively large and small
tooth sizes, respectively. The
diagonal line indicates the di-
rection of equivalent canine and postcanine proportions independent of size.
The five great ape taxa plotted are from left to right: P. paniscus, P. t. troglodytes,
P. t. schweinfurthi, Gorilla gorilla, and Pongo pygmaeus. Ar. ramidus is plotted
by using mean postcanine size and canine crown heights of probable female
(ARA-VP-6/500) and male (ARA-VP-1/300) individuals. A hypothetical female
body weight of 45 kg or 50 kg was used (right and left stars, respectively).
Ar. ramidus is shown to have small postcanine tooth sizes, similar to those of
Ateles, Presbytis sensu stricto, and Pan. Relative canine height of Ar. ramidus
is lower than that of the smallest-canined nonhuman anthropoids, P. paniscus
and Brachyteles arachnoides. See SOM text S2 for further details.
2 OCTOBER 2009 VOL 326
on October 12, 2009
The relative timing of canine eruption in Ar.
ramidus is revealed by two juveniles. The ARA-
VP-6/1 holotype, a probable male (table S6),
includes an unworn UC whose perikymata count
is 193, higher than that in Au. africanus/afarensis
(maximum 134, n = 4) (36) and lower than those
in small samples of female P. troglodytes and
Gorilla (minimum 204, n = 10) (37). The ARA-
VP-6/1 UC crown formation time was 4.29 or
4.82 years, depending on estimates of enamel
formation periodicity (fig. S26). This is a com-
paratively short formation time, around the mini-
mum reported for modern female apes (38).
The eruption pattern of a second individual,
ARA-VP-1/300, can be assessed from the pres-
ence or absence of wear facets and/or polish. The
ARA-VP-1/300 canines were just completing
eruption, its M2s were worn occlusally, and its
unerupted M3 crowns were barely complete
(Fig. 1 and fig. S27). Compared with extant apes,
both its UC and LC development are advanced
relative to M2 and M3 (fig. S28) (39).
The combined morphological and develop-
mental evidence suggests that selection for de-
layed canine eruption had been relaxed in Ar.
ramidus. We hypothesize that canine prominence
had ceased to function as an important visual sig-
nal in male competitive contexts.
Tooth size and diet. We consider relative in-
cisor and postcanine sizes to be potentially useful
in inferring dietary adaptations, although consist-
ent patterns across primates have not been ob-
tained (40). In particular, postcanine megadontia
has been considered a defining feature of Aus-
tralopithecus (41). We evaluated incisor and molar
sizes of Ar. ramidus in comparison to those of
Pan and Australopithecus. Among anthropoids,
Pan and Pongo are unique in having large in-
cisors relative to both postcanine and body size,
a condition not shared by Ar. ramidus (fig. S29).
This suggests that Ar. ramidus was not as inten-
sive a frugivore as are Pan and Pongo, incisor
length probably being functionally related to re-
moval of fruit exocarp (42) and/or feeding be-
havior such as wadging.
Although the M1 area, normalized by indi-
vidual postcranial metrics, lies well within the
range of extant chimpanzees, the total postcanine
area of ARA-VP-6/500 falls between Pongo and P.
troglodytes (Fig. 3). Ar. ramidus is not only less
megadont than Pongo and Au. afarensis but,
together with Pan, Ateles, and some Presbytis
species, lies at the small end of the range of
variation of large-bodied anthropoids (fig. S30).
The most megadont anthropoids include robust
Australopithecus, such as Au. boisei, as well as
papionins and Alouatta. Ouranopithecus was
probably as megadont as Australopithecus spe-
cies, whereas Dryopithecus and Pierolapithecus
probably had relative postcanine sizes closer to
Ar. ramidus and thus better approximate the
dentition–to–body size relationship of the last
common ancestor of humans and chimpanzees.
We conclude that Ar. ramidus was substantial-
ly less megadont than Australopithecus.
Molar structure and enamel thickness. Molar
structure, enamel thickness, and tooth wear further
illuminate dietary adaptation in Ar. ramidus. Com-
pared with the distinct occlusal structure of the
molars of each of the modern ape species (see
below), Ardipithecus occlusal morphology is more
generalized, with low, bunodont cusps and mod-
erate to strong basal crown flare. Such morphol-
ogy also characterizes Australopithecus as well
as a diversity of Miocene apes (43). Gorilla mo-
lars have much more salient occlusal topography
and enhanced shearing crests. Pan molars are
characterized by broad, capacious occlusal basins
flanked by moderately tall cusps, effective in crush-
ing relatively soft, fluidal mesocarp while retaining
the ability to process more fibrous herbaceous ma-
terials (Fig. 4) (44, 45). These features are ac-
centuated in Pan by the characteristically thin
enamel of its occlusal basin (45, 46).
To further elucidate molar structure and di-
etary adaptations of Ar. ramidus, particularly in
comparison with Pan and Australopithecus, we
used micro–computed tomography (micro-CT)
to study molar enamel thickness and underlying
crown structures (2). Although the weak contrast
of fossil enamel and dentin makes micro-CT–
based evaluations difficult, we were able to as-
sess several Ar. ramidus molars with this method.
These and analyses of CT sections and natural
fracture data (2) indicate that Ar. ramidus enamel
is considerably thinner than that of Australopith-
ecus but not as thin as in Pan [as originally
reported in (1)] (Fig. 4 and figs. S31 and S32).
Of particular importance is that Ar. ramidus
molars do not exhibit enamel distribution patterns
characteristic of P. troglodytes and P. paniscus.
Both Pan species have similar crown structure
and enamel distribution patterns (Fig. 4), although
P. paniscus molars exhibit a higher cuspal to-
pography, perhaps related to greater reliance on
fibrous food (46, 47). Ar. ramidus lacks the thin
occlusal fovea enamel of Pan and in this regard
is similar to both Australopithecus and Miocene
forms such as Dryopithecus (Fig. 4). The Pan
condition is most likely derived, probably as-
sociated with an increased reliance on higher-
canopy ripe fruit feeding.
Despite the generalized molar structure com-
mon to both Ar. ramidus and Australopithecus,
the adaptive difference between the two is ex-
pressed by enamel tissue volume, which we con-
sider to broadly track net resistance to abrasion.
Modern ape species exhibit a near-isometric re-
lation between molar durability (measured as
volume of enamel tissue available for wear per
unit occlusal area) and tooth size, despite diverse
dietary preferences and crown anatomy (Fig. 4).
Ar. ramidus falls near this isometric continuum,
but Australopithecus does not. Australopithe-
cus molars achieve greater functional durabil-
ity from increased enamel volume. Au. boisei
occupies an extreme position distant from the
modern ape baseline. Thus, both tooth size
and enamel thickness and volume suggest a
substantial adaptive shift from Ardipithecus to
This is further expressed in molar macro-
and microscopic wear patterns. In contrast to
Australopithecus, Ar. ramidus molars did not
wear flat but instead retained stronger bucco-
lingual wear slopes. The Aramis Ar. ramidus
dentition also exhibits consistently weak M1 to
M3 wear gradients (48). Microwear of the Ar.
ramidus molars tends to differ from that of Au.
afarensis, the latter characterized by a domi-
nance of buccolingually oriented scratches (49).
In contrast, the Ar. ramidus molars tend to ex-
hibit finer and more randomly oriented striae
(fig. S33). Collectively, the wear evidence sug-
gests that Ar. ramidus consumed a less abrasive
diet and engaged in less masticatory grinding
Fig. 3. Relative postcanine dental size in Ar. ramidus. Postcanine size is compared directly in reference
to associated postcranial elements; x axis is natural log of the size variable (body size proxy) of Lovejoy
et al. (23), derived from four metrics of the talus and five metrics of the capitate; y axis is natural log of
the square root of the sum of calculated areas (mesiodistal length multiplied by buccolingual breadth)
of lower M1(left) and lower P4to M3(right). A, Ar. ramidus ARA-VP-6/500; L, Au. afarensis A.L. 288-1;
c, Pan troglodytes troglodytes; g, Gorilla gorilla gorilla; o, Pongo pygmaeus (males blue, females red).
VOL 326 2 OCTOBER 2009
on October 12, 2009
Enamel thickness and phylogenetic implica-
tions. Since the initial description of Ar. ramidus
as a new species of Hominidae (1), its relatively
thin molar enamel has been a focus of atten-
tion. Some authors have suggested that its thin
enamel might be a shared derived feature with
Pan (7). The fuller study of molar enamel thick-
ness and patterns outlined above establishes the
following: (i) Although Ar. ramidus enamel is
thinner than that of Australopithecus, it is not as
thin as Pan’s; (ii) the thin enamel of Pan molars
can be considered a part of a structural adapta-
tion to ripe fruit frugivory (46) and therefore dif-
fers from the Ar. ramidus condition. Furthermore,
the distinct internal structure of Pan molars seems
lacking in Ar. kadabba, O. tugenensis, and S.
tchadensis (4, 8, 10). Hence, the Pan condition
is best considered derived relative to the an-
cestral and early hominid conditions.
Conclusions. Multiple lines of morphological
evidence suggest that Ar. ramidus was a general-
ized omnivore and frugivore that did not rely
heavily on either ripe fruits (as in Pan or Pongo),
fibrous plant foods (as in Gorilla), or hard and
Fig. 4. Enamel thickness and distribution patterns in Ar. ramidus. Left
panels: micro-CT–based visualizations of maxillary first molars in arbi-
trary size. (A) Outer enamel surface; (B) enamel thickness in absolute
thickness scale superimposed on topographic contours; (C) enamel thick-
ness in relative scale to facilitate comparison of pattern. The molars [labeled
in (A)] are as follows: 1 and 5, Au. africanus Sts 24 (mirrored) and Sts 57; 2,
Dryopithecus brancoi; 6, Ar. ramidus ARA-VP-1/3288; 3, Pan troglodytes; 4,
Pan paniscus; 7, Gorilla gorilla; 8, Pongo pygmaeus. The Pan species share
a broad occlusal basin and thin occlusal enamel. Both Ar. ramidus and D.
brancoi are thinner-enameled than Australopithecus but share with
Australopithecus a generalized distribution pattern. (D) Maximum lateral
enamel thickness, showing that Ar. ramidus enamel is thicker than those of
Pan and D. brancoi and thinner than that of Australopithecus species.
Horizontal line is median; box margins are central 50% range. (E) Ratio of
occlusal (volume/surface area) to lateral (average linear) enamel thick-
nesses, showing that Pan is unique in its distinctly thin occlusal enamel. (F)
Molar durability (enamel volume per unit occlusal view crown area) plotted
against projected occlusal view crown area. An isometric line (slope of 0.5)
is fitted through the centroid of the three measured Ar. ramidus molars. The
least squares regression (y = 0.418x− 1.806) of the combined modern ape
sample is also shown. This slope does not differ significantly from isometry.
Ar. ramidus and D. brancoi are close to, and Australopithecus species
considerably above, the regression line, indicating greater enamel volume
available for wear in Australopithecus molars. See (2) for further details.
2 OCTOBER 2009 VOL 326
on October 12, 2009
toughfooditems(asinPongoorAustralopithecus). Download full-text
Ar. ramidus also lacked adaptations to abrasive
feeding environments (unlike Australopithecus).
These inferences are corroborated by the isotopic
analysis of enamel, which indicates that Ar. ramidus
predominantly consumed (~85 to 90%) C3plant
sources in woodland habitats and small patches of
forest (50), thus differing from both savanna
woodland-dwelling chimpanzees (>90% C3) and
Australopithecus spp. (>30% C4) (51).
Conversely, extant Pan and Gorilla, each with
its distinctive dental morphology, are best con-
sidered derived in their dietary and dental adap-
tations. This is consistent with the Ar. ramidus
postcranial evidence and its interpretations (11, 23)
and strengthens the hypothesis that dental and
locomotor specializations evolved independent-
ly in each extant great ape genus. This implies
that considerable adaptive novelty was neces-
sary to escape extinction in the Late Miocene
forest and woodland environments.
These analyses also inform the social behav-
ior of Ar. ramidus and its ancestors. The dental
evidence leads to the hypothesis that the last
common ancestors of African apes and hominids
were characterized by relatively low levels of
canine, postcanine, and body size dimorphism.
These were probably the anatomical correlates of
comparatively weak amounts of male-male com-
petition, perhaps associated with male philopatry
and a tendency for male-female codominance as
seen in P. paniscus and ateline species (52, 53).
From this ancestral condition, we hypothesize
that the P. troglodytes lineage secondarily en-
hanced its canine weaponry in both sexes, where-
as a general size reduction of the dentition and
cranium (25) occurred in the P. paniscus lineage.
This suggests that the excessively aggressive in-
termale and intergroup behavior seen in modern
P. troglodytes is unique to that lineage and that
this derived condition compromises the living
chimpanzee as a behavioral model for the ances-
tral hominid condition. The same may be the case
with Gorilla, whose social system may be a part
of an adaptation involving large body size, a spe-
cialized diet, and marked sexual dimorphism.
In the hominid precursors of Ar. ramidus, the
predominant and cardinal evolutionary innova-
tions of the dentition were reduction of male
canine size and minimization of its visual prom-
inence. The Ar. ramidus dental evidence suggests
a less projecting and threatening male upper
canine. The fossils now available suggest that
male canine reduction was well underway by 6
million years ago and continued into the Pliocene.
of evolution before 6 million years ago.
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56. For funding, we thank NSF (grant nos. 8210897,
9318698, 9512534, 9632389, 9727519, 9729060,
9910344, and 0321893 HOMINID-RHOI) and the Japan
Society for the Promotion of Science (grant nos. 11640708,
11691176, 14540657, 16405016, 16770187, 17207017,
19207019, 19770215, and 21255005); the Ministry of
Tourism and Culture, the Authority for Research and
Conservation of the Cultural Heritage, and the National
Museum of Ethiopia for permissions and facilitation; the Afar
Regional Government, the Afar people of the Middle Awash,
and many other field workers for contributing directly to the
data; the institutions and staff of National Museum of
Ethiopia, National Museums of Kenya, Transvaal Museum
South Africa, Cleveland Museum of Natural History, Royal
Museum ofCentral Africa Tervuren, Naturalis Leiden,and the
Department of Zoology of the National Museum of Nature
and Science (Tokyo) for access to comparative materials;
H. Gilbert for graphics work on Fig. 1; D. DeGusta and
L. Hlusko for editorial assistance; R. Bernor, L. de Bonis,
M. Brunet, M. C. Dean, B. Engesser, F. Guy, E. Heizmann,
W. Liu, S. Moya-Sola, M. Plavcan, D. Reid, S. Semaw, and
J. F. Thackeray for cooperation with comparative data and
fossils; and T. Tanijiri, M. Chubachi, D. Kubo, S. Matsukawa,
M. Ozaki, H. Fukase,S. Mizushima, and A. Saso for analytical
and graphics assistance.
Supporting Online Material
Materials and Methods
Figs. S1 to S33
Tables S1 to S9
4 May 2009; accepted 18 August 2009
VOL 3262 OCTOBER 2009
on October 12, 2009