No known hominin species matches the expected
dental morphology of the last common ancestor
of Neanderthals and modern humans
Aida Gómez-Roblesa,b,1, José María Bermúdez de Castroc, Juan-Luis Arsuagad, Eudald Carbonelle, and P. David Pollyf

aDepartment of Anthropology, The George Washington University, Washington, DC 20052; bKonrad Lorenz Institute for Evolution and Cognition Research,
A-3422 Altenberg, Austria; cCentro Nacional de Investigación sobre la Evolución Humana, 09002 Burgos, Spain; dCentro de Investigación Sobre la Evolución
y Comportamiento Humanos, Universidad Complutense de Madrid–Instituto de Salud Carlos III, 28029 Madrid, Spain; eInstitut Català de Paleoecologia
Humana i Evolució Social, Universitat Rovira i Virgili, 43007 Tarragona, Spain; and fDepartments of Geological Sciences, Biology, and Anthropology, Indiana
University, Bloomington,IN 47405

Edited by Jukka Jernvall, University of Helsinki, Helsinki, Finland, and accepted by the Editorial Board September 19, 2013 (received for review
February 9, 2013)

A central problem in paleoanthropology is the identity of the last
common ancestor of Neanderthals and modern humans ([N-MH]
LCA). Recently developed analytical techniques now allow this
problem to be addressed using a probabilistic morphological frame-
work. This study provides a quantitative reconstruction of the
expected dental morphology of the [N-MH]LCA and an assessment
of whether known fossil species are compatible with this ancestral
position. We show that no known fossil species is a suitable candi-
date for being the [N-MH]LCA and that all late Early and Middle
Pleistocene taxa from Europe have Neanderthal dental affinities,
pointing to the existence of a European clade originated around
1 Ma. These results are incongruent with younger molecular diver-
gence estimates and suggest at least one of the following must be
true: (i) European fossils and the [N-MH]LCA selectively retained
primitive dental traits; (ii) molecular estimates of the divergence
between Neanderthals and modern humans are underestimated;
or (iii) phenotypic divergence and speciation between both species
were decoupled such that phenotypic differentiation, at least in
dental morphology, predated speciation.

phylogeny | node reconstruction | geometric morphometrics |
morphospace | European Pleistocene

Uncertainty about ancestry is typical for many nodes of the
hominin phylogeny. Species are usually suggested as com-

mon ancestors based on their geography, chronology, and mor-
phological affinities (1–3), but these criteria can be unsatisfactory
for two fundamental reasons: first, the inherent incompleteness
of the hominin fossil record precludes a clear understanding of
the spatial and temporal range of variation of hominin species;
and second, comparative morphological analyses are frequently
descriptive in nature, making them difficult to evaluate objectively.
Fossil dental remains are central to our understanding of

hominin evolution due to their commonness in archaeological
and paleontological sites, their normally good state of preserva-
tion, and the minor influence that environmental factors—apart
from wear—have on their morphology during an individual’s life.
Teeth provide the most consistently complete representation of
the hominin fossil record and are thus fundamentally important
for assessing the plausibility of competing evolutionary scenarios
and avoiding inadvertently biased interpretations (Tables S1 and
S2). The combination of quantitative evolutionary theory, geo-
metric morphometrics, and dental anthropology provides a pow-
erful framework for reconstructing statistical expectations of the
morphology of unknown ancestors (ref. 4 but see also ref. 5) and
for making posterior comparisons with actual fossil remains.
The main aim of our study is to evaluate whether several known

candidate species have morphologies that are statistically consistent
with them being the last common ancestor of Neanderthals and
modern humans ([N-MH]LCA). To be a credible ancestor, a fossil
must have lived at the appropriate time and be statistically close to
the ancestral morphology, taking into account the uncertainty of the

ancestral reconstruction that arises from lability of the evolutionary
process and alternative hypotheses of the phylogeny on which it is
based. To implement this, we used geometric morphometric data to
reconstruct ancestral dental shapes and their confidence ellipsoids
using the phylogenetic generalized linear model (GLM) approach
(ref. 6; see Materials and Methods and SI Text for detailed explan-
ations). Ancestral reconstructions are based on an independent
phylogeny, ideally one built from nondental characters to avoid
circularity (Fig. 1 and Fig. S1). Note, however, that the phylogenetic
relationships of hominin species are vigorously debated and that
they are based mainly on craniodental traits, although not on the
quantitative dental shape traits we use (Figs. S2 and S3). The an-
cestral dental reconstructions were based only on species whose
phylogenetic position is relatively uncontroversial; species whose
phylogenetic position is contested were evaluated as potential
candidate ancestors for nodes of relevant age. We considered 12
phylogenetic topologies that are collectively representative of the
range of credible alternative hypotheses about hominin rela-
tionships (7). The ages of fossils and nodes were calibrated using
comprehensive reviews of the chronology, geographical location,
morphology and ecology of hominin species (8). In addition to
the [N-MH]LCA, we evaluated ancestor candidates at two other
important nodes of hominin phylogeny, the last common ances-
tor (LCA) of the genus Homo (excluding transitional hominins
such as Homo habilis and Homo rudolfensis) and the LCA of
Paranthropus and Homo, as controls for whether our statistical
framework is too strict. Our method is not intended to be

Significance

The identity of the last common ancestor of Neanderthals and
modern humans is a controversial issue. This debate has been
often addressed by means of descriptive analyses that are
difficult to test. Our primary aim is to put questions about
human evolution into a testable quantitative framework and
to offer an objective means to sort out apparently unsolvable
debates about hominin phylogeny. Our paper shows that no
known hominin species matches the expected morphology of
this common ancestor. Furthermore, we found that European
representatives of potential ancestral species have had af-
finities with Neanderthals for almost 1 My, thus supporting
a model of early divergence between Neanderthals and
modern humans.

Author contributions: A.G.-R. and P.D.P. designed research; A.G.-R., J.M.B.d.C., J.-L.A.,
E.C., and P.D.P. performed research; P.D.P. contributed new reagents/analytic tools;
A.G.-R. analyzed data; and A.G.-R. and P.D.P. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission. J.J. is a guest editor invited by the Editorial Board.
1To whom correspondence should be addressed. E-mail: aidagomezr@yahoo.es.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1302653110/-/DCSupplemental.

18196–18201 | PNAS | November 5, 2013 | vol. 110 | no. 45 www.pnas.org/cgi/doi/10.1073/pnas.1302653110

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a phylogenetic reconstruction technique, but a means to evaluate
compatibility of potential ancestral species within the framework
of established phylogenies.
Phylogenetic scenarios differed from one another in the

number and age of tip species and in the age of the nodes
(branch lengths; Fig. 1 and Fig. S1). European Middle Pleisto-
cene fossils were grouped into one of two operational taxonomic
units based on previously recognized morphological differences
(9): the Homo heidelbergensis group (represented in our study
by fossils from Arago Cave) and the Sima de los Huesos (SH)
group. SH hominins, unlike other European Middle Pleistocene
fossils (such as those from Arago, Mauer, and Petralona), are
widely considered to be an early chronospecies of classic Nean-
derthals (3, 9–11). However, the markedly derived dentitions of
SH hominins (12) appear to contradict their placement as an
early member of the Neanderthal lineage and their morphology
substantially influences the reconstruction of the [N-MH]LCA;
therefore, we evaluated SH both as a taxon on the phylogenetic
tree and as a potential candidate for the [N-MH]LCA. For the
former, SH was considered to be a node in the Neanderthal
lineage at 350 ka following ref. 13, an age that is less contro-
versial than a subsequent, older assessment of circa 600 ka (14).
We considered two alternative estimates for the divergence time
between Neanderthals and modern humans (1, 11). One scenario
dates this divergence to 450 ka based on molecular clock esti-
mates (11, 15); the other dates this divergence to 1 Ma based on
morphological affinities observed in the fossil record (see Results

and Discussion). We also considered two dates for Homo erectus,
1 Ma or 500 ka, to account for the different age estimates of key
Javanese (16) and Chinese fossils (17). We included H. erectus
as a potential candidate species for the [N-MH]LCA in some
phylogenetic scenarios. For each candidate, we evaluated its
compatibility with the statistical reconstruction of the morphol-
ogy of the LCA under each of the 12 phylogenetic scenarios.
Species were considered implausible as ancestors if one or more
of their teeth was incompatible with the expected ancestral
morphology under all 12 of the phylogenetic scenarios.

Results
The statistical reconstruction of the dental morphology of the
[N-MH]LCA is characterized by symmetric and lingually re-
duced upper premolars (P3 and P4) and by slightly asymmetric
lower premolars (P3 and P4). The upper first molar (M1) has
a slightly skewed morphology and the lower first molar (M1),
a Dryopithecus pattern (also called “Y5”) with five well-
developed main cusps. The Dryopithecus pattern is the shared
ancestral condition for all hominin lower molars, and consists of
a five-cusped molar in which the mesiolingual cusp (metaconid)
and the distobuccal cusp (hypoconid) are in contact and create
a Y-shape fissure pattern. The upper second molar (M2) of the
reconstructed common ancestor has a mildly reduced hypocone,
whereas the upper third molar (M3) has strong reduction such
that a high proportion of individuals are expected to lack the
distolingual cusp. Lower second molars (M2) of the recon-
structed [N-MH]LCA are expected to have marked reduction of
the fifth cusp and frequent occurrence of non-Y5 morphologies
(mainly cruciform patterns). The lower third molar (M3) of
the expected ancestral phenotype has five cusps that are not
arranged in a Y pattern, and a reduction of the lingual half of the
molar relative to its buccal half (Fig. 2). This reconstruction of
the dental morphology of the [N-MH]LCA is generally consis-
tent with all 12 phylogenies, one of which is shown in Fig. 2 (the
one that includes the SH group as a pre-Neanderthal population,
that uses the earlier date of 1 Ma for the [N-MH]LCA, and
which dates H. erectus to 1 Ma; Fig. 3 and Figs. S4 and S5 are
based on the same phylogeny).
Our results reveal that no known species of the relevant age

is statistically consistent with the expected morphology of the
[N-MH]LCA, even given the considerable uncertainty of the
reconstructed ancestral morphologies. Graphical reconstructions
of the nodes in dental morphospace are shown in Fig. 3 and Fig.
S4, along with confidence ellipsoids that show the associated
uncertainties that arise from the stochastic nature of the evolu-
tionary process. The size of each confidence ellipsoid is directly
related to the lengths of the branches connected to the node. At
least two postcanine teeth fall outside the 95% confidence
intervals of the [N-MH]LCA reconstruction for all candidate
species under all 12 phylogenetic scenarios (Table 1). Further-
more, taxa such as H. heidelbergensis have several postcanine
teeth that are morphologically consistent with the [N-MH]LCA
only in one or two phylogenetic scenarios (Table S3). The ad-
dition of other European fossils to the H. heidelbergensis sample,
such as those from Mauer and Petralona, could alter this result,
but this is unlikely because they are similar (not only in dental,
but also in cranial and mandibular morphology) to the Arago
specimens relative to other taxa in our analysis (2, 3, 9, 18). Our
results demonstrate that morphological evidence for any of these
taxa being the [N-MH]LCA is, at best, weak. For these species to
be credible ancestors, the age of the Neanderthal–modern hu-
man split would have to be radically different from the range we
considered or selection on the dentition would have to have
caused the ancestor to radically deviate from the expectations of
Brownian motion evolution. In addition to ruling out these
candidate species, our results indicate that all three European
candidate groups are statistically closer to the Neanderthal lin-
eage than to the modern human lineage (Table 2 and Table S4),
which suggests that European hominins have had significant
dental affinities with Neanderthals for almost 1 My (the oldest

Fig. 1. Phylogeny used for ancestral state reconstruction and candidate
species. Numbers in parentheses represent the averaged chronology of the
corresponding species (although see ref. 56); italic numbers represent branch
lengths in millions of years; bold gray numbers represent ages of nodes.
Branch lengths corresponding to a 1-Ma divergence between Neanderthals
and modern humans are represented to the left of the slashes and values
corresponding to a 0.45-Ma divergence to the right. H. erectus has been
dated to 1 Ma (values before the slash in the H. erectus branch) or to 0.5 Ma
(values after the slash). Candidate species are represented below the phy-
logenetic tree with bars showing their approximate temporal spans (black,
candidates for the [P-H]LCA; dark gray, candidates for the [H]LCA; light gray,
candidates for the [N-MH]LCA). H. erectus and the SH group have been in-
cluded in the framework phylogeny in four (H. erectus) and six (SH) phylo-
genetic scenarios (Fig. S1) and evaluated as candidate species in the
remaining scenarios. H. ergaster has been evaluated as a candidate species
for the [H]LCA and the [N-MH]LCA. H. habilis has been evaluated as a can-
didate for the [P-H]LCA and the [H]LCA. Vertical guides indicate the age of
the evaluated nodes. Fig. S1 shows individualized representations of the 12
phylogenetic topologies.

Gómez-Robles et al. PNAS | November 5, 2013 | vol. 110 | no. 45 | 18197

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species, Homo antecessor, has been dated to ca. 950 ka; ref. 19).
African Homo ergaster and Asian H. erectus do not share this
European affinity, but they have nearly equal dental affinities
with Neanderthals and with modern humans (Table 2 and Table
S4). H. ergaster was evaluated as a [N-MH]LCA candidate be-
cause it is the youngest African species in our sample, despite it
being considerably older than this ancestor is expected to be.
Interestingly, H. ergaster fits the expected ancestral phenotype
better than some of the younger candidate species (Table 1).
Asian H. erectus was also evaluated as an ancestral candidate
because the fossil specimens included in our study lived during
the right time interval (0.5–1 Ma), but it has generally a worse fit
with the [N-MH]LCA than H. ergaster.
Our method identified compatible candidates for other nodes

in the phylogeny (Fig. S5). Our data show that H. ergaster and,
especially, H. habilis fit the expected morphology of the LCA of
the genus Homo ([H]LCA) at all tooth positions in one or more
of the 12 phylogenies (Table 1 and Table S3). Similarly, both
Australopithecus afarensis and Australopithecus africanus fit the
expected morphology of the LCA of Paranthropus and Homo ([P-
H]LCA) at all tooth positions in most or all of the phylogenetic
scenarios (Table 1 and Table S3). Despite being age-in-
appropriate, we also evaluated H. habilis as a candidate for the
[P-H]LCA because of its suggested affinities with Australopithecus
species (20). Interestingly, it has even stronger compatibility with
the expected morphology of this ancestor than do A. afarensis and
A. africanus (Table 1 and Table S3). The fact that several can-
didates are compatible with deeper nodes is not surprising be-
cause the long branch lengths leading to older nodes result in
broader confidence ellipses than at shallower nodes with shorter
branches (21). Regardless of uncertainty, Procrustes distances

show that the fit between candidates and their corresponding
nodes is substantially better at the older nodes than at the [N-
MH]LCA (Table 1). The main exception is the SH group, which
has some teeth that are comparatively close to the [N-MH]LCA
in terms of Procrustes distances, but which is incompatible as an
ancestor because some of its teeth are strongly derived and have
a very low probability of conforming to the expected ancestral
morphology.

Discussion
Our results demonstrate that, even though there are plausible
candidate species for deep nodes of the hominin phylogeny (A.
afarensis, A. africanus, and H. habilis for the [P-H]LCA and H.
habilis and H. ergaster for the [H]LCA), we still do not have
a good fossil candidate for the phenotypic LCA of Neanderthals
and modern humans. This result is striking because confidence
intervals of ancestral reconstructions are very broad, which
means that existing candidates are very incompatible. Species

Fig. 2. Dental morphology of the [N-MH]LCA. Estimated ancestral mor-
phologies are represented as TPS-grids showing the deformation from the
base of the phylogeny into the estimated ancestral shape. Photographs
(with landmarks represented as blue points) show examples of typical
morphologies found in the Neanderthal lineage (NEA) and in the modern
human (H. sapiens) lineage (SAP). Mesial margins are represented to the left,
distal margins to the right, buccal margins to the top, and lingual margins to
the bottom of the figure. Not to scale.

B

A

Fig. 3. Projection of the simplified hominin phylogenetic tree (represented
by lines connecting terminal species and nodes) with terminal species (large
dark-gray filled circles), ancestor shapes (small light-gray filled circles) and
candidate species (open circles) into the upper and lower first molar mor-
phospaces. Confidence ellipses (95%) around the three nodes discussed in
the text are represented with the three ancestors located in their centers
(solid line, confidence ellipse of the [N-MH]LCA; dashed line, confidence el-
lipse of the [H]LCA; dotted line, confidence ellipse of the [P-H]LCA). (A)
Upper first molar morphospace. (B) Lower first molar morphospace. Plots
corresponding to premolars and second and third molars are provided in Fig.
S4. Note that confidence ellipses in these graphs correspond only to the first
and second principal components (PCs), whereas P values in Table 1 are based
on all of the PCs. Phylogeny: BOI, P. boisei; ERE, H. erectus; NEA, H. nean-
derthalensis; ROB, Paranthropus robustus; SAP, H. sapiens; SH, SH group.
Candidates: AFA, A. afarensis; AFR, A. africanus; ANT, H. antecessor; ERG, H.
ergaster; GEO, Homo georgicus; HAB, H. habilis; HEI, H. heidelbergensis.

18198 | www.pnas.org/cgi/doi/10.1073/pnas.1302653110 Gómez-Robles et al.

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falling outside the confidence intervals for a given node can be
excluded from ancestry with high confidence presuming the
model of Brownian motion evolution is applicable. The use of
several different phylogenetic topologies in our study makes the
rejection of these candidates even stronger.
Even though none of the candidate species we evaluated were

compatible with the [N-MH]LCA, note that our study did not
include African populations of H. heidelbergensis or African
specimens dated to ca. 1 Ma. These groups deserve scrutiny as
potential ancestors, especially because they lived at the right
time and their cranial morphological affinities are ambiguous (2,
18, 22–24). Middle Pleistocene fossils from Africa (sometimes
referred to as Homo rhodesiensis) have been considered by some
as part of the lineage leading to H. sapiens (22) and by others
as belonging to the ancestral species of Neanderthals and
modern humans (3, 18, 23, 24). African fossils dated to ca. 0.5–1
Ma thus merit continued study and are currently the most prom-
ising source of candidates for the [N-MH]LCA.
The lack of a plausible [N-MH]LCA candidate among Euro-

pean groups and their dental affinity with Neanderthals back to

1 Ma suggests three possible scenarios (covered in the next three
sections), which are not necessarily mutually exclusive.

Neanderthals and the [N-MH]LCA Could Be Primitive in Their Dental
Morphology. One possible explanation of our results is that the
constellation of characters shared by European Pleistocene fos-
sils represents the primitive condition for the clade Homo
neanderthalensis–H. sapiens and that the true ancestral pheno-
type was closer to the Neanderthal condition than expected
under a Brownian motion model. This scenario would require
relative stasis in the evolution of dental morphology in the Ne-
anderthal lineage and either neutral or directional evolution in
the H. sapiens lineage. If this were the case, our ancestral re-
construction method would fail to recover the correct mor-
phology because it assumes similar, nondirectional evolutionary
changes in the lineages stemming from a node and subtending it.
We have tested and rejected this possibility elsewhere (25), and
so consider this scenario unlikely. Whereas some authors have
suggested that Neanderthals are morphologically more primitive
than modern humans (26), quantitative analysis of evolutionary

Table 1. Procrustes distances between expected ancestral morphologies and candidate species

Procrustes distance* (P value)†

P3 P4 M1 M2 M3 P3 P4 M1 M2 M3

[N-MH]LCA
SH group 0.045

(<0.001)
0.027
(0.072)

0.024
(0.373)

0.034
(0.710)

0.049
(0.392)

0.051
(0.042)

0.042
(0.103)

0.023
(0.432)

0.031
(0.169)

0.044
(0.074)

H. heidelbergensis 0.046
(0.785)

0.061
(0.147)

0.052
(0.006)

0.072
(0.001)

0.059
(0.255)

0.057
(0.310)

0.036
(0.487)

0.025
(0.991)

0.034
(0.194)

0.042
(0.980)

H. antecessor 0.038
(0.234)

0.037
(0.280)

0.051
(0.001)

0.058
(0.001)

N/A 0.081
(0.036)

0.046
(0.259)

0.030
(0.934)

0.048
(0.016)

0.041
(0.360)

H. erectus 0.031
(0.999)

0.023
(0.805)

0.028
(0.867)

0.053
(0.015)

0.067
(0.030)

0.084
(0.039)

0.043
(0.622)

0.029
(0.733)

0.038
(0.628)

0.038
(0.678)

H. ergaster 0.051
(0.206)

0.044
(0.920)

0.053
(0.013)

0.077
(0.001)

N/A 0.061
(0.250)

0.032
(0.608)

0.038
(0.913)

0.034
(0.670)

0.042
(0.811)

[H]LCA
H. georgicus 0.061

(0.456)
0.028
(0.580)

0.050
(0.918)

0.049
(0.307)

0.091
(<0.001)

0.059
(0.009)

0.030
(0.988)

0.033
(0.983)

0.036
(0.955)

0.050
(0.583)

H. ergaster 0.044
(0.394)

0.040
(0.995)

0.050
(0.060)

0.060
(0.170)

N/A 0.057
(0.256)

0.035
(0.694)

0.035
(0.894)

0.034
(0.765)

0.037
(0.805)

H. habilis 0.041
(0.627)

0.037
(0.596)

0.026
(0.868)

0.032
(0.300)

0.039
(0.602)

0.036
(0.813)

0.046
(0.497)

0.021
(0.965)

0.030
(0.919)

0.034
(0.971)

[P-H]LCA
H. habilis 0.028

(0.847)
0.027
(0.944)

0.024
(0.948)

0.029
(0.751)

0.023
(0.953)

0.046
(0.569)

0.040
(0.724)

0.022
(0.990)

0.031
(0.965)

0.037
(0.947)

A. africanus 0.031
(0.970)

0.029
(0.647)

0.029
(0.732)

0.031
(0.934)

0.056
(0.410)

0.043
(0.932)

0.026
(0.992)

0.025
(0.925)

0.035
(0.745)

0.043
(0.573)

A. afarensis 0.041
(0.962)

0.033
(0.868)

0.030
(0.688)

0.055
(0.282)

0.049
(0.509)

0.055
(0.951)

0.031
(0.960)

0.037
(0.664)

0.035
(0.729)

0.037
(0.642)

Bold represents P < 0.05 in all phylogenetic scenarios (candidate species is incompatible with ancestry in the specified tooth). N/A, not applicable (no M3 of
H. antecessor and H. ergaster are included in the sample).
*Mean Procrustes distance obtained in the 12 evaluated phylogenetic scenarios.
†Highest P value observed in the 12 different phylogenetic scenarios. P values represent the probability that a fossil species falls within the expected
distribution of an ancestral node under the assumption of a Brownian motion model of evolution.

Table 2. Morphological affinities of candidate species with Neanderthals and with modern humans

Candidate P3 P4 M1 M2 M3 P3 P4 M1 M2 M3

SH group NEA NEA NEA — SAP NEA SAP NEA NEA NEA
H. heidelbergensis SAP NEA — NEA NEA SAP NEA NEA NEA NEA
H. antecessor NEA NEA NEA NEA N/A SAP NEA SAP NEA NEA
H. erectus SAP NEA SAP NEA NEA SAP NEA SAP SAP SAP
H. ergaster SAP NEA SAP NEA N/A SAP SAP SAP NEA NEA

Affinities based on Procrustes distances (Table S4). N/A, not applicable; NEA, higher affinity with Neanderthals; SAP, higher affinity
with modern humans; —, higher but not significant affinity with Neanderthals.

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patterns in these lineages are consistent with a Brownian process
of nonadaptive, neutral evolution in both dental (25) and cranial
features (27). Moreover, detailed, comprehensive evaluations of
postcanine dental morphology have revealed that several dental
traits shared by European late Early and Middle Pleistocene
populations and classic Neanderthals are, in fact, derived (28–31).
The suite of dental traits shared by European hominins sug-

gests that a separate European clade with Neanderthal affinities
existed since at least 1 Ma. This does not necessarily imply
a continuity between all European Pleistocene populations
during the last 1 My (32), but it points to all these taxa being part
of a Neanderthal phenotypic clade separate from the lineage
leading to modern humans. It has been suggested that this Eu-
ropean group could have been composed of successive migrant
populations who shared their common phenotypes via gene flow
(ref. 33, see also refs. 15 and 34), resulting in a lack of linearity in
the pattern of acquisition of Neanderthal traits (33). It is worth
noting that extensive hybridization would hamper ancestral re-
construction because the expected morphological differences
would be attenuated by gene flow between diverging populations.

Molecular Divergence Times May Be Underestimated. The paleon-
tological estimate of the divergence time between Neanderthals
and modern humans at ca. 1 Ma is substantially older than most
molecular estimates, which set the divergence at less than 500 ka
(11, 15). The divergence between Neanderthals and modern
humans has also been dated to 300–400 ka using neutrally
evolving cranial measurements (35), an estimate that is highly
dependent on assumptions and parameters that are not known
without error, but which is broadly consistent with the youngest
molecular clock estimates. In light of the young molecular and
cranial dates, several analyses have dismissed the early di-
vergence model of Neanderthal origins (1, 3, 11). However,
a late divergence model has been recently challenged on the
basis of slower mutation rates that result in earlier split times in
ape and human evolution (refs. 36–38 but see also refs. 39 and
40). Attempts to reconcile paleontological and molecular dates
have to face the fact that alternative molecular estimates for the
timing of the [N-MH]LCA vary considerably, with confidence
intervals ranging from 300 to 850 ka (11, 37). Our results are
however incongruous with even the lowest boundary of molecular
confidence intervals, and thus lend support to the early divergence
model and suggest that molecular estimates of divergence time
can be underestimated.

Phenotypic Divergence and Speciation Could Be Decoupled. A third
possible alternative that can conciliate molecular and paleonto-
logical observations is that phenotypic divergence in dental traits
between Neanderthals and modern humans significantly pre-
dated the completion of speciation. This scenario could explain
why someEuropean Pleistocene populations appear to be derived
in dental traits but still show primitive cranial and postcranial
features. Such mosaicism is particularly evident in H. antecessor’s
combination of some derived Neanderthal dental features (29–
31) and generally plesiomorphic nondental traits (at least for the
clade H. neanderthalensis-H. sapiens; refs. 41–43), and in SH’s
cranial morphology, which is transitional to the Neanderthal form
(10), combined with its strongly derived dental phenotype (12).
It is most likely that the large discrepancy between molecular

dates and phenotypic differentiation results from the wide con-
fidence intervals of the molecular estimates and from the un-
certainty associated with dating fossil materials. Regardless, our
results indicate that dental morphology developed derived fea-
tures as early as almost 1 Ma in the Neanderthalization process
(12), raising interesting questions about which evolutionary
forces may have caused this early dental differentiation with
respect to other traits and over what time interval occurred. The
evolutionary mechanisms behind this process are likely to consist
of a mosaic of random factors (such as genetic drift) and non-
random factors (such as lineage-specific patterns of environ-
mental selection and rates of evolution of different traits; ref. 44).

New paleontological, molecular, and quantitative phenotypic stud-
ies are needed to elucidate the exact nature of these factors.

Conclusions
Our study presents a statistical framework for addressing ques-
tions about ancestry and the relationships of particular fossils
that can serve as a model for making paleoanthropological hy-
potheses more testable. The quantitative approach we propose
offers an objective means to test hypotheses that capitalize on
the comparatively rich dental fossil record and address appar-
ently unresolvable debates about hominin phylogeny. The same
approach can be applied to other skeletal parts via 2D and 3D
quantifications of morphology, and it can be extended to in-
clude models of evolution other than Brownian motion pro-
cesses should there be evidence that they are appropriate. Our
approach thus provides a promising and extensible statistical
context for evaluating fossil remains of uncertain phylogenetic
position.

Materials and Methods
Materials. Our study analyzed the morphology of 1,200 hominin teeth rep-
resenting their 10 postcanine tooth positions (upper and lower premolars and
molars) from 13 different species/morphotypes (Tables S1 and S2). We chose
to split controversial named taxa for which all teeth are represented in our
samples to evaluate their ancestral status independently on their own
merits, but we lumped taxa when their dentitions were incompletely rep-
resented so as to provide more statistical power (e.g., Paranthropus aethio-
picuswas included in Paranthropus boisei and H. rudolfensis in H. habilis). The
only exceptions were H. ergaster and H. antecessor, which were retained as
separate candidate species despite their lack of M3 due to their strong can-
didacy as [N-MH]LCA. Although other taxonomic arrangements are plausible
(e.g., merging H. erectus, H. ergaster, and Dmanisi fossils under H. erectus
sensu lato), the purpose of our study is not to address taxonomic questions,
but to evaluate the plausibility that previously recognized taxa occupy
ancestral positions. In this regard, the most informative approach is a de-
tailed evaluation of morphologically, geographically, and chronologically
cohesive groups.

Geometric Morphometrics. Dental morphology was quantified using 2D
landmarks and sliding semilandmarks (45) digitized from photographs of the
occlusal surface of premolars and molars. Depending on the tooth, 4–8
landmarks and 30–40 semilandmarks were used (Fig. S2 and S3). Coordinates
were digitized using tpsDig2 software (46). Orientation of dental specimens
was standardized such that the occlusal surface was parallel to the lens of
the camera. Unworn and moderately worn teeth were included in our
evaluation, whereas severely worn teeth were excluded. A generalized
Procrustes analysis (47) and a principal components analysis (48) were carried
out using the mean configurations of the species (Dataset S1) to provide
shape variables. Ancestral state calculations were carried out on these var-
iables in the principal components space (Fig. 3 and Fig. S4) using all prin-
cipal components (5).

Ancestral State Reconstruction. The GLM method for estimating ancestral
traits (6, 49, 50) was used, implemented in Mathematica by one of us (51).
As is standard practice (52), our implementation of ancestral state recon-
struction assumes that the traits are evolving under a Brownian motion
model of the sort that results either from genetic drift or from selection
whose direction and magnitude varies randomly through time and across
space. Our previous study indicated that hominin dental evolution is con-
sistent with a Brownian motion model, although considerable stabilizing
selection has been identified in first molars and slight directional trends in
lower third premolars and upper third molars (25). Estimates of ancestral
states are not badly affected by stabilizing processes, only by long-term
unidirectional selection that occurs in parallel in different lineages (21, 53).

Ancestral node reconstruction identifies the single most likely ancestral
condition and a multivariate confidence ellipsoid (95%) containing other
plausible but less probable ancestral phenotypes (6, 50, 54). The likelihood
distribution of the ellipsoids was used to calculate the probability that fossils of
appropriate age could feasibly occupy those nodes (SI Text).

The reconstructed ancestral shape variables were converted back into
landmark configurations (55), after which the Procrustes distances of can-
didate species to the expected ancestor were calculated. Procrustes distance
is a measure of shape difference between superimposed conformations of

18200 | www.pnas.org/cgi/doi/10.1073/pnas.1302653110 Gómez-Robles et al.

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http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302653110/-/DCSupplemental/pnas.201302653SI.pdf?targetid=nameddest=ST1
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302653110/-/DCSupplemental/pnas.201302653SI.pdf?targetid=nameddest=ST2
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302653110/-/DCSupplemental/pnas.201302653SI.pdf?targetid=nameddest=SF2
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302653110/-/DCSupplemental/pnas.201302653SI.pdf?targetid=nameddest=SF3
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302653110/-/DCSupplemental/sd01.txt
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302653110/-/DCSupplemental/pnas.201302653SI.pdf?targetid=nameddest=SF4
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302653110/-/DCSupplemental/pnas.201302653SI.pdf?targetid=nameddest=STXT
www.pnas.org/cgi/doi/10.1073/pnas.1302653110


landmarks calculated as the square root of the sum of the squared differences
between the positions of homologous landmarks. The species that falls
within the confidence ellipsoid and has the smallest Procrustes distance to
the hypothetical ancestor can be considered the best candidate to occupy
the ancestral position. Procrustes distance was also used to calculate the
affinity of candidate species with Neanderthals and modern humans taking
into account the phylogenetic topology (SI Text).

ACKNOWLEDGMENTS.We thank EmíliaMartins, James Rohlf, Michelle Lawing,
Bernard Wood, Asier Gómez-Olivencia, and David Sánchez-Martín for dis-
cussion on several aspects of the manuscript. We also thank the editor and

three anonymous reviewers for their help in improving our manuscript. Ac-
cess to fossil specimens was made possible by O. Kullmer, B. Denkel, and
F. Schrenk (Senckenberg Institute); D. Lordkipanidze, A. Vekua, and G. Kiladze
(Georgian National Museum); H. de Lumley, M. A. de Lumley, and A. Vialet
(Institut de Paléontologie Humaine); P. Mennecier (Musée de l’Homme);
I. Tattersall, G. Sawyer, and G. García (American Museum of Natural History);
L. Jellema and J. Haile-Selassie (Cleveland Museum of Natural History); and
M. Botella (Laboratory of Physical Anthropology, University of Granada). This
workwas partially supported by funding by the Spanish Ministry of Science and
Innovation (Project CGL2009-12703-C03-01-02-03). Fieldwork at Atapuerca is
supported by the Consejería de Cultura y Turismo (Junta de Castilla y León)
and the Fundación Atapuerca.

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