Brain enlargement and dental reduction were not
linked in hominin evolution
, Jeroen B. Smaers
, Ralph L. Holloway
, P. David Polly
, and Bernard A. Wood
Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052;
Department of Anthropology, Stony Brook University, Stony Brook, NY 11794;
Department of Anthropology, Columbia University, New York, NY 10027;
Department of Geological Sciences, Indiana University, Bloomington, IN 47405
Edited by Timothy D. Weaver, University of California, Davis, CA, and accepted by Editorial Board Member C. O. Lovejoy November 21, 2016 (received for
review May 31, 2016)
The large brain and small postcanine teeth of modern humans are
among our most distinctive features, and trends in their evolution are
well studied within the hominin clade. Classic accounts hypothesize
that larger brains and smaller teeth coevolved because behavioral
changes associated with increased brain size allowed a subsequent
dental reduction. However, recent studies have found mismatches
between trends in brain enlargement and posterior tooth size
reduction in some hominin species. We use a multiple-variance
Brownian motion approach in association with evolutionary simula-
tions to measure the tempo and mode of the evolution of endocranial
and dental size and shape within the hominin clade. We show that
hominin postcanine teeth have evolved at a relatively consistent
neutral rate, whereas brain size evolved at comparatively more
heterogeneous rates that cannot be explained by a neutral model,
with rapid pulses in the branches leading to later Homo species. Brain
reorganization shows evidence of elevated rates only much later in
hominin evolution, suggesting that fast-evolving traits such as the
acquisition of a globular shape may be the result of direct or indirect
selection for functional or structural traits typical of modern humans.
In comparison with other hominins, modern humans are char-
acterized by their large brain and small posterior teeth. These
traits are among our most distinctive features, and trends in their
evolution are well studied because of the phylogenetic and func-
tional implications of variation in dental and cerebral anatomy (1–3).
Brain expansion and postcanine reduction appear to follow parallel
trends during hominin evolution, and classic views consider that an
increase in brain size was linked to more complex behavior that
included the manufacture and use of stone tools, which allowed a
subsequent dental reduction. A shift toward a higher-quality diet
during the evolution of early Homo also has been related to brain
size increase and posterior tooth reduction (4, 5). However, it has
been suggested recently that brain expansion in early Homo,as
inferred from endocranial volume, substantially preceded dental
reduction (6). It also has been noted that early in the Neanderthal
lineage strong dental reduction preceded the additional brain ex-
pansionseeninthelater“classic”Neanderthals (7). The suggestion
that stone tool use and manufacture substantially predated the in-
crease in brain size observed in early Homo (8) adds further com-
plexity to this scenario.
Recent developments in ancestral state reconstruction (9, 10)
allow lineage-specific patterns of brain expansion and dental re-
duction to be quantified and compared. Unlike traditional ap-
proaches to ancestral state reconstruction that assume a neutral
evolutionary scenario, which is likely unrealistic in most cases, we
used a variable rate approach that estimates differences in evolu-
tionary rates across different branches of a given phylogeny. We
applied this approach to quantitative data on endocranial and
postcanine dental size and shape to develop a comprehensive sce-
nario of trends in endocranial and dental evolution across the
hominin clade (Fig. 1). Our assessment used a framework phylog-
eny based on widely agreed evolutionary relationships and on the
currently estimated first and last appearance dates for eight of the
most broadly accepted hominin species (Fig. 1 and Table S1)(11).
Amounts of change along each branch of the hominin phylogenetic
tree estimated through this variable-rate approach were compared
with the amount of change observed in evolutionary simulations
that used a constant-variance Brownian motion (BM) model (12) in
which traits evolve neutrally and at a constant rate without di-
rectional trends in any particular branch of the hominin phylogeny
(Materials and Methods).
Endocranial volume is the only trait whose evolution has given rise
to patterns of variation that are significantly different from those
obtained from neutral simulations (Fig. S1). The standard deviation
(SD) of the amounts of change per branch observed across the
phylogeny is significantly greater than the SDs obtained in constant-
rate simulations of the evolution of endocranial size (P=0.017).
This finding indicates that lineage-specific patterns of brain size
evolution are more heterogeneous than expected under a neutral
model and are unlikely to be explained by genetic drift. In addition,
the rates of change for endocranial and dental size and shape
through time differ substantially in different parts of the hominin
phylogeny (Figs. 2 and 3). These differences are robust to different
sample composition (P<0.001 for all pairwise comparisons of the
four traits) and to corrections for small sample size (Fig. S2), and
they are substantial for most branches of the hominin phylogeny
(Fig. S3 and Table S2). Although we use the term rate to make
reference to branch-specific amounts of change, it should be noted
that these values are not rates in the strict sense because they do not
represent amounts of change per unit of time but rather the ratio of
observed to simulated change per branch (Materials and Methods).
The evolution of the brain and of posterior teeth seem to follow
parallel trends in hominins. Larger brain size is associated with
reduced premolars and molars, but this association is not ob-
served in all hominin species. We have evaluated this association
in a quantitative way by measuring lineage-specific rates of
dental and cerebral evolution in the different branches of the
hominin evolutionary tree. Our results show that different species
evolved at different rates and that brain evolution in early Homo
was faster than dental evolution. This result points to different
ecological and behavioral factors influencing the evolution of
Author contributions: A.G.-R. designedresearch; A.G.-R. performed research; J.B.S. and P.D.P.
contrib uted new re agents/ analyti c tools; A .G.-R., R .L.H., an d B.A.W. c ollected data; A .G.-R.
analyzed data; and A.G.-R., J.B.S., R.L.H., P.D.P., and B.A.W. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. T.D.W. is a Guest Editor invited by the Editorial
To whom correspondence should be addressed. Email: email@example.com.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
www.pnas.org/cgi/doi/10.1073/pnas.1608798114 PNAS Early Edition
Our results show that sustained rapid evolution in brain size
started before the separation of Paranthropus and Homo and peaked
before the divergence between Homo erectus and the lineage leading
to Neanderthals and modern humans (Fig. 3A). That peak rate was
more than four times greater than that observed in simulated neutral
scenarios (Table S2). Additional rapid brain increase was observed
in the lineage immediately predating the Neanderthal–modern
human split, but this increase was only twice as fast as that observed
in a neutral scenario (Table S2). Other branches within the hominin
phylogeny show much slower rates of change than those observed
in a pure BM process, as is consistent with stabilizing selection
and constrained evolution. These estimates are similar to the ones
obtained using a more traditional approach to quantify branch-
specific change based on a generalized least squares (GLS) ancestral
reconstruction method (Table S3), which detects fast and slow
evolutionary rates in the same branches but with less extreme values.
Our results support the long-standing hypothesis that within the
hominin clade brain organization, as inferred from endocranial
shape, evolved independently of brain size (13). The ratios between
the change in endocranial shape measured along each branch and
those simulated using the BM model were all close to 1, leading to
a general scenario that is not statistically different from those ob-
served in constant-rate simulations (P=0.355) (Fig. S1). This result
indicates that endocranial shape evolved according to a quasi-
neutral model, as is consistent with a scenario in which genetic drift
is predominant (Fig. 3B). Rapid change, about twice that expected
under a BM model, was observed only along the branch leading to
modern humans from their last common ancestor with Neander-
thals (Table S2). This rapid evolutionary change is reflected in the
principal component analysis (PCA) of endocranial shape variation,
which shows that Homo sapiens strongly diverges from all other
species along the first principal component (PC1) (Fig. 2B). The
eigenvector of this axis shows that the dorsal arc connecting the
frontal and occipital poles is the only variable loading positively
on PC1, thus separating flatter from the more globular endocasts
that distinguish H.sapiens (Table S4)(14–16). Although frontal
changes also can influence this variable, researchers have suggested
that globularization is driven by upper parietal reorganization and
that this anatomical change can be associated with enhanced
visuospatial integration and memory in modern humans (17). The
comparatively fast evolution of the dorsal arc trait in the lineage
leading to H.sapiens is consistent with such a link between brain
anatomy and function, although it could be an indirect result of
selection on other craniofacial hard-tissue changes (18). If some
individuals that do not show a globular anatomy, such as Jebel
Irhoud 1 and 2 and Omo 2, are early members of H.sapiens (19),
then the endocranial anatomy typical of modern humans may have
evolved within the H.sapiens lineage.
Although there are differences in branch-specific evolutionary
rates for dental size, they are still within the expectations of a
constant-rate model (P=0.257) (Fig. S1). Sustained reduction in
the posterior dentition began in the branches antedating the origin
of the genus Homo and continued along the sequence of branches
leading to H.sapiens (Figs. 2Cand 3C). Dental reduction along all
these branches occurred at a rate that was approximately twice as
fast as expected under a neutral evolutionary model (Table S2).
Although the posterior teeth of Homo habilis and Australopithecus
afarensis are similar in size, a fast evolutionary rate is inferred
before the evolution of early Homo because this change is calcu-
lated with respect to the last common ancestor of Paranthropus
and Homo, and this last common ancestor is inferred to have had
larger posterior teeth than A.afarensis (Fig. 2C). A rapid rate of
dental reduction is observed in the lineage leading to modern hu-
mans but not in Neanderthals, resulting in the comparatively small
postcanine dentition of our species (Fig. 2C) (20). Contrary to our
results, a previous quantitative study of molar size found that molar
reduction observed in H.erectus, Neanderthals, and modern humans
occurred at a faster rate than in early Homo (21). That study,
however, used the area of the second molar (M2) as a proxy for
molar size without considering variation in molar proportions across
the molar row. Those proportions are known to change in the
genus Homo in concert with absolute molar size, thus making
M2s and M3s disproportionately small in species with overall
small dental size (22, 23). Reduction in the dentition was not
A. afarensis (2.9)
A. africanus (1.9)
P. robustus (0.9)
P. boisei (1.2)
H. habilis (1.7)
H. erectus (0.4)
H. neanderthalensis (0.03)
H. sapiens (0)
0 50000 100000 150000
0 50000 100000 150000
0 50000 100000 150000
Fig. 1. Methodological setup of the study. (A)The
hominin phylogeny used in our analyses indicating
the dates used for terminal species (blue) and nodes
(orange). (B) Linear metrics used in the study of
endocranial variation. FW, frontal width at Broca’s
cap; HLC, hemispheric length chord; MW, maximum
endocranial width; HLD, hemispheric length dorsal
arch; BB, basion–bregma distance; VT, vertex-lowest
temporal distance; BAC, biasterionic chord; MCW,
maximum cerebellar width. (C) Landmark and semi-
landmark datasets used in the study of postcanine
dental variation. Upper teeth are on the left, and
lower teeth are on the right. Postcanine teeth are
represented from top to bottom following the se-
quence P3, P4, M1, M2, and M3. (D) BM simulation
of the evolution of one trait (PC1 score) across the
hominin phylogeny. (Top) Green traces show evo-
lution along the A.afarensis and A.africanus
branches. (Middle) Simulated evolution along the
Paranthropus clade (orange and red traces) is added
to the above plot. (Bottom) Simulated evolution
along the Homo clade (blue and purple traces) is
added to the above graphs.
www.pnas.org/cgi/doi/10.1073/pnas.1608798114 Gómez-Robles et al.
the only rapidly evolving trend, because dental expansion occurred
at similarly high rates in the lineage leading to Paranthropus species
(Fig. 3Cand Table S2). Our data suggest that posterior tooth size in
Paranthropus robustus stabilized after its divergence from the Par-
anthropus boisei lineage, whereas P.boisei continued its dental
expansion but in a way consistent with quasi-neutral evolution.
Assuming that the Paranthropus clade is monophyletic, which is
the most common assumption even if other explanations are
possible (24), these observations suggest that the postcanine meg-
adontia of this genus is the result of long-term selective pressures
that predate the divergence of the Paranthropus species.
As with endocranial shape, the shape of tooth crowns also evolved
under a quasi-neutral model in which the evolutionary change along
each branch is close to and statistically indistinguishable from that
expected from a pure BM model (P=0.528) (Fig. 3Dand Fig.
S1). The difference that drives PC1 of dental crown shape is a
preferential reduction of the distal areas of premolars and mo-
lars in Neanderthals and modern humans (Fig. 2Dand Fig. S4).
The most rapid evolutionary change on the tree (1.5×greater
than expected in a neutral scenario) is associated with this
change along the branch antedating the separation of Nean-
derthals and modern humans (Table S2). Although the distal
regions of posterior teeth are strongly reduced in both species,
they have their own species-specific configurations. The char-
acteristically derived dentition of Neanderthals (25, 26) is reflec-
ted in the relatively fast rate of evolution of dental shape in this
lineage (Table S2).
Our results show clear differences in evolutionary patterns corre-
sponding to endocranial and dental size and shape during hominin
evolution. Endocranial volume evolved at relatively heterogeneous
rates that differ significantly from those observed under a constant-
rate neutral model (Fig. S1). Endocranial shape and dental size
and shape evolved at comparatively more uniform rates, with shape
traits evolving under a quasi-neutral model. Although the evolution
of these traits does not differ significantly from the expectations of
a constant-rate scenario, endocranial shape, dental size, and dental
shape still show significantly different evolutionary patterns. Given
similar genetic variance, drift is expected to affect all traits in the
same population equally (27). However, studies of brain anatomy
in chimpanzees and modern humans have shown that brain size
and brain organization have substantially different heritabilities
(28) representing the proportion of total phenotypic variance in a
population that has a genetic basis. Likewise, genetic variances of
the traits included in our study can plausibly be different and might
explain their different evolutionary behavior even if neither sig-
nificantly differs from neutrality.
The observed patterns of branch-specific variation are consistent
regardless of sample size and composition (Fig. S2), but they could
be affected by changes in the phylogenetic scenario. We have
chosen to deal with phylogenetic uncertainty by removing from our
analyses those species whose phylogenetic position is particularly
controversial, such as Homo ergaster,Homo antecessor,andHomo
3.8 3.6 3.4
-0.1 0.0 0.1
6.0 6.5 7.0 7.5
PC1 (42.6%)Flat Globular
PC2 (28.5%)PC2 (14.4%)
-0.1 0.0 0.1 -0.10
-0.1 0.0 0.1 -0.10
Fig. 2. Variation in endocranial and dental size and shape through time. (A) Change in endocranial size (logarithm of cranial capacity, LogCC) over time
showing extreme examples of variation. (B) PCA of endocranial shape variation over time (Left) and projection of PC1 and PC2 without time (Right). (C)
Change in dental size (logarithm of centroid size, LogCS) over time. (D) PCA of dental shape variation over time (Left) and without time (Right). In Aand B,the
small and flat endocasts are the A.afarensis Sts 5 and P.robustus SK 1585 specimens, respectively. The large, globular endocast is a recent H.sapiens. En-
docasts are in the same orientation as in Fig. 1. In Cand Ddental silhouettes representing large and distally expanded dentitions are based on the P.robustus
specimens SK 13/14 (upper teeth) and SK 23 (lower teeth). Small and distally reduced dentitions are based on a recent H.sapiens. The orientation of teeth is the
same as in Fig. 1. AFA, A. afarensis; AFR, A. africanus;BOI,P. boisei;ERE,H. erectus;HAB,H. habilis;NEA,H. neanderthalensis;ROB,P. robustus;SAP,H. sapiens.
Gómez-Robles et al. PNAS Early Edition
heidelbergensis. The resulting phylogenetic topology generally agrees
with most quantitative and qualitative assessment of hominin phy-
logenetic relationships (21, 29, 30), but new fossil findings resulting
in different relationships or branch lengths could potentially modify
some of our findings.
Our results, which indicate that the evolution of hominin brain
organization and brain size are decoupled, are consistent with
larger brain size being positively selected across the entire genus
Homo (31). Strong selection for larger brains has been linked to the
selective advantages associated with the enhanced computational
abilities of a larger neocortex with more neurons (32), but it also
can be linked to other neural modifications such as an increased
level of developmental plasticity arising from changes in the de-
velopmental patterns associated with larger brains (28, 33, 34).
Selection for certain aspects of brain organization, particularly in
the upper parietal reorganization that is arguably associated with
modern human-specific functional modifications (17), is confined
primarily to the branch leading directly to H.sapiens.Noother
aspects of brain reorganization as described by our set of variables
show evidence of fast evolution across the hominin clade. However,
many aspects of brain reorganization are not captured by those
endocranial metrics, particularly those related to finer-grained or-
ganization such as sulcal variation, brain asymmetries, and volu-
metric changes of certain areas, among others. The predominant
role of neutral mechanisms in the evolution of endocranial shape is
consistent with previously published work reporting a major role of
genetic drift in craniofacial evolution during the Australopithecus–
Homo transition (35, 36) and during the divergence of Neander-
thals and modern humans (37). Although our study focuses on
endocranial variation, our findings are consistent with a general
neutral scenario for the evolution of craniofacial shape in hominins.
The evolution of tooth crown size and shape is more closely
linked than the evolution of brain size and shape. The branch
antedating the separation of Neanderthals and modern humans
is characterized by strong reduction in overall dental size asso-
ciated with strong localized reduction of the distal areas of the
crown of all postcanine teeth (20, 26). However, this anatomical
change took place over a long period and does not show evi-
dence of particularly fast evolution indicating strong selection.
Although H.sapiens shows substantially faster reduction in dental
size than Neanderthals, the two species share similar evolutionary
rates of crown shape evolution, thus demonstrating that their
species-specific dental traits have been subject to similar selection
intensities. Our results show that crown shape evolution does not
depart radically from a BM model, and that postcanine dental
shape evolved at very similar rates within most branches of the
hominin phylogeny. This observation lends quantitative support to
dental shape as a useful proxy for reconstructing phylogenetic
relationships in hominin fossil species. Indeed, the utility of dental
shape for inferring evolutionary relationships is also supported by
recent DNA analyses that confirmed a relationship of Middle
Pleistocene European fossils to Neanderthals (38, 39) as initially
proposed using fossil evidence (7, 26).
If branch-specific trends are not quantified, the sustained brain
expansion found in some branches of the genus Homo may appear
to be associated with sustained dental reduction. However, our
results, which show that teeth and brains evolved at different rates
in different hominin species, suggest that the two trends were
decoupled. Our analysis shows that the apparent coupling of the
traits is confined to the three branches that connect the last
common ancestor of Paranthropus and Homo with the last com-
mon ancestor of Neanderthals and modern humans and that, even
in those cases, brain evolution occurred at faster rates than dental
evolution. We suggest that the context-specific ecological and
behavioral factors that influenced the evolution of teeth and
brains were not the same for the two morphological regions, nor
were the combinations of those factors the same at different stages
during hominin evolution.
Fig. 3. Evolution of endocranial and dental size and
shape. (A) Comparison of observed and simulated
branch-specific amounts of endocranial size varia-
tion. (B) Comparison of observed and simulated
amounts of endocranial shape variation. (C) Com-
parison of observed and simulated amounts of
dental size variation. (D) Comparison of observed
and simulated amounts of dental shape variation.
Red represents stasis along a given branch, and
green represents fast evolution along a given
branch, regardless of the directionality of change.
Branch thickness is proportional to the observed
amount of change along a given branch. In Aand C,
the plus sign represents size increase, the minus sign
represents size decrease along fast-evolving branches,
and tip and node size are proportional to endocranial
and dental size. In Band Dtheamountofchangeper
branch is based on shape distances that include all
dimensions of the morphospace, and node and tip
size are proportional to the amount of shape change
with respect to the ancestral-most node. The speci-
men examples are the same as in Fig. 2. Orientation of
endocasts and teeth is the same as in Figs. 1 and 2.
www.pnas.org/cgi/doi/10.1073/pnas.1608798114 Gómez-Robles et al.
Materials and Methods
Materials. We used four datasets to evaluate postcanine and endocranial size
and shape (Table S1 and Datasets S1–S4).The dataset for dental size and shape
was assembled by A.G.-R. as part of quantitative descriptions of occlusal
postcanine morphology (26, 40). Those samples were pruned to include only
species with relatively uncontroversial phylogenetic positions (see below) and
for which data on endocranial size and shape were also available. Endocranial
size was studied using species-specific endocranial volumes based on values
listed in ref. 41. This dataset does not reflect the reduction in endocranial
volume seen in recent H.sapiens. Mean cranial capacity in H.erectus was es-
timated from a subsample of Asian H.erectus with a geographical and chro-
nological origin similar to that of the dental sample (41). Endocranial shape
was evaluated in a smaller sample of complete or partial hominin endocasts.
Quantitative Description of Dental and Endocranial Size and Shape. Postcanine
dental shape was characterized with configurations of landmarks and sliding
semi-landmarks on the occlusal surface of tooth crowns (26, 40), and dental size
was quantified as the centroid size of those configurations (defined as the
square root of the sum of the squared distances between each landmark and
the center of gravity of the configuration). Procrustes superimposition (42) was
used to remove variation in position, size, and orientation, and species-specific
mean shapes were obtained by averaging Procrustes-superimposed coordi-
nates for each species (26). PCAs of Procrustes coordinates were used to obtain
the principal component (PC) scores used in subsequent analyses (12). When all
dimensions of shape variation are considered, as we did throughout all our
analyses, PC scores contain the same information as original variables but are
mathematically more convenient (12).
Tooth-specific size and shape data were pooled to analyze the complete
postcanine dentition. For shape analyses, landmark coordinates corresponding to
the 10 postcanine teeth (upper and lower premolars and molars) were subjected to
different Procrustes superimpositions and then were combined in the same PCAs.
Overall dental size was estimated by summing up centroid sizes across all the
postcanine teeth. Analyses of dental size therefore reflect i ncreases or decreases of
total postcanine occlusal areas but not changes in dental proportions among teeth.
Endocranial size was evaluated using species-specific mean endocranial
volumes. Endocranial shape was quantified using a set of classic linear metrics
measured by R.L.H. These metrics included eight variables used in other studies
of hominin endocranial variation (Fig. 1) (43). Size variation was removed from
these analyses by dividing each of these metrics by the cube root of cranial
capacity in each individual. Species-specific mean values for each of these
variables were subjected to PCA, and PC scores were used in ancestral recon-
structions of endocranial shape.
The robustness of our results to sample composition was evaluated by
bootstrapping the original samples 1,000 times and then recalculating species-
specific mean values and running all the analyses in bootstrapped samples.
Likewise, we assessed if the more heterogeneous evolutionary rates obtained for
endocranial evolution with respect to dental evolution result from differences in
sample size. Because some of the species in our samples are represented by only
three endocasts, we jackknifed all the samples to three individuals per species. This
down-sampling process was also repeated 1,000 times. Resampling rounds for
both approaches were performed independently for each tooth position because
most individuals in the dental samples do not preserve all postcanine teeth.
Hominin Phylogeny. Because our methodological approach requires the use of
an a priori phylogeny, we used only species whose phylogenetic positions are
relatively uncontroversial. Following the most widely accepted view, we con-
sidered Homo and Paranthropus as two monophyletic clades (29, but also see
ref. 44). Australopithecus africanus was considered to be a sister group to both
Paranthropus and Homo clades following ref. 45, although some analyses have
suggested other phylogenetic positions for this species (29), including a recent
classification as a sister group only to Homo (30). We chose not to use a pruned
version of the recently published Bayesian phylogeny proposed in ref. 30 for
two reasons. First, the supermatrix on which this analysis is based pools traits
and character states based on different studies, criteria, and scoring systems;
this approach may bias results by recovering nodes that have little or no support
or by failing to recover nodes that do have high support (46). Second, posterior
probabilities yielded by this analysis for most of the nodes included in our phy-
logeny are very low. Although they are unquestionably valuable for considering
alternative scenarios for hominin evolution, we believe that evolutionary rela-
tionships reflected in the summary of best trees presented in ref. 30 have weaker
support in general than the relationships used in our study.
Times of nodedivergence and ages ofterminal species followed ref. 11. Tips
were dated to the last appearance date (LAD) for each species listed in table 1
of ref. 11, whereas nodes were dated to the corresponding first appearance
date (FAD). Assuming that FADs and LADs observed in the fossil record are
unlikely to represent the actual FADs and LADs for each species, we used the
nonconservative version of these dates, which incorporate “the age, and the
publishederror of the age, of the nearest underlying dated horizon in the case
of the FAD, and the age, and the published error of the age, of the nearest
overlying dated horizon in the case of the LAD”(11, p. 55).
To account for some phylogenetic patterns that are not reflected in these
values, we dated the oldest ancestor in our tree to 4.4 Ma assuming an evolu-
tionary continuity between Australopithecus anamensis and A.afarensis (47),
which was dated to 2.9 Ma. The divergence between P.robustus and P.boisei
was established at 2.3 Ma. To account for the recent early Homo findings that
have pushed the FAD of the genus Homo back to at least 2.8 Ma (48), we set the
origin of this genus at 2.9 Ma. The divergence of the Paranthropus and Homo
clades was estimated at 3.5 Ma. Because our samples do not include late
H.erectus fossils, we dated H.erectus to 400 ka. An early Neanderthal status for
the Middle Pleistocene hominins from Sima de los Huesos is strongly supported
by both the paleontological and molecular evidence (7, 38, 49), so we established
the divergence date of Neanderthals and modern humans at 0.5 Ma, although
morphological studies suggest that an earlier divergence time for these species is
likely (26, 30). The averaging of data points at the LADs used for each species is
likely to provide conservative estimates of branch-specific amounts of change.
However, the use of data at time points that are closer to individual values
would artificially inflate the measured amounts of change per branch because of
the uncertainty regarding finer-grained population-specific dates and their
Ancestral Estimation. A multiple-variance Brownian motion (mvBM) frame-
work was used to estimate ancestral values in the hominin phylogeny (10).
Most ancestral estimation approaches assume a standard BM model of
character evolution (50). In standard BM the rate of evolution is assumed to
have a single mean and variance across all branches, and trait divergence is
proportional to the square root of time. Biologically, these assumptions
imply there is no sustained difference in the direction and rate of change
among the different lineages of the phylogeny. In many cases we expect this
assumption to be unrealistic because selection may be associated with en-
vironments that differ systematically between subclades or with particular
evolutionary or environmental events that occurred on only one branch of
the tree, thus producing different evolutionary rates and directions in dif-
ferent lineages. Our approach relaxes the pure BM model to capture dif-
ferent patterns of trait variation along each branch of the phylogeny (10).
Specifically, ancestral values were estimated using a two-step process. The
first step infers branch-specific patterns of change based on a model that
assumes that trait values for ancestral nodes are a compromise between
global and local effects. The baseline assumption that phylogenetic re-
latedness accurately reflects how traits evolve is hereby leveraged against
local deviations from this expectation. Specifically, a global estimate (a
weighted estimate based on the phylogenetic tree and the tip values) is
combined with a local estimate (accounting for information from a node’s
closest relatives without taking tree structure into account). Measures of the
rate of evolution then are estimated by dividing the squared trait difference
by the branch length for each ancestor–descendant pair. Rates hereby
represent the extent to which lineage-specific changes are found to align
with the baseline expectation that phylogenetic relatedness is an accurate
proxy for trait evolution. Each branch rate can be considered to be a point
estimate of the rate of change along each individual branch under an
In the second step, the branch lengths of the original phylogenetic tree are
rescaled according to the estimated rates of evolution. The model with the
rescaled branches is then parameterized using a standard BM model to produce
ancestral estimates. This procedure makes use of the analytical power of BM
estimation techniques while allowing local variation in evolutionary rates. This
method, which is explained in greater detail in ref. 10 and implemented in the R
package evomap (51), was applied to the hominin phylogeny and endocranial
and dental datasets.
Evolutionary Simulations. Results obtained through the previously described
process were compared with results obtained through a simulated pure BM
scenario. For size traits, e volutionary variation was simulated on log-transformed
size values, whereas for shape variation, PC scores were used (12). Simulations
were initiated at the ancestral-most values estimated through the mvBM ap-
proach. A per-generation variance rate (per-generation σ
) was estimated after
rescaling the hominin phylogeny to generations using a constant generation
time of 25 y (52). A GLS approach (53) implemented in the package Phyloge-
netics for Mathematica (54) was used to estimate a constant per-generation
variance rate for each variable (log-size and PC scores) based on available data.
Gómez-Robles et al. PNAS Early Edition
Using trait-specific constant per generation rates, evolutionary change was
simulated as a uni- or multidimensional random walk (12) on the hominin
phylogeny. Simulations were run 1,000 times, and the mean change be-
tween all ancestors and descendants was used as the expectation of the
amount of change if each branch had evolved neutrally under a pure BM
model. For endocranial and dental shape, this simulation was performed in
PC morphospace. Shape distances between ancestors and descendants were
calculated as the square root of the sum of the squared differences in all PC
scores between two given species, which is equivalent to the definition of
Procrustes distance for landmark data. For dental and endocranial size,
branch-specific amounts of change were calculated simply as the difference
between descendants and ancestors. Transformations between landmark
coordinates and PC morphospace were done with the package Geometric
Morphometrics for Mathematica (55).
The mvBM branch-specific changes were compared with the pure BM
changes as the mvBM/BM ratio. A value larger than 1 indicates that a given
branch has experienced more change than expected under a BM model (i.e.,
that branch has evolved faster thanexpected under a neutral model regardless
of the directionalityof the change). A value smallerthan 1 is indicative ofslower
evolution than expected under a neutral model, which in turn is indicative of
stabilizing selectionalong a certain branch.As we emphasized earlier, although
we refer to these values as rates, we recognize that they are not rates in the
strict sense but are the ratios of observed to simulated changes per branch.
These values were color coded and overlaid on the original phylogeny.
ACKNOWLEDGMENTS. Images of endocranial models were provided by José
Manuel de la Cuétara (H.sapiens endocast), Antoine Balzeau (P.robustus en-
docast), and Simon Neubauer (A.africanus endocast, which is based on a CT
scan from the University of Vienna database). We thank the following peo-
ple for discussion, facilitating access to material, constructive peer review,
or technical support: C. Sherwood, J. M. Bermúdez de Castro, J. L. Arsuaga,
E. Carbonell, O. Kullmer, B. Denkel, F. Schrenk, M. A. de Lumley, A. Vialet,
I. Tattersall, G. Sawyer, G. García, Y. Haile-Selassie, L. Jellema, M. Botella,
P. Gunz, and D. Sánchez-Martín.
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