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Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 145:231–246 (2011)
Assessing Endocranial Variations in Great Apes and
Humans Using 3D Data From Virtual Endocasts
Thibaut Bienvenu,1,2* Franck Guy,1 Walter Coudyzer,3 Emmanuel Gilissen,4,5,6
Georges Roualdès,7 Patrick Vignaud,1 and Michel Brunet1,2
1
Institut International de Paléoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironnements (iPHEP),
CNRS/Université de Poitiers, 86022 Poitiers, France
2
Collège de France, Chaire de Paléontologie humaine, 75231 Paris Cedex 05, France
3
Department of Radiology, University Hospitals Leuven, B-3000 Leuven, Belgium
4
Department of African Zoology, Royal Museum for Central Africa, B-3080 Tervuren, Belgium
5
Université Libre de Bruxelles, Laboratory of Histology and Neuropathology, B-1070 Brussels, Belgium
6
Department of Anthropology, University of Arkansas, Fayetteville, AR 72701
7
CHU La Milétrie, Service de Neurochirurgie, 86021 Poitiers, France
KEY WORDS
brain; endocast; comparative anatomy; evolution; hominoids
ABSTRACT
Modern humans are characterized by
their large, complex, and specialized brain. Human brain
evolution can be addressed through direct evidence
provided by fossil hominid endocasts (i.e. paleoneurology), or through indirect evidence of extant species comparative neurology. Here we use the second approach,
providing an extant comparative framework for hominid
paleoneurological studies. We explore endocranial size
and shape differences among great apes and humans, as
well as between sexes. We virtually extracted 72 endocasts, sampling all extant great ape species and modern
humans, and digitized 37 landmarks on each for 3D
generalized Procrustes analysis. All species can be differentiated by their endocranial shape. Among great apes,
endocranial shapes vary from short (orangutans) to long
(gorillas), perhaps in relation to different facial orientations. Endocranial shape differences among African
Modern humans are characterized by their large, complex, and specialized brain. Understanding the timing
and processes of brain evolution in hominids is an important objective of paleoanthropological studies. We use the
term hominid here to denote all taxa that are more closely
related to humans (Homo sapiens) than to chimpanzees
(Pan troglodytes) and bonobos (Pan paniscus). Human
brain evolution can be addressed in two different ways:
direct and indirect. The direct approach consists of studying fossil hominid endocranial casts (or endocasts), as
these are the only remnants of hominid ancestors’ brains.
This direct method is the ‘‘bread and butter’’ of paleoneurology (Falk, 2007). The other way to address human brain
evolution is to study and compare brains of our closest
extant relatives, the great apes, with those of humans.
We use the term apes referring to hominoids excluding
humans; great apes are chimpanzees, bonobos, gorillas,
and orangutans; African apes are chimpanzees, bonobos,
and gorillas. Such comparative neurological data constitute the indirect evidence of human brain evolution.
Endocasts constitute the only direct way to access
brain morphology when soft tissues are not available, for
example in fossil specimens. However, endocasts are
only an estimate of brain anatomy, as the brain surface
is separated from the internal bony table by the three
meningeal layers, containing cerebrospinal fluid and
blood vessels. Endocasts, thus, provide additional inforC 2011
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WILEY-LISS, INC.
apes are partly allometric. Major endocranial traits distinguishing humans from great apes are endocranial
globularity, reflecting neurological reorganization, and
features linked to structural responses to posture and
bipedal locomotion. Human endocasts are also characterized by posterior location of foramina rotunda relative to
optic canals, which could be correlated to lesser subnasal
prognathism compared to living great apes. Species with
larger brains (gorillas and humans) display greater
sexual dimorphism in endocranial size, while sexual
dimorphism in endocranial shape is restricted to gorillas,
differences between males and females being at least
partly due to allometry. Our study of endocranial variations in extant great apes and humans provides a new
comparative dataset for studies of fossil hominid endocasts. Am J Phys Anthropol 145:231–246, 2011. V 2011
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Wiley-Liss, Inc.
mation concerning brain vascularization that isolated
brains do not display. In this article, we use the terms
brain and endocast interchangeably to refer to our work
that deals exclusively with casts of the braincase.
Many previous studies concerning fossil hominid endocasts relate to endocranial volume, which provides an estimate of brain size (Conroy et al., 1998, 2000a,b). According
to Falk (2007) and Falk et al. (2009), the notion that brain
size suddenly began to increase with the evolution of the
genus Homo around 2 Ma needs reevaluation. Indeed,
Additional Supporting Information may be found in the online
version of this article.
Grant sponsor: Agence Nationale de la Recherche; Grant number:
ANR-09-BLAN-0238; Grant sponsor: Allocation de Recherche of the
French Ministère de l’Enseignement Supérieur et de la Recherche.
*Correspondence to: Thibaut Bienvenu, iPHEP, 40 Avenue du
Recteur Pineau, F-86022 Poitiers Cedex, France.
E-mail: thibaut.bienvenu@univ-poitiers.fr
Received 15 July 2010; accepted 13 December 2010
DOI 10.1002/ajpa.21488
Published online 1 March 2011 in Wiley Online Library
(wileyonlinelibrary.com).
232
T. BIENVENU ET AL.
with the exclusion of Paranthropus specimens, which may
not be directly ancestral to humans (González-José et al.,
2008), and the inclusion of ‘‘transitional’’ specimens from
Dmanisi (Gabunia et al., 2000; Vekua et al., 2002), brain
size appears to increase from before 3 Ma, in gracile
australopithecines (Falk, 2007; Falk et al., 2009). Brain
size relative to body size (or relative brain size) is often
expressed as an encephalization quotient, which is the
ratio of actual brain size of any given taxon or specimen on
the brain size predicted for a baseline animal of equivalent
body size. Encephalization quotients depend on the database used to derive the basic brain/body allometric equations (Holloway et al., 2004a). Encephalization quotients
reported below are derived from an ape-based regression.
Two important fossil skeletons provide data that enable
the assessment of encephalization quotients. The encephalization quotient of Lucy AL 288-1 (Australopithecus
afarensis, 3.2 Ma, Ethiopia) is estimated to be one—there
are not enough cranial remains of Lucy to measure cranial
capacity, but Holloway et al. (2004a) estimate it between
375 and 400 cm3, based on the size of the occipital portion—i.e., its brain size is similar to that predicted for an
ape of similar body size. The skeleton from Nariokotome
KNM-WT 15000 (Homo erectus, 1.5 Ma, Kenya) has an
encephalization quotient of two, while modern humans
have encephalization quotients of three. Therefore, relative brain size also increased from 3 Ma until today.
The second important issue concerning fossil hominid
endocasts relates to their shape, as it can provide information pertaining to the level of neurological reorganization. Shapes of fossil and extant hominid endocasts
have been analyzed with traditional morphometrics
(Neubauer et al., 2004; Falk et al., 2005; Falk and
Clarke, 2007; Falk et al., 2007) and 2D or 3D geometric
morphometrics (Bruner et al., 2003; Bruner, 2004, 2008;
Bruner and Ripani, 2008; Bastir et al., 2008; Neubauer
et al., 2009). Among reorganizational changes that
occurred during hominid evolution, the most often cited
are 1) expansion of parietal association cortex, concomitant to a reduction of primary visual cortex, resulting in
a posteriorly located lunate sulcus, 2) widening of the
prefrontal portion of frontal lobes, and 3) development
of cerebral asymmetries (Broca’s cap and petalias)
(Holloway et al., 2004a; Falk et al., 2009).
Much debate has centered on brain size versus neurological reorganization, and which came first (Holloway
et al., 2001, 2004b). The description of Homo floresiensis
(Brown et al., 2004) and analysis of a virtual endocast of
the type specimen LB1 (Falk et al., 2005, 2007) sheds
even more light on this ‘‘falsely perceived dichotomy’’
(Gould, 2001). Despite LB1 having an ape-sized brain
and an encephalization quotient of 1, its brain shows
many features of neurological reorganization (Falk et al.,
2009) consistent with the higher cognitive abilities that
have been attributed to Homo floresiensis (Brown et al.,
2004; Morwood et al., 2004). Whether reorganization
occurred in big- or small-brained ancestors of LB1
remains a matter of debate. However, the findings associated with LB1 provide significant evidence that
encephalization cannot be interpreted as an index of
some general intelligence (Preuss, 2001). There is a general trend of increasing encephalization and increasing
intelligence during hominid evolution, but brain size
alone is not a good predictor variable for intelligence.
Rather, LB1 extends considerably the realm of possible
combinations of brain size and neurological reorganization in fossil hominids (Falk et al., 2009).
American Journal of Physical Anthropology
Studies aiming to reconstruct human brain evolution
through the indirect evidence of comparative neurological
data focus on the differences between human and other
primate brains (e.g., Rilling and Insel, 1999). Living
great apes, especially African apes, have often been viewed
as convenient proxies to infer brain morphology of early
hominids as they share similar endocranial volumes.
Comparative anatomical studies can be performed from
cytoarchitectural (Brodmann, 1909; Preuss, 2001) to gross
anatomical scales of analysis (Semendeferi et al., 1997;
Semendeferi and Damasio, 2000). More recently, functional
brain processing has been explored through functional
magnetic resonance imaging (fMRI), allowing for the
assessment of the relationships between structure and
function (e.g., Biswal et al., 2010).
Comparative studies have shown that human brains,
along with being threefold larger, are not simply allometrically scaled versions of ape brains, and have, for example, an overall larger proportion of neocortex (Rilling,
2006). Contrary to the widespread thought, human brains
do not have larger frontal lobes than expected for an ape
brain of human size (Semendeferi et al., 1997; Semendeferi and Damasio, 2000). Rather, human frontal lobes are
characterized by differences in individual cortical areas
and a richer interconnectivity (Semendeferi et al., 2002),
demonstrated by an increase in prefrontal white matter
volume (Schoenemann et al., 2005). In addition, human
brains are more lateralized than those of great apes,
reflecting hemispheric specializations. Other studies have
shown that asymmetries are also present in great ape
brains, whether in areas implicated in language in
humans (Gannon et al., 1998; Cantalupo and Hopkins,
2001) or in the petalial pattern (relative projection of
frontal lobes and occipital lobes, correlated to handedness
in humans) (Holloway and Coste-Lareymondie, 1982;
Balzeau and Gilissen, 2010).
Some studies have concentrated on the description of
local shape variations among great apes, such as sulcal
(Connolly, 1950) or meningeal arterial pattern (Falk,
1993). However, most studies to date have neglected
global shape differences among great ape brains. Holloway (1981) was the first to quantitatively address overall
endocranial shape variation among extant great apes. He
observed global differences for the whole extant sample
but did not explore the differences among species.
Actual brain anatomy cannot be analyzed in fossil
specimens, but endocranial shape provides evidence in
addition to endocranial size. A few previous analyses of
endocranial shape have used geometric morphometrics.
Bruner (2004, 2008) compares the 2D lateral projections
of endocasts of extant and fossil humans. Three-dimensional endocranial morphologies have also been analyzed
through geometric morphometrics in modern and fossil
humans (Bruner et al., 2003; Bruner and Ripani, 2008;
Bastir et al., 2008; Neubauer et al., 2009). Before analyzing
endocranial shape in fossils, it is important to understand
the variation of endocranial shape in living primates.
Here we report the first global 3D geometric morphometric
analysis carried out on endocasts of all extant great ape
species and humans. Landmark coordinate analyses are
used to quantify and describe the morphological variation
among a set of specimens. Patterns of variation in endocranial size and shape among extant great ape species and
humans are explored, as well as patterns of variation
related to sexual dimorphism. In doing so, this study provides a comparative framework for future analyses of fossil
endocasts.
233
HOMINOID ENDOCRANIAL 3D GEOMETRIC MORPHOMETRICS
MATERIALS AND METHODS
Sample
The study was conducted on 72 extant cranial specimens, comprising 14 orangutans (Pongo pygmaeus), 16
gorillas (Gorilla gorilla), 16 chimpanzees (Pan troglodytes),
10 bonobos (Pan paniscus), and 16 modern humans (Homo
sapiens) (Table 1). All specimens are adults (third molars
fully erupted) and males and females are equally represented in each species. Modern human specimens are from
Europe (11), Greenland (two), Patagonia (one), Tierra
del Fuego (one), and Africa (one). Specimens are from
Musée Royal de l’Afrique Centrale of Tervuren (Belgium),
Anthropologisches Institut und Museum of Zürich (Switzerland), Natural History Museum of London (United
Kingdom), and Staatssammlung für Anthropologie und
Paläoanatomie München of Munich (Germany).
Data acquisition
Each cranium was scanned using a medical computerized tomography (CT) scanner, with a pixel size and a slice
thickness adjusted according to specimen cranial size.
Pixel size ranged from 0.30 (bonobos) to 0.70 mm (gorillas,
humans) and slice thickness from 0.30 (bonobos) to
1.0 mm (humans). Depending on their repository location,
specimens were scanned either in the Department of
Radiology in Universitair Ziekenhuis (UZ) in Leuven
(Belgium), in Kantonsspital in Winterthur (Switzerland),
in Hammersmith Hospital in London (United Kingdom),
or in the medical practice of Dr. Wuttge and colleagues in
Munich (Germany).
Data processing
Two methods were used to extract virtual endocasts
from CT scanned crania (Supp. Info. Figs. S1 and S2).
The first method is a semi-automated segmentation
using Avizo 6.0 software (Visualization Sciences Group).
On a coronal CT slice, the endocranial cavity was
roughly delineated manually by selecting also a bit of
surrounding bone (about 10 pixels). This selection was
propagated to adjacent slices using Snakes algorithm
without extrapolation (filter which fits the contour of a
selection to the regions with a high contrast) (Supp. Info.
Fig. S1). Gray values corresponding to bone were
removed from the selection by threshold segmentation
on the complete image stack. Manual corrections were
made where the endocast did not fit the inner table of
TABLE 2. Endocranial volumes (cm3) of five virtual endocasts
produced by both methods
TABLE 1. Extant sample
Species
Males
Females
Total
Species
First method
Second method
% difference
Pongo pygmaeus
Gorilla gorilla
Pan troglodytes
Pan paniscus
Homo sapiens
Total
7
7
8
4
9
35
7
9
8
6
7
37
14
16
16
10
16
72
P. pygmaeus
G. gorilla
P. troglodytes
P. paniscus
H. sapiens
464
410
282
352
1285
460
405
278
346
1275
0.9
1.4
1.4
1.7
0.8
Percentages of difference in endocranial volume are indicated.
Fig. 1. Right lateral view and ventral view (anterior at top) of an endocast of a female Homo sapiens produced by the second
method of extraction (consisting in a segmentation of the bone, followed by a removal of the outer surface and a filling of the basicranial foramina), gray level-coded to show the surface distance with the endocast produced by the first method of segmentation of
the endocranial cavity. Gray level map is coded from 0 to 1 mm. The distance between the two surfaces is greatest at foramina
because it corresponds to zones either manually segmented on the coronal slices (first method), or manually cut in the 3D surface
(second method).
American Journal of Physical Anthropology
234
T. BIENVENU ET AL.
TABLE 3. Landmarks digitized on virtual endocasts of all
specimens
Number
1,
3,
5,
7,
9
2
4
6
8
10
11
12
13
14
15
16
17, 18
19, 20
21,
23
24,
26,
28,
30,
32,
22
25
27
29
31
33
34, 35
36, 37
Landmark
Frontal pole
Occipital pole
Temporal polea
Cerebellar poleb
Anterior end of olfactory bulb (cribriform plate)
in the sagittal plane 5 foramen caecum
Posterior end of olfactory bulb (cribriform plate)
in the sagittal plane 5 anterior sphenoid spine
Posteriormost point of anterior cranial fossa in
the sagittal plane on limbus sphenoidalis
Sella
Dorsum sellae
Endobasion
Endopisthion
Internal occipital protuberancec 5 torcular herophili
Sylvian fissure: point at which the posterior border
of the anterior cranial fossa fuses with the
endocranial lateral walld
Pyramidal root 5 maximum curvature point
between transverse and petrous curve
Pyramidal apex
Endovertex
Optic canal, inferior border
Foramen rotundum, inferior border
Foramen ovale, posterior border
Internal acoustic meatus, inferior border
Posteriormost point on jugular foramen,
i.e., anteriormost point of sigmoid sinus
Maximum cerebral width
Maximum cerebellar width, sigmoid sinuses included
Landmarks 9–16 and 23 are located on the midline, the remainder are bilateral landmarks (right, left).
a
Temporal pole is defined as anteriormost point on temporal lobe
(Falk et al., 2007) and not as point of maximum curvature of the
temporal lobe (Bruner, 2004).
b
Cerebellar pole is the posteriormost point on cerebellar lobe.
c
If the protuberance is too flat, the landmark is located at the
point most representative of the interhemispheric and cerebrocerebellar separation (Bruner and Ripani, 2008).
d
Bruner and Ripani (2008).
bone, for example at foramina or the cribriform plate.
Finally, a surface of the endocast was computed from the
segmentation data object, yielding a 3D closed object.
A second method of virtual extraction was also used.
The cranium was automatically segmented by setting a
gray value range for the bone on all the coronal slices. A
blocking transverse section was set to separate the vault
and the basicranium. Gray value range was set more
conservative (wider range) for the basicranium than for
the vault, as basicranial bone is often very thin and we
aimed to avoid many manual corrections. Cavities inside
the bone, like paranasal sinuses or mastoid pneumatization, were automatically integrated within the bone. A
3D surface of cranial bone was computed. This surface
was then processed by using Geomagic Studio 11 software
(Geomagic). The outer surface of the cranium was
removed. The remaining inner surface of bone was kept,
thus giving a 3D surface of the endocast. Contrary to endocast extraction methods described by Falk et al. (2007) and
Neubauer et al. (2009), the internal braincase is closed at
foramina after surface extraction of the virtual endocast is
performed (Supp. Info. Fig. S2). Foramina are closed near
the remaining endocranial surface. Therefore they do not
contribute significantly to endocranial volume.
American Journal of Physical Anthropology
Both procedures were compared for five specimens,
one of each sampled extant species. No significant differences were observed, either in cranial capacity or in
endocranial shape and details (Table 2, Fig. 1). Moreover, no significant differences in endocranial volume or
shape were found between five human endocasts
extracted by our methods and by that of Neubauer et al.
(2009). Differences in cranial capacity between our first
and second method (always \2% of total volume) are
mainly due to differences of segmentation at the level of
foramina (Fig. 1). Initially, the first method was used.
Then it was replaced by the faster second method once
we determined that both methods give similar results.
Geometric morphometric analysis and statistical
analyses
Thirty-seven 3D landmarks were identified and their
locations recorded from the endocranial surfaces with
Landmark 3.6 software (Wiley et al., 2007) (Table 3,
Fig. 2). Endocast orientation may influence the position
of some landmarks and has been the cause of many
discussions (Falk, 1986; Holloway and Kimbel, 1986;
Holloway and Shapiro, 1992; Falk et al., 1994). Here we
start by placing frontal poles and occipital poles, defined
respectively as the frontal and occipital ends of the maximal length of each cerebral hemisphere (Connolly, 1950).
These poles define the conventional horizontal plane for
orienting endocasts (Holloway and Shapiro, 1992; Falk
et al., 1994), and subsequent landmarks (e.g., temporal
poles, cerebellar poles, and endovertex) are placed
according to this plane, which is equivalent to Frankfurt
horizontal plane for skull orientation, but not parallel
with it (Falk et al., 1994).
To test landmark repeatability, five specimens (one
of each species) were sampled twice. We estimated
intraobserver error by subtracting the coordinates of a
particular landmark from the coordinates of the same
landmark collected during another digitization, following
the approach outlined by Corner et al. (1992), since the
coordinate system does not change between two repeated
measurements of one individual when using CT scans
(von Cramon-Taubadel et al., 2007). This enables to calculate localized error to each landmark as the square
root of the sum of the squared differences between corresponding coordinates. Error local to each landmark is
then averaged across specimens. In addition, Procrustes
distances (see below details concerning Procrustes analysis) between repeated measurements of the same individual were compared with Procrustes distances between
different individuals, and an unweighted pair group
method with arithmetic (UPGMA) mean analysis
was performed using the Procrustes distances between
specimens.
Generalized Procrustes analysis (GPA) was performed
on the 3D configurations using Morphologika 2.5 software
(O’Higgins and Jones, 2006), landmark configurations
being scaled to unit centroid size, translated, and rotated,
minimizing the sum of squared landmark deviations from
the sample mean. Geometric morphometric methods offer
many benefits (Rohlf and Slice, 1990; Bookstein, 1991;
Dryden and Mardia, 1998), including the possibility to
treat size and shape separately and to analyze morphologies as a whole and not only trait by trait.
Statistical analyses were performed using Statistica
7.1 software (StatSoft). An analysis of variance (ANOVA)
was performed on endocranial volumes to test for differ-
235
HOMINOID ENDOCRANIAL 3D GEOMETRIC MORPHOMETRICS
Fig. 2. Landmarks used in the Procrustes superimposition (right lateral view and ventral view). Landmarks are displayed on a
male Pan paniscus endocast. See Table 3 for numbers correspondence.
ences among species and between sexes (acceptable Type
I error rate is set at 0.05). While centroid size is an
appropriate measure of size in most geometric morphometric analyses, in our application centroid size as
computed from 37 landmarks captures only a part of
endocranial size. Consequently, we use cranial capacity
as a preferred measure of size in our application.
Endocranial volume is better suited for comparison with
literature. Moreover, endocranial volume and centroid
size are highly correlated (R2 5 0.95, P \ 0.05) (Supp.
Info. Fig. S3). The Bonferroni post hoc test was used
to assess pairwise species differences and intraspecific
sexual differences in endocranial volume. In this test,
adjustment is performed by dividing the Type I error
rate by the number of tests (Zelditch et al., 2004).
A principal component analysis (PCA) based on variance–covariance matrix was performed using Procrustes
shape coordinates, yielding new variables (principal components or PCs) that are linear combinations of the original ones and independent of each other. The scree test
was used to determine which PCs were significant. The
scree test, first proposed by Cattell (1966), is done by
plotting principal components versus their percentage of
total variance explained and retaining only components
with percentages above a threshold where the decrease
of percentages graphically appears to level off. To better
describe shape changes associated with each significant
PC, the influence of any single landmark on an eigenvector
was computed as the square root of the sum of the squared
coordinate loadings for that landmark (Baab and McNulty,
2009).
To test for endocranial shape differences between taxa
or sexes, a multivariate analysis of variance (MANOVA)
was performed on significant PC scores. Pairwise species
differences and species-specific sex differences were tested
along each principal axis, using the Bonferroni post hoc
test.
Static allometry was studied by regressing (least
squares regressions) significant PC scores on log endocranial volume and testing for significance of squared
correlation coefficients.
TABLE 4. Mean distances (mm) between corresponding
landmarks of five virtual endocasts digitized twice
Landmark
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
Average
Mean 6 s.d.
2.71
2.32
1.57
1.61
2.04
1.66
1.41
2.28
0.53
0.63
0.58
1.38
0.59
1.57
1.65
2.42
1.99
2.21
2.48
2.06
1.05
1.84
0.94
0.89
1.24
0.56
0.82
0.97
0.80
1.13
1.27
1.68
1.26
1.05
0.41
0.56
0.44
1.37
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
2.50
1.90
1.01
0.54
0.94
1.35
0.89
2.21
0.43
0.36
0.37
1.02
0.66
1.79
1.55
1.64
1.25
1.88
1.96
1.54
0.60
1.71
0.37
0.45
0.67
0.29
0.57
0.49
0.46
0.29
0.23
0.95
0.80
0.98
0.27
0.64
0.18
1.30
Distances greater than 2.00 mm are italicized. See Table 3 and
Figure 2 for landmarks identification.
American Journal of Physical Anthropology
236
T. BIENVENU ET AL.
TABLE 5. Endocranial volumes (cm3)
Species
Sex
P. pygmaeus
M
F
Both
M
F
Both
M
F
Both
M
F
Both
M
F
Both
G. gorilla
P. troglodytes
P. paniscus
H. sapiens
This study,
mean 6 s.d. (n)
406.1
345.0
375.6
540.9
451.2
490.4
418.3
366.9
392.6
341.4
345.1
343.6
1399.5
1253.3
1335.6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
45.5 (7)
24.1 (7)
47.2 (14)
41.7 (7)
32.6 (9)
58.1 (16)
29.9 (8)
47.1 (8)
46.4 (16)
37.4 (4)
24.7 (6)
28.4 (10)
128.0 (9)
56.6 (7)
125.0 (16)
Isler et al. (2008),
mean 6 s.d. (n)a
422.1
338.5
383.5
523.2
459.2
500.5
386.2
350.5
367.6
356.3
326.2
344.3
6
6
6
6
6
6
6
6
6
6
6
6
37.9
29.5
54.0
49.9
32.6
54.0
42.9
30.0
40.7
16.3
36.0
28.7
(57)
(49)
(106)
(40)
(22)
(62)
(55)
(60)
(115)
(6)
(4)
(10)
Holloway (1981),
min–max (n)
Beals et al.
(1984)
Falk et al.
(2005)
Suwa et al.
(2009)b
375
422–615 (16)
490
375c
385–449 (15)
412.4
375.9
357.7
344.4
327–439 (16)
1166–1659 (13)
1349
1350
a
Calculated from their Appendix 2 listing individual data and considering only one species for Pongo (i.e., clustering Pongo pygmaeus and Pongo abelii in the same species), and one species for Gorilla (i.e., clustering Gorilla beringei and Gorilla gorilla in the
same species).
b
After Fenart and Deblock (1973) and Cramer (1977).
c
Falk and Clarke (2007) report a mean cranial capacity for adult chimpanzees of 390 cm3 (after Ashton and Spence, 1958).
Finally, phenetic affinities derived from endocranial
shape data were examined and compared to extant hominoid phylogeny (Goodman et al., 1994; Ruvolo et al.,
1994; Ruvolo, 1997). For this purpose, we computed a dendrogram via a UPGMA of Procrustes distances between
specimens.
RESULTS
Intraobserver error
The average distance between two corresponding landmarks is 1.37 mm (Table 4). Endocranial poles and notably
frontal poles (landmarks 1 and 2), internal occipital protuberance (landmark 16), sylvian fissures (landmarks 17
and 18), and pyramidal roots (landmarks 19 and 20) are
more prone to error. Within each species, the Procrustes
distance between repeated measurements is inferior to the
Procrustes distances between different individuals. In
the UPGMA analysis using the Procrustes distances, the
resampled individuals cluster together, suggesting that
they are more similar to each other than to any other
individual in the sample. All these data indicate an acceptable level of error of landmark repeatability and a low
within-observer error.
Endocranial volume
Means and standard deviations of the cranial capacities for each species are listed in Table 5. Our results
are consistent with previous literature. Notably, our
endocranial volumes are nearly identical to the ones
presented in Falk et al. (2005) (Pongo pygmaeus, Gorilla
gorilla), Falk and Clarke (2007) (Pan troglodytes), and
Isler et al. (2008) (Pan paniscus). The main difference
between our estimates of endocranial volumes and those
provided in previous studies concerns the mean volume
of male bonobos, which is lower than the mean volume
of female bonobos in our sample. This difference is probably due to the limited number of individuals (n 5 4 for
male bonobos).
Differences in endocranial volume between species are
statistically significant (F[4,62] 5 759.9, P \ 0.05), as well
American Journal of Physical Anthropology
Fig. 3. Scree plot. Significant PCs are PC1-2.
as differences between sexes (F[1,62] 5 23.6, P \ 0.05)
and species-sex interaction (F[4,62] 5 2.79, P \ 0.05).
Bonferroni test shows significant differences for each
species pairwise comparison, except for Pongo pygmaeus
versus Pan troglodytes, Pongo pygmaeus versus Pan
paniscus, and Pan troglodytes versus Pan paniscus.
Differences between males and females are only significant in humans. Dimorphism approaches statistical significance in gorillas and a larger sample would probably
show significant differences in endocranial volume
between male and female gorillas. As species-sex interaction is significant, species with larger brains (humans
and gorillas) show greater dimorphism than species with
smaller ones (orangutans, chimpanzees, and bonobos).
Endocranial shape
In our PCA of endocranial shape, only PC1-2 are significant according to the scree test (Fig. 3), representing
55.8% of total variance. Plot of PC1-2 specimen scores are
HOMINOID ENDOCRANIAL 3D GEOMETRIC MORPHOMETRICS
237
Fig. 4. PC1 (39.5% of variance) versus PC2 (16.3% of variance). Triangles pointing downward represent Pan paniscus, triangles
pointing upward Pan troglodytes, circles Gorilla gorilla, diamonds Pongo pygmaeus, and squares Homo sapiens. Solid symbols represent males and open symbols females. Frames represent extreme morphologies. See Figure 2 for frame orientation and landmarks
identification. Isolated points in lateral view are foramina.
presented in Figure 4. PC3 and PC4 are not significant
but provide additional information for the comparison of
species (Supporting Information). Plots of PC1 versus
PC3 and PC4 are displayed in Supp. Info. Figure S4.
Depending on their species, specimens are differently
distributed in PC1-2 shape space (Fig. 4). The first principal
component mostly separates great apes (lower scores) from
humans (higher scores). African apes are also segregated
along PC1, from gorillas with lower scores to bonobos with
higher scores, while orangutans have PC1 scores which
overlap those of gorillas and chimpanzees. Along PC2, gorillas display the lowest scores and orangutans the highest
scores, while chimpanzees, bonobos, and humans have
intermediate PC scores.
The weightings of landmarks on each significant PC
are presented in Table 6 and are helpful in interpreting
the wireframes presented in Figure 4. Specimens scoring
higher on PC1 (39.5% of variance) differ from lower
scoring individuals in having brains with a more globular shape overall (i.e., they are relatively taller and
broader), greater basicranial flexion and shorter basicranium (pattern drawn by foramina compressed anteroposteriorly, but also mediolaterally), more anterior and
horizontally oriented foramen magnum, greater posterior
projection of the occipital lobes and cerebellar poles more
medially positioned (making posterior endocranial morphology more pointed). The olfactory bulb is also longer
and more posteriorly positioned, protruding less anteriorly relative to the frontal poles which are located more
anteroinferiorly. Pyramids are less obliquely oriented
anteriorly and the region between endopisthion and the
internal occipital protuberance is more anteroinferiorly
angled rather than being more vertical.
The second principal component (16.3% of variance)
primarily describes the transition from long and narrow
to short and wide brains. In specimens scoring higher on
PC2, the foramen magnum becomes more oblique
through a great elevation of endopisthion (highest loading on PC2, Table 6). The frontal poles and olfactory
bulb get further apart. The posterior point of anterior
fossa and optic canals become more posteriorly located
than foramina rotunda.
In PC1-2 shape space, differences in endocranial shape
among species and between sexes are statistically significant (Wilk’s kspecies effect 5 0.007, F[8, 122] 5 172.4, P \
0.05; Wilk’s ksex effect 5 0.821, F[2, 61] 5 6.66, P \ 0.05).
MANOVA does not reveal a significant species-sex interaction in endocranial shape in PC1-2 shape space (Wilk’s
ksex*species 5 0.814, F[8, 122] 5 1.65, P 5 0.12). Along PC1,
Bonferroni test shows significant differences for each
species pairwise comparison. Along PC2, differences are
significant for each species pairwise comparison, except
for Pan troglodytes versus Pan paniscus and Pan troglodytes versus Homo sapiens.
American Journal of Physical Anthropology
238
T. BIENVENU ET AL.
TABLE 6. Loadings of landmarks on each significant
eigenvector
Landmark
PC1
PC2
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
0.28
0.29
0.15
0.16
0.09
0.10
0.15
0.14
0.11
0.27
0.13
0.13
0.15
0.25
0.36
0.08
0.19
0.18
0.08
0.09
0.09
0.08
0.26
0.11
0.11
0.14
0.13
0.10
0.09
0.11
0.11
0.20
0.19
0.11
0.12
0.08
0.07
0.26
0.25
0.12
0.12
0.13
0.15
0.10
0.11
0.23
0.14
0.21
0.11
0.09
0.08
0.35
0.11
0.12
0.12
0.14
0.15
0.03
0.04
0.11
0.23
0.24
0.08
0.08
0.11
0.13
0.16
0.19
0.13
0.16
0.15
0.21
0.23
0.21
Landmarks with loadings equal or greater than 0.20 are italicized. Comparable loadings of a same landmark on different
eigenvectors (e.g., frontal poles) may reflect various contributions of x, y, and z coordinates.
Differences in endocranial shape are most marked
between Homo sapiens and the other species (Fig. 5).
These shape differences are notably those associated
with PC1, mainly an increase in endocranial globularity and basicranial flexion. Orangutans are characterized by a short braincase, a dorsally oriented foramen
magnum, a wide space between frontal poles and olfactory bulb, the latter projecting downward, and widely
spaced foramina in the mediolateral direction. Gorillas
are characterized by a long and narrow brain (Fig. 5),
an extended basicranium, an olfactory bulb protruding
anteriorly, an anterior position of optic canals and
posterior point of anterior fossa relative to foramina
rotunda, and pyramids obliquely oriented anteriorly.
The brain of chimpanzees has a low endovertex, posteriorly located maximum cerebellar width, pyramids
less tilted anteriorly compared to other great apes, and
an olfactory bulb protruding anteriorly like gorillas.
Compared to chimpanzees, bonobos are characterized
by pyramids more coronally oriented and more inclined
anteriorly, a pattern drawn by foramina more compressed anteroposteriorly, a greater basicranial flexion,
an olfactory bulb protruding less anteriorly (Fig. 5),
American Journal of Physical Anthropology
and higher endovertex and maximum cerebral width.
In a recent study of MRI scans of hominoid brains,
Aldridge (2011) determines cortical and subcortical features that distinguish the human brain from that of
apes. Among these, human brains notably show an
anteroposterior expansion of the frontal regions, as
well as an expansion of the temporal lobes and the anterior parietal regions. Here all of these features are
observed endocranially, contributing to overall globularity of the human endocast. Aldridge (2011) also shows
patterns of morphology that uniquely differentiate each
ape species, among which an anteroposterior elongation of nonfrontal cerebral structures of gorillas that
can be observed here in the elongated shape of their
endocasts.
According to Bonferroni test, sexual dimorphism in
endocranial shape is only significant along PC1 within
gorillas. A separate PCA (not shown) was conducted on
mean shapes of male and female gorillas to free from
influences of the variation among species and better
assess ‘‘true’’ shape dimorphism within gorillas. Compared to males, endocasts of female gorillas display an
overall widening, inferior displacement of the frontal
poles, anterior and inferior displacement of endopisthion,
anterior displacement of jugular foramina, and posterior
displacement of occipital poles.
Static allometry
Correlations between the first two principal component
scores and log endocranial volume (Fig. 6) are significant
for African apes taken together (R2 5 0.58, P \ 0.05,
and R2 5 0.40, P \ 0.05, respectively). Hence, endocranial shape differences among African ape species along
PC1 and PC2 at least partially reflect endocranial size
differences, as they all follow a common pattern of
allometric shape change. On the contrary, humans are
clearly separated from the great apes and orangutans
markedly depart from the African apes allometric trajectories (Fig. 6). Correlation between PC1 and log endocranial volume is also significant within gorillas (R2 5 0.44,
P \ 0.05). Other intraspecific correlations between
PC1-2 and log endocranial volume are not significant,
but there seems to be a trend of males and females
separated within Pongo along PC1 (Fig. 6a), and males
of Pan troglodytes seem to display higher endocranial
volumes than females. These results suggest that a
larger sample may reach statistical significance for
dimorphism in endocranial volume in Gorilla, Pongo,
and Pan troglodytes, and for dimorphism in endocranial
shape along PC1 in Pongo.
Phenetic affinities
Figure 7 shows the result of the UPGMA of Procrustes distances. Overall, individuals from a species
cluster together, except for two chimpanzees: one clusters with bonobos, and another is situated at the root
of the cluster composed by chimpanzees and bonobos.
The tree displays the same topology as extant hominoid
molecular phylogeny, when humans are excepted
(Goodman et al., 1994; Ruvolo et al., 1994; Ruvolo,
1997). Pongo pygmaeus link at the base of a cluster
composed of African apes, both Pan species clustering
HOMINOID ENDOCRANIAL 3D GEOMETRIC MORPHOMETRICS
239
Fig. 5. Species pairwise Procrustes superimpositions of mean endocasts and corresponding frames. For each comparison, a specimen is put orange and transparent (by order of priority: Homo sapiens, Pongo pygmaeus, Pan paniscus, and Pan troglodytes) while
the other one is green and opaque. See Figure 2 for landmarks identification. (a) Right lateral view: Upper triangle, endocasts;
lower triangle, frames (for readability, foramina are connected). (b) Ventral view: Upper triangle, frames; lower triangle, endocasts.
closer to each other than to Gorilla gorilla. Humans
link at the root of the cluster formed by great apes,
supporting the peculiar morphology of human endo-
casts. Therefore, selected landmarks are well-suited to
capture endocranial differences among great apes and
humans.
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240
T. BIENVENU ET AL.
Fig. 6. Log endocranial volume versus PC1 (a) and PC2 (b).
Symbols are the same as for Figure 4. Dashed lines are regression axes for African apes.
DISCUSSION
Interspecific endocranial shape variation
Basicranial flexion and neurocranial globularity.
The first principal component mainly separates great
apes from humans and accounts for well known human
traits: neurocranial globularity and basicranial flexion.
Neurocranial globularity, or the three-dimensional
roundedness of the cranial vault (Lieberman et al., 2003)
is reflected by dorsal (vertex), anterior (frontal poles),
posterior (occipital poles), and lateral (maximum width)
expansion. However, this last feature does not appear
clearly in humans, except when compared to the relatively
narrow gorilla brain (Fig. 5). Neurocranial globularity
is linked to the development of visuospatial integration
(reorganization of parietal lobes), as well as verbal, cognitive, and social skills (reorganization of frontal lobes)
(Bruner, 2004; Holloway et al., 2004a). The other main
shape change associated with PC1 is basicranial flexion.
According to the spatial packing hypothesis, basicranial
flexion is a structural response to an increase in brain
size relative to cranial base length (Ross and Ravosa,
1993; Strait, 1999). Cranial base flexion, in combination
American Journal of Physical Anthropology
with a large brain and a small face, has been shown to
contribute to neurocranial globularity in recent human
evolution (Lieberman et al., 2002, 2003). Both characters
are correlated in the shape changes associated with PC1,
stressing that they are not independent from each other.
However, the combination of cranial base flexion and
neurocranial globularity is driven by the unique morphology of humans. Indeed, a separate PCA excluding
humans (not shown) displays an increase in basicranial
flexion along PC2—in this analysis of great apes alone,
morphological changes observed along PC1 correspond to
the ones observed along PC2 when including humans—
associated with a lateral expansion, but without the
strong dorsal, anterior, and posterior expansions typical
of the neurocranial globularity observed when humans
are included.
Basicranial flexion has also been linked to human
cranial modifications related to posture and bipedal
locomotion (Wood Jones, 1917; Weidenreich, 1941),
together with other shape changes related with PC1,
like shortening of the cranial base, anterior displacement
and horizontal positioning of the foramen magnum
(Zollikofer et al., 2005), and tilt of the line protuberanceendopisthion (roughly corresponding to the external
nuchal plane). Even though the postural hypothesis has
been rejected by several studies favoring the spatial
packing hypothesis (Ross and Ravosa, 1993; Strait and
Ross, 1999; Ross et al., 2004), Lieberman et al. (2000)
mention the possibility of an indirect link between basicranial angle and head posture, and McCarthy (2001)
suggests that the postural hypothesis may still be relevant for understanding hominid basicranial flexion. The
fossil record provides direct evidence that basicranial
flexion and neurocranial globularity can exist independently in early hominid evolution. Indeed some fossil
hominids are known to have flexed cranial bases without
any major increase in brain size or neurocranial globularity compared to great apes (Spoor, 1997; Lieberman
et al., 2003). This may reflect their bipedality (Spoor,
1997). Bastir et al. (2010) recently confirmed the multifactorial nature of basicranial flexion, showing that only
60% of variance in basicranial flexion among primates is
explained by brain and facial size.
Endocranial shape and facial morphology. Along
PC2, gorillas display the lowest scores, reflecting the
elongated appearance of their brains, and orangutans
the highest scores, corresponding to their short brains.
Using both internal and external cranial landmarks,
Zollikofer et al. (2008) show correlations between neurocranial shape, size of frontal sinuses and interorbital
space, and facial orientation. Their analysis separates
orangutans with a shorter neurocranial shape, absence
of frontal sinuses, narrow interorbital space, and
upwardly oriented (airorhynch) face, from African apes,
characterized by a more elongated neurocranial shape,
large frontal sinuses, wide interorbital space, and downwardly oriented (klinorhynch) face. The endocranial
modifications we observe along PC2 may have developed
in association with the facial modifications detailed in
Zollikofer et al. (2008), but this would need a study of
the relationships between endocranium and ectocranium, which is beyond the scope of this article.
Middle cranial fossa anatomy and relative disposition of foramina. Bastir et al. (2008) performed a 3D
geometric morphometric analysis of the middle cranial
fossa in humans, fossil hominids, and chimpanzees.
HOMINOID ENDOCRANIAL 3D GEOMETRIC MORPHOMETRICS
241
Fig. 7. Phenetic affinities between extant great apes and humans. Specimens were clustered by applying UPGMA on Procrustes
distances. Symbols are the same as for Figures 4 and 6. Gray branches represent repeated measurements of the same specimens.
They conclude that modern humans differ in having
anterolaterally projecting temporal poles relative to optic
canals and foramina rotunda (see shape changes associated with PC1 in Fig. 4, and Fig. 8). They also state that
in chimpanzees, temporal poles are at the same anteroposterior level as optic canals. Here we find that temporal poles are anterior to optic canals in every analyzed
species (Fig. 8). This contrasting observation may be
due, in part, to the way of digitizing landmarks. Indeed,
while we locate our temporal pole at the anteriormost
point on the temporal lobe, Bastir et al. (2008) define
their middle cranial fossa pole as the maximal 3D curvature of greater sphenoid wing.
Contrary to other studied species, gorillas and humans
are characterized by foramina rotunda located posteriorly relative to the optic canals (relatively low PC2
scores) (Fig. 8). In gorillas, this layout seems to be
mainly due to an anterior displacement of optic canals
relative to the temporal poles (Fig. 8). In humans, compared to great apes, a broad bridge of bone separates the
superior orbital fissure from the foramen rotundum (Fig.
9c). This, associated with the laterally extended shape of
the fissure, may be considered as a derived condition of
robust australopithecines and genus Homo (Rak et al.,
1996), depending on the phylogenetic relationships one
assumes between these taxa (Strait and Grine, 2004;
González-José et al., 2008). Formation of this broad
bridge of bone is associated with a more posteriorly
placed foramen rotundum, closer to the foramen ovale
(Figs. 8 and 9d). This posterior position of the foramen
rotundum in humans may be associated with a posteriorly situated distal portion of the maxillary nerve
(branch of trigeminal nerve, which passes through the
foramen rotundum to innervate mostly the lower face),
American Journal of Physical Anthropology
242
T. BIENVENU ET AL.
Fig. 8. Ventral view of mean endocasts. Endocasts were placed with the plane defined by frontal poles and occipital poles perpendicular to the view axis. Temporal poles were used to align specimens (straight line). Black points indicate optic canals medially,
foramina ovalia posterolaterally, and foramina rotunda. Note the more anterior position of optic canals relative to foramina rotunda
in humans and gorillas.
Fig. 9. (a) Posterior view of the inside of a chimpanzee cranium showing the relative disposition of optic canals (o.c.), superior
orbital fissures (s.o.f.), and foramina rotunda (f.r.). Thick black arrows indicate the thin bridges of bone separating superior orbital
fissures from foramina rotunda. d.s., dorsum sellae; m.c.f., middle cranial fossa. (b) Dorsal view of the inside of a chimpanzee
cranium. Because of their anterior position, foramina rotunda are not visible. f.o., foramen ovale; s.t., sella turcica. (c) Posterior
view of the inside of a human cranium. Thick black arrows indicate the broad bridges of bone separating superior orbital fissures
from foramina rotunda. Note also the laterally extended shape of superior orbital fissures. (d) Dorsal view of the inside of a human
cranium. Foramina rotunda are visible and much closer to foramina ovalia than in the chimpanzee.
perhaps correlated with reduction of the subnasal portion
of the face in humans compared to great apes. However,
the relationship between subnasal morphology and the
point at which the maxillary nerve exits the endocranium
deserves further studies.
Static allometry among African apes. African apes
display common allometric trajectories along PC1 and
PC2 (Fig. 6). Except for PC1-related shape differences
within gorillas, shape is only correlated with log endocranial volume interspecifically, not within other species
of African apes. Therefore, shape differences associated
with PC1 and PC2 among African ape species may be
accounted for, at least partly, by size differences. From
bonobos with lowest endocranial volumes to gorillas with
highest endocranial volumes, these shape differences
include a less flexed basicranium, a pattern drawn by
American Journal of Physical Anthropology
foramina less compressed anteroposteriorly, a more
anteriorly protruding olfactory bulb, and a longer and
narrower endocast.
McNulty (2004) has shown that allometry has a great
influence on hominoid cranial morphology. His phenetic
analysis based on ectocranial data corrected for allometry
clusters African apes with gibbons, which the author
interprets as a conservative hominoid morphology of
African apes, especially gorillas. By extrapolating his
interpretation to endocranial morphology, observed phenetic relationships between great apes (Fig. 7) might be
due partly to a primitive endocranial pattern shared by
African apes, rather than to endocranial synapomorphies.
According to this hypothesis, the common allometric trajectory shared among African apes would be conservative,
with orangutans and humans departing from this primitive trajectory. However, gibbons do not lie along the same
HOMINOID ENDOCRANIAL 3D GEOMETRIC MORPHOMETRICS
243
allometric trajectory as African apes (unpublished data).
Testing which endocranial morphologies are more primitive
and which ones are more derived would need further
studies, and notably the inclusion of fossil hominoids in
the model.
ferences. Rather, differences between the brains of
men and women appear in the internal organization
(proportions of gray and white matter) but are not
reflected externally.
Sexual dimorphism
CONCLUSIONS
Size sexual dimorphism. Gorillas and humans exhibit
the largest endocranial volumes among extant hominoids,
and they also show greater differences in endocranial
volume between males and females (though dimorphism
does not reach significance within gorillas). In apes, as in
many mammals, sexual dimorphism in body mass is more
pronounced in larger species (Rensch’s rule; Isler et al.,
2008). Gorillas are the largest living apes, hence the most
sexually dimorphic in body mass. As endocranial volume
is strongly correlated with body mass among apes (Isler
et al., 2008), higher levels of sexual dimorphism in endocranial volume observed in gorillas might be explained
by their more pronounced sexual dimorphism in body
mass.
However, this explanation is not adequate for humans.
The greatest part of brain size differences between men
and women is not due to differences in body size (Falk,
2001). Moreover, men and women have different neurological ‘‘Bauplans,’’ men having a higher percentage of
white matter and women a greater percentage of gray
matter (Gur et al., 1999). Falk (2001) suggests a possible
evolutionary interpretation of brain differences between
men and women. Her hypothesis assumes that discrepancies between the brains of men and women are related
to differential reproductive strategies in their ancestors.
A higher percentage of gray matter in women reflects
ancestral selection for skills appropriate for mothering,
like anticipation, forward planning, and vocal communication. This may be related to women’s superior performance in language tasks (Falk, 2001). On the other hand,
greater proportions of white matter in men are the
result of ancestral selection for better performance in
visuospatial tasks, allowing for mobility from the natal
group, and finding and competing for mates. Greater
proportions of white matter enhance intrahemispheric
connections, for example, between posterior visual areas
and motor cortex of the frontal lobe. This hypothesis of
male brain evolution explains why men perform better
at mental rotation of objects, spatial navigation, and
guiding or intercepting projectiles (Kimura, 1992).
Differences in the proportion of gray to white matter
may explain endocranial size differences between men
and women. Indeed, smaller endocranial volumes of
women require shorter distances for information transfer, hence a lesser need for white matter, which is the
myelinated connective tissue for information transfer
across distant regions (Gur et al., 1999).
Shape sexual dimorphism Endocranial shape dimorphism is significant only in gorillas, along PC1. As gorillas show significant dimorphism in endocranial volume
and PC1 is correlated with log endocranial volume, sexual dimorphism along PC1 is at least partly a consequence of allometry. Even though Bruner and Ripani
(2008) found significant sexual dimorphism in the
human cranial base, it seems that shape sexual dimorphism within Homo, Pan, and Pongo is mostly restricted
to the ectocranium (Schaefer et al., 2004). Interestingly,
contrary to gorillas, brain size sexual dimorphism in
humans is not accompanied by endocranial shape dif-
Our analysis of great ape and human endocasts demonstrates that endocranial shape varies greatly among
species. Major endocranial traits that distinguish
humans from great apes are endocranial globularity,
reflecting neurological reorganization, and features
linked to structural responses to posture and bipedal
locomotion, such as basicranial flexion. Among great
apes, orangutans are characterized by short brains with
a dorsally oriented foramen magnum, and a wide space
between frontal poles and the olfactory bulb, the latter
projecting downward. Gorillas have long and narrow
brains, with the optic canal anteriorly located relative
to the foramen rotundum. The brain of chimpanzees
displays a low endovertex, a posteriorly located maximum cerebellar width, and pyramids less tilted anteriorly compared to other great apes. The brain of bonobos
is characterized by an olfactory bulb projecting less anteriorly compared to that of chimpanzees and gorillas, and
a higher maximum cerebral width than in other great
apes. Common allometric trajectories for African apes
show that endocranial shape differences among these
species are partly due to size differences.
Aside from endocranial globularity and features
linked to bipedality, one peculiar trait of human endocasts is the posterior location of the foramen rotundum
relative to the optic canal, and its proximity to the foramen ovale. This trait may be considered as a synapomorphy of robust australopithecines and genus Homo
(Rak et al., 1996), depending on the phylogenetic relationships one assumes among these taxa (Strait and
Grine, 2004; González-José et al., 2008). Posterior displacement of the foramen rotundum may be associated
with a similar displacement of the distal portion of
maxillary nerve, which could be correlated to a lesser
subnasal prognathism in humans compared to living
great apes.
Species with larger brains (gorillas and humans) display greater sexual dimorphism in endocranial volume.
Whereas sexual dimorphism in brain size in gorillas is
at least partly a consequence of sexual dimorphism in
body mass, other explanations must be sought for
humans. Brain size dimorphism in humans may be due
to differential selection in male and female ancestors
(Falk, 2001), which would also explain differences in the
internal organization of the brain (proportions of gray
and white matter). Gorilla gorilla is the only species
which displays sexual dimorphism in endocranial shape,
differences between males and females being at least
partly due to allometry. Brain size dimorphism in
humans is not reflected in external brain shape.
During the past two decades, the development of new
techniques such as computed tomography and geometric
morphometrics has initiated new perspectives for the
study of endocasts, with taxonomic, evolutionary, and
functional implications. Application of these techniques
here has allowed for investigation of patterns of variation in endocranial shape and size among extant adult
great apes and humans. The present analysis constitutes
a basis for future work on juveniles and fossil hominids
American Journal of Physical Anthropology
244
T. BIENVENU ET AL.
(direct evidence of brain evolution) and investigation of
the relationship between endo- and ectocranial shape.
ACKNOWLEDGMENTS
We wish to thank the following institutions and people
for allowing us the access to their specimens: Dr. W. Wendelen of the Musée Royal de l’Afrique Centrale (Tervuren,
Belgium), Pr. C.P.E. Zollikofer and Dr. M. Ponce de León of
the Anthropologisches Institut und Museum (Zürich, Switzerland), the Natural History Museum (London, United
Kingdom), and the Staatssammlung für Anthropologie
und Paläoanatomie München (Munich, Germany). We also
thank the following facilities and people for the CT-scans
data acquisition: Pr. Marchal of the Department of Radiology of UZ Leuven (Leuven, Belgium), the Kantonsspital
Winterthur (Winterthur, Switzerland), the Hammersmith
Hospital (London, United Kingdom), and the medical practice of Dr. Wuttge and colleagues (Munich, Germany). We
thank Dr. D. Pushkina, Dr. R. Lebrun, and Dr. F. Bibi
for fruitful discussion. We acknowledge all the iPHEP
(Université de Poitiers; CNRS: INEE Institut Ecologie et
Environnement) members for technical support and
administrative guidance. We greatly thank an associate
editor and two anonymous reviewers for their helpful
comments on earlier drafts of this manuscript.
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