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evolution in the genus Homo
Dipartimento di Biologia Animale e dell’Uomo, Universita` La Sapienza, P.le A. Moro 5, 00185 Roma, Italy
Istituto Italiano di Paleontologia Umana, P.za Mincio 2, 00198 Roma, Italia
Received 13 November 2003; accepted 18 March 2004
Paleoneurology concerns the study and analysis of fossil endocasts. Together with cranial capacity and discrete
anatomical features, shape can be analysed to consider the spatial relationships between structures and to investigate
the endocranial structural system. A sample of endocasts from fossil specimens of the genus Homo has been analysed
using traditional metrics and 2D geometric morphometrics based on lateral projections of endocranial shape. The
maximum and frontal widths show a size-related pattern of variation shared by all the taxa considered. Furthermore, as
cranial capacity increases in the non-modern morphotypes there is a general endocranial vertical stretching (mainly
centred at the anterior ascending circumvolution) with ﬂattening and relative shortening of the parietal areas. This
pattern could have involved some structural stress between brain development and vault bones at the parietal
midsagittal proﬁle in the heavy encephalised Neandertals. In contrast, modern humans show a species-speciﬁc
neomorphic hypertrophy of the parietal volumes, leading to a dorsal growth and ventral ﬂexion (convolution) and
consequent globularity of the whole structure.
Brain tensors such as the falx cerebri have been hypothesised to represent one of the main physical constraints on
morphogenetic trajectories, with additional inﬂuences from cranial base structures. The neurofunctional inferences
discussed here stress the role of the parietal areas in the visuo-spatial coordination and integration, which can be
involved in higher cerebral functions and related to conceptual thinking.
Ó 2004 Elsevier Ltd. All rights reserved.
Keywords: human evolution; endocranial morphology; fossil endocasts; brain shape
* Dipartimento di Biologia Animale e dell’Uomo, Universita´ La Sapienza, P.le A. Moro 5, 00185 Roma, Italy. Tel. C39 06 4991
2690; Fax: C39 06 4991 2771.
E-mail address: email@example.com
0047-2484/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved.
Journal of Human Evolution 47 (2004) 279e303
Considering the tight ontogenetic relationship
between brain shape and skull bones (Moss and
Young, 1960; Enlow, 1990), the endocasts from
fossil crania are a useful source of information on
hominid cerebral morphology and anatomy. This
principle is the basis of paleoneurology, namely
the examination and analysis of natural or
artiﬁcial endocasts that reproduce details of the
external morphology of the brain (Holloway,
1978; Falk, 1986, 1987; Bruner, 2003a).
Although brain size has been the principal issue
considered in the paleoanthropological literature,
paleoneurology also focuses on speciﬁc anatomical
traits, like vascular patterns (e.g. Kimbel, 1984;
Falk, 1993; Saban, 1995; Grimaud-Herve´ , 1997),
cerebral asymmetries (Le May, 1976; Holloway
and De La CosteLareymondie, 1982), or speciﬁc
circumvolutions (Grimaud-Herve´ , 1997).
Brain shape variation has rarely been analysed,
mainly because of the fragmentary nature of the
fossil record. Furthermore, there are some diﬃ-
culties in coding and quantifying endocranial
morphology, because of the smooth geometry of
the brain itself. A pioneering approach to endo-
cranial shape variation in fossil hominids was
performed using a polar coordinate stereoplotting
technique to compare extant and extinct Homi-
noidea (Holloway, 1978, 1981a). This research
suggested that a large amount of variation can be
localised in the lower parietal areas in the extant
taxa, and in the upper parietal districts considering
the extinct groups.
It has been hypothesised that early changes in
the frontal areas in Australopithecus were followed
by a late and gradual evolution of posterior
districts in early human representatives (Falk
et al., 2000). In earlier hominids the principal
diﬀerences from apes may have been a reduction
of the primary visual striate cortex, a reorganisa-
tion of the frontal lobe (mostly at the third frontal
circumvolutions), and the expression of hemi-
spheric specialisation (Holloway, 1995). Subse-
quently, the development of the posterior parietal
cortex may have been related to an increase in
visuospatial integration, sensory reception, and
One of the most studied area in fossil endocasts
is represented by the frontal lobes, because of their
presumed role in higher cognitive functions and
language. Generally, the frontal lobes are nar-
rower in the most archaic Homo taxa, showing
a clear ‘‘encephalic rostrum’’ (Grimaud-Herve´ ,
1997). The lateral development of these structures
in more encephalised hominids leads to a more
pronounced expression of the Broca’s cap, which
is involved in speech potentialities (e.g. Aboitiz
and Garcia, 1997; Cantalupo and Hopkins, 2001).
The frontal midsagittal proﬁle is less variable,
without marked shape diﬀerences between Middle
Pleistocene and modern humans (Bookstein et al.,
1999). The position of the frontal lobes can be
strongly inﬂuenced by a marked pneumatisation,
which pushes backward the entire orbital plate in
some robust Middle Pleistocene specimens such as
Petralona and Kabwe (Seidler et al., 1997). At the
opposite extreme, the occipital lobes project back-
ward behind the parietal proﬁle in more archaic
brains, shifting under the parietal areas as brain
size increases. Accordingly, the cerebellar struc-
tures are located under the occipital poles in
archaic Homo erectus, under the parietals in more
derived taxa and almost under the temporal areas
in modern humans (Grimaud-Herve´ , 1997). The
brain’s maximum width is located at the temporal
base in Homo erectus and other Middle Pleistocene
groups, between the temporal and parietal areas in
Neandertals, and at the parietals in anatomically
modern humans (Holloway, 1980; Grimaud-
Herve´ , 1997; Seidler et al., 1997). KNM-WT
15000 (dated to about 1.5 Ma) and the other
specimens included in the Homo ergaster hypo-
digm show an endocast comparable to those of
Asian Homo erectus, but with a less developed
frontal diameter and without a marked occipital
projection (Begun and Walker, 1993).
A recent study on the shape variation of the
endocast in the genus Homo showed two major
patterns of variation (Bruner et al., 2003): an
archaic structural trajectory shared by non-
modern taxa and characterised by an allometric
vertical development, frontal enlargement, and
parietal relative shortening, versus a modern pat-
tern characterised by parietal development leading
to brain globularity.
280 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
In this paper, the endocranial shape of some
fossil specimens included in the hypodigm of the
genus Homo is investigated using traditional
metric comparisons and two-dimensional geomet-
ric morphometrics performed on projected lateral
views of the endocast. The aim is to consider in
detail some speciﬁc variables of the human fossil
endocasts, and to characterise the endocranial
morphology in norma lateralis. This approach is
used to check and improve previous results from
three-dimensional analyses. The lateral view (and
particularly the midsagittal vault proﬁle) has been
frequently considered in evolutionary studies
because of its recognised availability, usefulness,
and evolutionary meaning (e.g. Manzi et al.,
2000b; Lieberman et al., 2002; Bruner et al.,
2004). Also, projections and 2D data allow the
use of type III landmarks (Bookstein, 1991),
geometrically deﬁned by chords or fractions of
curvature. Type III landmarks have no biological
meaning in terms of homology, but can be used to
deﬁne structures or areas that lack clear anatom-
ical references. These points can be extremely
useful when considering endocranial shape, for
which type I (i.e. homologous) and type II
(structurally corresponding) landmarks are rare.
The null hypothesis of this analysis is that
human brain evolution was based on quantitative
encephalisation, i.e., endocranial enlargement
without change of the structural model. This
hypothesis suggests that endocranial variation
within the genus Homo was characterised by
scaled (i.e. allometric) versions of a plesiomorphic
morphological plan, described by a shared struc-
tural trajectory. Conversely, the recognition of
group-speciﬁc patterns would suggest the presence
of neomorphic processes.
Materials and methods
Data were collected from high-quality endo-
casts at the Museum of Anthropology ‘‘Giuseppe
Sergi’’ (Dipartimento di Biologia Animale e
dell’Uomo, Universita` La Sapienza, Roma), the
Istituto Italiano di Paleontologia Umana (IsIPU,
Roma), and the Institut de Pale´ontologie Humaine
As in previous analyses (Bruner, 2003b; Bruner
et al., 2003), the specimens were included in
three main groups in order to identify general
1. Archaic morphotypes (ARC): specimens re-
ferred to Homo erectus sensu lato (s.l.), namely the
Asian Early and Middle Pleistocene remains
(Homo erectus sensu stricto e s.s.) plus the
specimens from Sale´ (Africa) and Arago (Europe).
It is assumed that, even if the Asian specimens
show some apomorphic or autapomorphic traits,
they represent a less derived model with respect to
Neandertals and modern humans. The Sale´ skull is
not entirely interpreted, but it is assumed to
represent a plesiomorphic pattern compared to
more encephalised taxa of the genus Homo.
Asymmetries at the nuchal ectocranial structure
in Sale´ suggest a pathological congenital torticollis,
related to atrophy of some nuchal muscles, and
asymmetrical reduction of the surface insertions
(see Hublin, 2002). In contrast, no marked
asymmetry is shown at the internal surface, except
for minor diﬀerences related to a common left
occipital petalia tilting the midsagittal axis and the
underlying cerebellar poles. Furthermore, the
relative independence between inner and outer
tables of the skull (involving epigenetic muscle-
related traits) suggests that endocranial morphol-
ogy is not strongly aﬀected by the hypothesised
The Arago endocast is the result of a hybrid
reconstruction composed of the Arago frontal and
parietal (respectively Arago 21 and Arago 47) and
the occipital from Swanscombe and the temporals
from Sangiran 17. Therefore, it represents a het-
erogeneous but in any case less derived system
with respect to Neandertals and modern humans.
Clearly, all of these assumptions are based on a set
of inferences about the phylogenetic status of these
specimens, but they are necessary to produce
a reference variability
2. Neandertals (NDR): European Wurmian
Neandertals, here recognised as Homo neandertha-
lensis. A stereolithographic model of the virtual
endocast of Saccopastore 1 (Bruner et al., 2002)
has been included in this group. Although the
281 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
fossils from Saccopastore are dated to about 120
Ka, they show Neandertal derived traits both for
the ectocranial (Sergi, 1944; Condemi, 1992) and
endocranial (Bruner, 2003b) morphology. The
skull from Teshik-Tash represents a juvenile in-
dividual, but its ontogenetic stage is assumed not
to aﬀect the endocranial comparison. Brain
growth is almost complete at this age, with the
brain weight of modern human populations rea-
ching 96% and 99.7% of the adult values at
the puberty and adolescence respectively (Pen˜ a-
Melian, 2000). Furthermore, Neandertal cranial
shape shows rate-hypermorphosis compared to
modern humans, and the taxonomic diﬀerences
are expressed early during ontogeny (Ponce de
Leo` n and Zollikofer, 2001). According to its
cranial development, Teshik-Tash, about 8.5 years
old, is comparable to Qafzeh 11, approximately
13.5 years old (Ponce de Leo` n and Zollikofer,
2001). Therefore, the cranial shape must be
assumed suﬃciently comparable with the adult
3. Modern Humans (MOD): anatomically mod-
ern humans, from Late Pleistocene to recent
populations. This group includes the endocast of
Vatte di Zambana, recovered near Trento (Italy) in
1967-68 and dated to 8 ka (Corrain et al., 1976;
Newell et al., 1979). A modern endocast from
a recent Javan individual is also included in this
group. It shows an extreme brachycephalic ex-
pression of the modern cerebral packing, present-
ing an almost globular structure that may be useful
to understand the trends and variability of the
Homo sapiens model.
In Table 1 a list of the entire sample is provided,
with information about the repository source, the
reference group, and the labels used in the text.
Univariate and bivariate metrics
Fig. 1a shows the diameters employed in this
analysis, and Table 2 provides a list of the
endocranial variables, together with the respective
labels and deﬁnitions. Lengths and widths were
measured with a spreading caliper directly on the
endocast. Chords and heights were measured by
projecting the respective landmarks onto the left
hemisphere in lateral view through a dioptograph.
Endocasts were aligned using the plane passing
through the frontal crest, the internal occipital
protuberance, and the endovertex. Absolute values
have been considered as well as relative values,
which were divided by the maximum length of the
endocast (averaged hemispheres). Diﬀerences be-
tween groups were analysed by Kruskal-Wallis
analysis of variance. Regressions were analysed by
the least-squares procedure and both Pearson’s
and Spearman’s correlation coeﬃcient. Statistical
signiﬁcance was set at p ! 0.05. A Major Axis
regression has been computed by Model II
(Legendre, 2001 - http://www.fas.umontreal.ca/
biol/legendre). Repeated measures of diameters
on the endocast sample revealed an average error
of 0.6 mm, due mostly to uncertainty in local-
isation of type II (Bookstein, 1991) and fuzzy
landmarks (Valeri et al., 1998). The maximum
average error for repeated measures was 0.9 mm (a
discrepancy less than 5%). Considering these
limits in the metric resolution, the diameters were
taken to the nearest millimetre.
List of the whole sample, with labels used in the text, reference
group, and repository site
Specimen Label Group Repository*
Trinil 2 TRN2 ARC IsIPU
Sangiran 2 SNG2 ARC IPH
Sale´ SAL ARC BAU
Sinanthropus III ZKD3 ARC BAU
Sinanthropus X ZKD10 ARC IPH
Sinanthropus XII ZKD12 ARC IsIPU
Arago (rec) ARA ARC IsIPU
Saccopastore 1 SCP1 NDR BAU
La Chapelle-aux-Saints CHP NDR IsIPU
La Ferrassie 1 FRS NDR IPH
Teshik-Tash TST NDR IPH
Guattari 1 GTT NDR IsIPU
Feldhofer Grotto FLD NDR BAU
Predmostı` 3 PRD3 MOD IPH
Predmostı` 4 PRD4 MOD IPH
Predmostı` 9 PRD9 MOD IPH
Predmostı` 10 PRD10 MOD IPH
Combe-Capelle CCP MOD IsIPU
Vestonice 2 VST2 MOD IPH
Vatte di Zambana VTT MOD IsIPU
Recent Human Endocast RHE MOD IPH
*BAU: Dipartimento di Biologia Animale e dell’Uomo.
IsIPU: Istituto Italiano di Paleontologia Umana.
IPH: Institut de Pale´ontologie Humaine.
282 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
Endocranial shape was also analysed by a land-
mark-based approach, according to the proce-
dures of geometric morphometrics (Bookstein,
1989; Rohlf and Bookstein, 1990; Bookstein,
1991; Marcus et al., 1993; Rohlf and Marcus,
1993; Marcus et al., 1996). In geometric morpho-
metrics, systems of coordinates are superimposed
to minimise the size diﬀerences between specimens,
with the aim of identifying the shape component of
the total form (see Richtsmeier et al., 2002; Rohlf,
2003). A two-dimensional conﬁguration of nine-
teen landmarks was selected to describe the
endocranial lateral proﬁle. Landmarks were cho-
sen based on an operational homology deﬁnition
(see Smith, 1990). Table 3 shows the list of
landmarks, together with their labels and deﬁni-
tions. Fig. 1b shows the entire conﬁguration. The
left hemisphere was used, except for Combe
Capelle that shows excessive damage on that side.
A Generalised Procrustes Analysis (GPA) was
performed, except in the 2D pairwise comparison
in which a Bookstein superimposition was pre-
ferred. The ﬁrst procedure superimposes the
conﬁgurations through translation of the cent-
roids, scaling to unitary size, and least-square
rotation, while the second uses a reference baseline
between two landmarks (Bookstein, 1991). For the
Bookstein superimpositon the frontal and occipital
poles were used as references for the baseline. This
superimposition was used in the pairwise compar-
isons considering the hemispheric length a good
index of quantitative encephalisation, useful to
display diﬀerences in shape at the same endocra-
nial antero-posterior development. Furthermore,
Fig. 1. a) Interlandmark distances sampled on the endocasts, in left lateral and upper view. The diameters have been measured directly
on the endocasts, while chords and projections have been obtained using a dioptograph (see Table 2 for labels and deﬁnitions). b)
landmark conﬁguration used in the 2D geometric morphometric analysis (left hemisphere - see Table 3 for labels and deﬁnitions); for
the PCA a reduced conﬁguration has been used, considering only the vault morphology (landmarks between FP and OP).
283 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
this conﬁguration is mainly based on the anterior
and posterior extremes. Anyway, in this analysis
superimpositions using the baseline or the pro-
crustes procedure gave the same results, more
evidenced in the former approach. Centroid size is
used as size index, deﬁned as the square root of the
sum of squared distances of a set of landmarks
from their centroid (Marcus et al., 1996). Data
were sampled using a dioptograph and digitised by
tpsDig 1.20 (Rohlf, 1998a). The Principal Compo-
nent Analysis (PCA) required a minimum statis-
tical balance between specimens and landmarks,
and the use of missing data was unsuitable.
Therefore, to keep a suﬃcient fossil sample, only
the landmarks from the vault (between FP and
OP) were used (9 landmarks, 21 specimens). The
vault conﬁguration was used in a Cluster Analysis
of individual specimens based on the Procrustes
distance matrix and the unweighted pair-group
method using arithmetic averages (UPGMA). As
stressed before, this analysis is aimed at character-
ising phenotypes only in terms of shape, having
landmarks a geometrical and structural meaning.
The perpendicular scissure (i.e. the crossing
point in lateral view between this scissure and the
interhemispheric one) has not been used in the 2D
conﬁguration because of incompatibility between
ﬁxed homologous landmarks and shifting geo-
metric landmarks. The sequence along the midline
presents the perpendicular scissure situated be-
tween the 2
posterior chord projection
(thus, between P2 and P3) in Homo erectus and
Homo sapiens specimens. In contrast, in Nean-
dertals and the specimen from Sale´ the perpendic-
ular scissure lies before the midpoint of the
posterior projection (thus, anterior to P2). This is
probably related to the occipital projection in
Homo erectus, and to the parietal development in
Homo sapiens. This inversion leads to some
visualisation diﬃculties in spatial deformation,
but it is still a useful geometric indication that
must be considered in future studies. Considering
the landmarks used in these analyses, it must be
stated that the terms ‘‘parietal’’ is used here to
describe a surface that should overlap with the
underlying cortical structure. When the Rolandic
and perpendicular scissures are involved (as in the
interlandmark metrics), this relationship is quite
tight, and it is used to describe the presumed
boundaries of the parietal lobes. Conversely, when
the general outlines are considered (as in the
geometric morphometric approach), ‘‘parietal
List of the interlandmark distances used in the metric analysis, with labels and deﬁnitions
Label Measure Deﬁnition
ML maximum length maximum hemispheric length from frontal to
occipital poles - averaged hemispheres
MW maximum width maximum width of the endocast, orthogonal to
the midsagittal cerebral plane
BW Broca width maximum width of the endocast at the base of the third
H1 anterior height vault height at the anterior quarter - 25% - of the maximum
H2 middle height vault height at the middle - 50% - of the maximum
H3 posterior height vault height at the posterior quarter - 75% - of the
maximum length chord
VM vault module mean value between maximum length, maximum
width and middle height
FC frontal chord chord between the most anterior point of the frontal pole and the
rolandic scissure at the midsagittal plane
PC parietal chord chord between the Rolandic scissure and the perpendicular
scissure at the midsagittal plane
OC occipital chord chord between the perpendicular scissure and the torcular
herophili at the midsagittal plane
284 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
areas’’ are used to describe surfaces that are not
necessarily related to speciﬁc circumvolutions.
Other functionally interesting structures - like
the supramarginal gyrus or other speciﬁc circum-
volutions - have not been included in this analysis
because of the excessive uncertainty with respect to
the available variation. For the supramarginal
gyrus, problems arose in the exact localisation of
the boundaries of this area, which is smooth and
irregular. This gyrus is included in Wernicke’s area
and it represents one of the major sources of
asymmetry in the human brain, generally being
more strongly expressed on the left hemisphere.
Therefore, cerebral dominance leads to a diﬀerent
location of the homologous counterpart on the
right side. Once the gyrus has been localised, the
choice of the landmarks to represent this area is
not unequivocal, and often the centroid of the boss
does not overlap with the point of maximum
curvature of the circumvolutions. Structures like
the supramarginal or the angular gyrus would be
better considered only in group-averaged and
As cautionary note, it must be noted the
bidimensional projections of volumes can be
misleading if the geometric properties of the model
are not considered carefully. In this 2D conﬁgu-
ration, the results will be inﬂuenced by the
diﬀerent orientation of speciﬁc areas, as the
cerebellar lobes. The more angled they are relative
to the midsagittal plane, the shorter they will
appear to be in a 2D projection. In any case, such
an approach is necessary to consider geometrically
derived landmarks from chords and projections
and to characterise areas that lack clearly local-
isable points. It must be stressed that, because of
the group-speciﬁc limited sample size, it is diﬃcult
to conduct between-group tests of signiﬁcance.
Instead, pairwise comparisons, cluster procedures,
and multivariate approaches are used to character-
ise and describe the main phenotypic aﬃnities
among specimens. Morpheus et al. (Slice, 2000 -
http://life.bio.sunysb.edu/morph/) was used to
compute average shapes and pairwise compari-
sons. Applied Procrustes Software 2.3 (APS; Penin,
2000 - http://www.cpod.com/monoweb/aps/) and
tpsRelw 1.18 (Rohlf, 1998b - http://life.bio.sunysb.
edu/morph/) were used for the PCA. Procrustes
distances were obtained by tpsSmall 1.19 (Rohlf,
1998c). Cluster Analysis was performed by
List of the landmark used in the geometric morphometric analysis, with labels and deﬁnitions
Label Landmarks Deﬁnition
FP frontal pole the most anterior point of the endocast according to the maximum length
RS rolandic scissure meeting point between the rolandic and interhemispheric scissures
F1-F3 frontal projections meeting points between the endocranial outline and orthogonal chords drawn
at fractions of the frontal chord (respectively at 0.25, 0.50, 0.75)
OP occipital pole the most posterior point of the endocast according to the maximum length
P1-P3 posterior projections meeting points between the endocranial outline and orthogonal chords
drawn at fractions of the posterior chord (respectively at 0.25, 0.50, 0.75)
TH torcular herophili point of maximum depression at the internal occipital protuberance
TOC temporo-occipito-cerebellar meeting point between the cerebro-cerebellar scissure and the preoccipital
scissure, between the 3
temporal and 3
TV temporal valley posterior end of the temporal valley, between the temporal and cerebellar areas,
at the angle between the temporal and cerebellar lobes
ACC anterior cerebellar anterior point of the cerebellar outline, at the meeting
with the temporal lobe
PCC posterior cerebellar posterior point of the cerebellar outline, at the meeting
with the occipital lobe
C1-C3 cerebellar projections meeting points between the cerebellar outline and orthogonal chords drawn at
fractions of the cerebellar chord ACC-PCC (respectively at 0.25, 0.50, 0.75)
TP temporal pole point of maximum curvature of the temporal lobe
BA Broca area point of maximum curvature between the pars opercularis and pars
triangularis at the 3
285 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
UPGMA using the Phylogeny Inference
Package (PHYLIP, 3.57c; Felsenstein, 1989
html), while phenograms were computed with
TREEVIEW (Page, 1996 - http://taxonomy.
Univariate and bivariate metrics
Univariate distributions are reported for each
main group by median and quartile values (Table
4). Considering the absolute diameters, the more
derived groups (NDR and MOD) show signiﬁ-
cantly larger values for the vault module and
maximum endocranial length when compared to
the archaic average.
Neandertals and modern humans show a signif-
icant larger value for the frontal chord, with
modern humans also showing a larger parietal
chord. Considering the relative values, Neandertals
display a larger frontal and a shorter parietal chord,
while modern humans have a relatively greater
development of the parietal value. A bivariate plot
of frontal and parietal chords shows that, moving
from the archaic specimens (mostly the small
individuals) to the Neandertals, an increase of the
ﬁrst value is not associated with an increase of the
second. In contrast, the modern sample shows an
increase in both variables (Fig. 2a).
The vault heights show a clear pattern of
increasing values from the archaic group to
Neandertals to modern humans. The diﬀerences
between NDR and MOD are signiﬁcant for the
posterior height (H3 - both absolute and relative
values). The anterior and middle heights show
signiﬁcant diﬀerences for the smaller values of the
archaic group (absolute data) or between archaic
and modern humans (relative data), even if the
trend is similar to that of posterior height. The
heights show the strongest correlation with
the vault module (r Z 0.87, 0.91, and 0.85
respectively). Considering this allometric relation-
ship, the modern specimens seem to depart from
a trajectory shared by the non-modern sample
(Fig. 2b). The diﬀerences in the relative height T
286 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
values are attenuated but conﬁrm the gradual
increase between the main groups, and for the
posterior height the diﬀerences are again pro-
nounced. A full statistical approach to the species-
speciﬁc regression coeﬃcients has not been
performed because of the limited sample size.
Nevertheless, if we pool the archaic and Neander-
tal specimens into a non-modern group, the
regressions between vault module and heights
show a set of slopes distinctly diﬀerent from the
modern pattern (Fig. 2c). Interestingly, the within-
group scheme seems comparable (with middle
height more sensitive to size), but with higher
values in the modern group. Among the relative
measures, heights are the only variables maintain-
ing a signiﬁcant correlation with the vault module
(r Z 0.48, 0.58, and 0.58 respectively).
The maximum width presents signiﬁcantly
greater values for moderns and Neandertals,
slightly higher for the latter group. When the
maximum width is corrected for the hemispheric
length, the diﬀerences seem to fade, with a large
range of variation in modern humans and slightly
higher mean values for Neandertals. The modern
range is strongly inﬂuenced by the rounded (wide
and short) RHE endocast and the lengthened (thin
and long) VST2 brain. The width at Broca’s cap
shows an absolute distribution very similar to the
Fig. 2. Bivariate comparisons. a) frontal chord vs. parietal chord. b) vault module vs. posterior height (H3). c) slopes (alpha) for the
regression between vault module and heights (H1, H2, H3) for the non-modern (bold line) and modern (plain line) groups. d)
maximum width vs. frontal width at the Broca’s cap. The three groups are represented by circles (ARC), squares (NDR) and triangles
(MOD). Values are in mm. See Table 1 for labels.
287 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
maximum width. With respect to the hemispheric
length, the mean values of the two derived
morphotypes are still above that of the archaic
group. The ratio between the Broca and maximum
widths expresses an archaic pattern, with a limited
frontal diameter compared with the total breadth,
and two derived morphotypes (Neandertals and
moderns) with relatively enlarged frontal width. A
Kruskal-Wallis test between archaic and non-
archaic values is signiﬁcant at 0.08 level (which is
indicative, considering the small number of speci-
mens). A bivariate plot of MW vs. BW (Fig. 2d)
suggests no clear species-speciﬁc departure from
a shared trajectory. A correlation between these
two diameters and the vault module shows
coeﬃcients of 0.84 (MW) and 0.91 (BW). In-
terestingly, a least square regression shows the
frontal width scaling with a slope of 0.95, while the
maximum (parieto-temporal) width scaling with
a slope of 0.80. Because of the small sample size,
the 95% conﬁdence intervals of these slopes are
large, overlapping each other and both including
isometry. The major axis computed on the same
variables shows slopes respectively of 0.94 (maxi-
mumwidth vs. vault module) and 1.04 (Broca width
vs. vault module), with the same considerations on
the conﬁdence intervals. In general, this second
approach would be more appropriate to analyse the
relationship between two variables but, because of
the limited sample size and because of the likely
non-normal distribution of the variation (which
includes multiple taxa), it could be a less robust
result (see Martin and Barbour, 1989; Legendre and
Legendre, 1998). The regressions are all signiﬁcant,
but the coeﬃcients cannot be properly analysed and
should be considered only indicative. Generally,
these data may suggest that as size increases the
frontal diameter widens slightly faster than the
maximum (temporo-parietal) breadth.
The occipital chord is larger in Neandertals and
modern humans, but the diﬀerences are not
signiﬁcant when the relative values are considered.
The PCA applied to the vault coordinates
shows a polarised morphospace, in which the ﬁrst
two components account for 89% of the total
variance (Fig. 3a). The 1
component (69% of the
total variance) is related to parietal development.
At lower values the parietal outline ﬂattens and
shortens, with consequent relative lengthening of
the vault. The frontal area enlarges and bends
upward, while the occipital pole undergoes a ver-
tical shortening. At higher values, the parietal area
grows almost orthogonal to the midsagittal proﬁle.
The vault thus becomes higher and relatively
shorter, with reduction of the most frontal surface
and vertical development of the posterior districts.
This ﬁrst axis mostly separates modern humans,
with a developed parietal outline and shortened
frontal and occipital poles, from non-modern
specimens, which show endocranial ﬂattening at
the parietal outline. The 2
component (20% of
the total variance) involves a general stretching of
the vault vertically at lower values and a vertical
ﬂattening on at higher values. The vertical
stretching/ﬂattening is particularly localised ante-
rior to the Rolandic scissure, namely at the
ascending frontal circumvolutions. This second
axis separates Neandertals with relatively high
vaults and developed frontal areas, from the
archaic samples, which are more platycephalic
and have a reduced frontal development. The
modern sample is split by this component into
more rounded proﬁles versus high and lengthened
ones (mostly VST2 and CCP). A plot of the ﬁrst
two principal components shows a good separa-
tion of the three main groups (Fig. 3b), modern
humans showing a developed parietal outline,
Neandertals displaying high vaults and ﬂattened
parietals, and the archaic group with a low vault
and ﬂattened parietals. The following axes are
related to small percentages of variability (!4%).
When the ﬁrst axis is plotted against the centroid
size, two clusters are easily identiﬁed (Fig. 3c). The
modern sample is separate, with large size and
derived parietal growth. The other two groups lie
contiguously with Neandertals having larger but
slightly more ﬂattened parietals. Therefore, in non-
modern specimens there is a change of size without
marked changes of shape, while there is a morpho-
logical gap between modern and non-modern
specimens in the relationship of shape to size.
Considering the whole shape variation, both
multiple regression and partial least-square
288 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
regression onto centroid size do not ﬁnd other
allometric vectors. Considering just the archaic
and Neandertal specimens, a PCA shows a ﬁrst
axis of variation weakly correlated with centroid
size (partial least-square regression: r Z 0.64,
p Z 0.02), separating archaic specimens from
Neandertals, and involving (from smaller to
larger conﬁgurations) parietal ﬂattening and
shortening associated with frontal vertical de-
velopment (Fig. 4). Clearly, a larger number of
specimens would be required for a useful statis-
tical approach to the species-speciﬁc allometric
A UPGMA applied to the Procrustes distances
between specimens using this endocranial vault
conﬁguration shows the main separation to be
between modern and non-modern samples
(Fig. 5a). Within the non-modern group, Archaic
and Neandertal specimens show two principal
clusters that, however, do not represent exactly the
two respective taxa. The Asian Homo erectus
specimens show a close phenetic aﬃnity to each
Using the complete conﬁguration, the consen-
sus average shapes of the two more derived groups
were compared to the mean archaic conﬁguration
Fig. 3. Vault shape 2D analysis. a) distortion grids showing the two extreme conﬁgurations along the PC1 and PC2 vectors (left
hemisphere). PC1 is mainly characterised by parietal reduction/development, with consequent bending/convolution of the vault. PC2
describes a vertical stretching/ﬂattening of the vault, localised mainly anteriorly to the Rolandic scissure (frontal ascending
circumvolution) b) plotting of PC1 and PC2 values computed on the Procrustes residuals. c) PC1 values are plotted against centroid
size (groups and labels like Fig. 2).
289 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
by superimposition of the fronto-occipital baseline
ARC vs. NDR. The entire structure stretches
vertically in NDR, and the frontal area enlarges.
The occipito-cerebellar complex shifts forward.
There is increased development of the temporo-
occipital surface. The grid generally describes a
vertical development, with an upward bending of
the vault. The endocast undergoes a slight dorsal
ﬂexion by means of an upward shifting of the ex-
tremities and a retrograde movement of the upper
landmarks. The internal occipital protuberance
(and the whole posterior district) shows a geomet-
ric compression, as a structural meeting point of
forces deriving from the dorsal bending and verti-
cal stretching. The conﬂuence of sinuses becomes
less deepened under the ﬂattening occipital poles.
ARC vs. MOD. The vault enlarges and develops
vertically in MOD, mostly because of an
extreme enlargement of the parietal contour. The
vault development involves an opposite bending
with respect to the previous pattern, namely a
‘‘convolution’’ of the whole structure. The term
‘‘convolution’’ is used here not to describe an
increase of the cerebral gyriﬁcation, but to describe
a dorsal (parietal) growth that involves a globular-
isation process of the entire structure. While the
parietal enlarges, the temporo-cerebellar areas
approach the frontal poles. The extremities turn
downward by the action of the parietal pressure,
approaching each other with shortening of the
basal lengths and the development of a more
rounded morphology. The relative endocranial
length decreases, with relative shortening of the
frontal and occipital poles. The cerebellum is
pushed downward by this deformation.
A further note can be added regarding the
position of the Rolandic scissure. Generally, in
non-modern specimens the Rolandic scissure lies
behind the midpoint of the maximum length, and
the middle vault height (H2) crosses the proﬁle
approximately at the frontal ascending circumvo-
lution. In contrast, in modern humans the middle
height position approaches the Rolandic scissure,
or even lies behind it, at the ascending parietal
Paleoneurology generally has limitations be-
cause of the poor preservation of fossils, the low
prevalence of brain traces on the inner table, a very
small sample size, and the heterogeneous training
of the few scholars working on this issue (Hollo-
way, 1978). Metric tools in paleoneurology present
several additional challenges.
First, cerebral landmarks are seldom clearly
localisable, because of the ‘‘fuzzy’’ nature of the
whole structure. ‘‘Fuzzy landmarks’’ have been
deﬁned as ‘‘the position of a biological structure
that is precisely delineated, but occupies an area
that is larger than a single point in the observer’s
reference system’’ (Valeri et al., 1998). However,
a within-observer error test proved that the
uncertainty of fuzzy landmarks is limited and can
be reduced by experience; moreover, literature
studies report errors comparable with the values
reported in this analysis for the more localisable
landmarks (Valeri et al., 1998; Free et al., 2001).
Type I landmarks (biologically homologous)
are rare, and most of the suitable references can be
included in type II, such as points of maximum
curvature, projections or depths. Many of the
endocranial landmarks are often ‘‘hard Type II’’,
i.e. deﬁned by smooth surfaces or strongly de-
pendent on variables like the orientation of the
Fig. 4. PC1 values from a PCA including only the non-modern
specimens (ARCCNDR). The grids show the relative distor-
tion in the two opposite directions of the morphological vector.
290 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
specimen or even the handling of the surfaces.
Actually, both orientation and perspective play
a crucial role during the localisation of some
points. For the same reasons, there are few and
weak references available to build geometric
constructed landmarks, such as chords or projec-
tions. Asymmetries play an additional confound-
ing role, making landmarks and diameters
extremely dependent upon hemispheres and lead-
ing to easy misinterpretation of morphological
relationships. One of the consequences of hemi-
spheric asymmetry is the curvature of the in-
terhemispheric scissure, which is the only reference
available to localise the midsagittal plane. There-
fore, the only plane available to localise landmarks
and relative diameters is rather biased by the direct
or indirect inﬂuence of cerebral dominance.
Incompleteness of specimens, damage, subjec-
tivity of the reconstructions, and limits of mould-
ing techniques must be taken into account within
this context. Thus, a constant ‘‘anatomical un-
certainty’’ will necessarily be involved in any data
set, and any inference will necessarily be limited by
some sort of morphological doubt. Even the rare
type I landmarks are not immune from subjective
decisions. Points such as the Rolandic or the
transverse scissure at the midsagittal plane are
seldom easily recognised on an endocast, and
a certain degree of experience and ‘‘personal
intuition’’ is required. Moreover, they represent
the boundaries of some circumvolutions, and
therefore are often expressed not as points but as
areas, whose geometry shows a high inter-
individual variation. Experience can limit random
error (within-observer), but the results may be
inﬂuenced by a certain degree of systematic
Two more sources of biases must be considered.
First, the correspondence between endocranial and
brain morphology is not complete and univocal,
and the endocasts represent only a part of the
cerebral structures (Mannu, 1911; Kimbel, 1984;
Zollikofer and Ponce de Leo´ n, 2000). Second,
cranial capacity and brain size do not overlap
entirely, as cranial capacity includes a subarach-
noidal space of about 300 cc (see Pen˜ a-Melian,
2000). These biases are obviously related, with the
second being the main cause of the ﬁrst. Therefore,
much caution has to be used when inferences
about brain morphology are made from endocast
Fig. 5. a) UPGMA phenogram computed on the Procrustes distance matrix from the geometric morphometric analysis of the vault; b)
distortion grids showing the pair-wise comparison between averaged conﬁgurations after Bookstein superimposition (baseline: FP-
OP): ARC compared to MOD (top), and ARC compared to NDR (bottom). Reference shape (ARC) in bold.
291 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
analyses, which mainly describe the variation of
endocranial features and not the original cerebral
structures. All the noise generated by these
variables aﬀects the resolution power of the
paleoneurological approach, as well as any land-
mark-based analysis on cerebral living tissues
(Free et al., 2001). The control and consideration
of these properties represent the operational bases
of paleoneurology. Data must be calibrated on the
resolution power available, and results must be
discussed only on the basis of a robust approach,
taking into account the real numeric meaning of
physical diﬀerences. It must be remarked that the
methodological notes described in this context
should be considered not as limits of the approach,
but as a priori parameters of the models used in
this analysis. They represents limits when ignored,
confounding and producing noise in the results. In
contrast, they become intrinsic components of the
model if taken into account, improving the range
of available analysis. Clearly, a more complete
and resolute formalisation of brain geometry
must be one of the main future targets of paleon-
In this paper, univariate and bivariate metrics
and 2D geometric morphometrics generally sup-
port and improve the results obtained from
a multivariate interlandmark approach and 3D
analyses (Bruner et al., 2003). A comparison
between the two studies is useful to reinforce the
results considering the possible biases of the
paleoneurological approach. The data from 3D
analysis of the endocasts are largely based on type
I landmarks, related to a speciﬁc biological
meaning, but more scattered on the surface and
associated with a larger uncertainty related to the
exact localisation of the structures (e.g. the
perpendicular scissure). In contrast, the present
analysis is based largely on type III landmarks,
and a lateral projected bidimensional geometry.
Thus, information is not associated with speciﬁc
functions but simply with overall shape and
morphology. Furthermore, in the present paper
the complementary metrics from interlandmark
distances strengthen the results because they
contribute to a synthetic approach, including
information from the third dimension (frontal
and maximum widths), and considering the vault
morphology in terms of frontal and parietal
chords (type I-based landmarks) as well as
function-independent variables (type III-based
Considering the convergence of the results from
two- and three-dimensional approaches, the use of
both geometric and anatomical landmarks are
necessary to a full complementary discussion on
endocranial shape evolution.
Human brain evolution in the Middle Pleistocene
Figure 6 synthesises the major diﬀerences
between four indicative specimens, namely the
Sale´ conﬁguration (African Middle Pleistocene)
warped into Zhoukoudian III (Asian Middle
Pleistocene), La Chapelle-aux-Saints (European
Wurmian Neandertal) and Vatte di Zambana
(European Mesolithic modern human). They
represent just indicative morphotypes, and the
comparisons are not necessarily intended to be
phylogenetic representations. Sale´ is considered as
reference because of the general plesiomorph
endocranial (Holloway, 1981b) and ectocranial
(Hublin, 2002) morphology, associated with its
geographical localisation. The patterns of varia-
tion described in this analysis will be discussed
according to each main endocranial districts.
Frontal area. The frontal lobes have been
suggested to have a major role in human
evolution, because of an interesting development
in those morphotypes hypothesised to be the
earliest representatives of the genus Homo, and
formerly included in the hypodigm of Homo
habilis (Holloway, 1995; Tobias, 1995). In the
frontal lobes the coronal diameters increase in
the more derived taxa, mostly by means of the
development of the 3
(Grimaud-Herve´ , 1997). Actually, what seems
more interesting is the development of the frontal
width compared to the maximum (parieto-tempo-
ral) breadth. This ratio increases in larger endo-
casts, following an allometric pattern shared
within the whole genus. In larger hominids it leads
to an allometric expression and development of
the Broca’s cap, while in the opposite direction
leads to the typical frontal narrowing of the
292 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
Concerning the frontal vertical development,
the anterior midsagittal brain proﬁle has been
hypothesised to have undergone a long stasis since
the Middle Pleistocene, independently from the
large variations of the outer bony morphology
related to the brow ridge and associated structures
(Bookstein et al., 1999). The analyses of the
interlandmark and landmark data here show
a general size-related vault elevation, particularly
at the level of the ascending frontal circumvolu-
tion, with the archaic Asian specimens showing
more pronounced ﬂattening. This pattern is
combined with a backward shifting of the Rolan-
dic scissure, with consequent relative lengthening
of the frontal lobe. Comparable results were
obtained by superimposition of averaged three-
dimensional conﬁguration of the endocasts (Bru-
ner et al., 2003). Therefore, even if only some
minor variations are recorded in the frontal
proﬁle, its shape is nevertheless inﬂuenced by size
and by a generalised vertical stretching, and
absolute stasis is improbable considering the
encephalisation processes. Conversely it may be
stated that, if the frontal shape diﬀerences in
extinct human taxa are considered only as the
consequence of brain enlargement, it should be
possible to hypothesise an ‘‘allometric stasis’’, as
shape variations along a plesiomorph size-
dependent morphological trajectory. The term
‘‘allometric stasis’’ is used here to indicate
Fig. 6. Distortion grids showing diﬀerences in 2D left lateral conﬁguration between the hypothesised less derived phenotype (Sale´ )
towards three representative specimens (Zhoukoudian III, La Chapelle aux Saints, Vatte di Zambana), with a draw of the respective
endocasts. Note that this comparison is aimed at a description of the main morphotypes, and does not represent any phylogenetic
293 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
evolutionary changes mainly based on a non-
derived structural system, thus shape variations
without major neomorphic relationships. The
morphology changes, while the biological model
does not (at least concerning a large percentage of
variability). In any case, in modern humans the
generalised endocranial convolution involves a rel-
ative shortening of the frontal pole that reduces
the eﬀect of the allometric stretching. This result,
although secondarily induced by the parietal
development, must also be taken into account.
It should be emphasised that in this study the
Asian variability was included, and the frontal
area was entirely considered (until the Rolandic
scissure). In Bookstein et al. (1999) the Asian taxa
were not considered and only the shape of the
anterior cranial fossa was taken into account.
Therefore, in the present analysis the Asian
specimens may have increased the size-related
diﬀerences, which moreover may be situated more
at the frontal ascending circumvolutions than in
the prefrontal cortex housed in the anterior cranial
fossa. This volume is further reduced by the post-
orbital (backward) shifting of the frontal lobes in
some robust Middle Pleistocene specimens (Seidler
et al., 1997). Moreover, in previous work the inner
(endocranial) proﬁle was analysed together with
the outer (ectocranial) proﬁle (Bookstein et al.,
1999). Extreme variation in the latter proﬁle may
have obscured the more limited variation in the
It is worth noting that recent volumetric
analyses show a comparable development of the
frontal lobes in modern humans and apes,
considering their speciﬁc brain size (Semendeferi
et al., 1997; Semendeferi and Damasio, 2000),
suggesting an allometric stasis within the Homi-
noidea and supporting the hypothesis of a general-
ised evolutionary inertia of the frontal lobes. This
may diminish the importance of these areas during
human evolution compared to what has been
historically assumed. However, it cannot be
excluded that the trespassing of some size bound-
aries could have involved some discrete (emergent)
changes in neuro-functional organisation. Consid-
ering the role of the frontal circumvolutions in
higher cognitive functions and language, this
hypothesis needs to be thoroughly investigated.
Parietal area. There is some evidence suggesting
that changes in the parietal lobes can be involved
in the evolution of early hominids, considering the
information available on the Australopithecinae
endocasts (Holloway, 1983, 1995; Tobias, 1995).
The lower parietal areas are extremely variable in
extant Hominoidea, while the upper parietal
structures show wide variation in extinct hominids
(Holloway, 1981a). It seems than the parietal areas
maintained a key role in the subsequent radiation
of the genus Homo, particularly when modern
humans are considered and compared to the
extinct taxa. In general, the whole parietal and
temporo-parietal complex widens in diﬀerent
lineages as brain size enlarges, along with an
associated decrease of the occipital area (Grimaud-
Herve´ , 1997). All the taxa considered here show
a common pattern of size-related parieto-temporal
widening. In contrast, as the brain enlarges the
parietal outline shows a negative allometric
pattern, leading to a relative shortening of the
midsagittal proﬁle and ﬂattening of the upper-
posterior areas. The posterior height shows a size-
related vertical development of the vault along
a shared trajectory in the non-modern sample. The
high level of encephalisation of the Neandertals
exaggerates these patterns, with parietal areas high
and wide, but short and ﬂattened. It must be noted
that posterior height (H3) and parietal ﬂattening
are not fully comparable variables, and they
should not be confused. The parietal development
concerns shape, i.e. a more rounded or ﬂattened
outline, while its height concerns size, i.e. the
absolute elevation above the fronto-occipital
chord. Multivariate traditional metrics has been
used to characterise two diﬀerent morphological
trajectories based on this inverse relationship
between brain size and parietal structure, separat-
ing modern from non-modern specimens (Bruner
et al., 2003). As a result of relative parietal
shortening, the brain undergoes a generalised
dorsal bending as it enlarges, and the endocast is
It is useful to evaluate the relationship between
the inner and outer cranial surfaces, particularly
considering the ectocranial lambdoid ﬂattening of
Neandertals. The Neandertals ontogenetic trajec-
tory, compared with the pattern expressed in
294 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
modern humans, shows a relative development of
the lower-lateral neurocranial outer bones and
a relative reduction of the upper vault surfaces,
particularly at the parietal roof (Ponce de Leo` n and
Zollikofer, 2001). This pattern perfectly matches
the vertical development of the Neandertal brains
associated with a shortening of the parietal outline:
the ﬁrst process is related to lateral vertical
development, the second to the negative allometric
pattern of the upper parietal areas.
The allometric development and the midsagittal
parietal shortening lead to a parietal ‘‘dispropor-
tion’’: encephalisation involves increased parietal
widths and heights on the one hand, but parietal
longitudinal reduction and ﬂattening on the other.
It can be hypothesised that this pattern could lead
to some structural loss of balance in addition to
some functional constraints. This factors can be
included in the neural-processing limits related to
the neural architecture (Hofman, 2001). It is
interesting that some analyses of Neandertal
functional craniology revealed hypostotic traits
and ‘‘ontogenetic stress’’ of the posterior cranial
districts in these populations (Manzi et al., 1996,
2000a; Manzi, 2003), previously described as
‘‘morphological instability’’ of the Neandertal
parieto-occipital structures (Sergi, 1934, 1944,
1948). Taking into account the tight ontogenetic
and structural relationship between brain and
vault bones (Moss and Young, 1960; Enlow,
1990), these results must be carefully considered
within the hypotheses on the Neandertals evolu-
The modern endocasts show a pattern of
parieto-temporal widening similar to the non-
modern specimens. In contrast, the modern
morphotype is characterised by a species-speciﬁc
(actually autapomorphic) parietal development.
The parietal chord lengthens, and the midsagittal
proﬁle grows orthogonal to the outline. The
posterior vault elevation and the parietal longitu-
dinal development showed in this analysis are
associated with the upper parietal widening
characterising the modern ‘‘housed’’ posterior
proﬁle. The result of the parietal enlargement,
both midsagittally and coronally, is the develop-
ment of a more globular brain case. The parietal
growth involves the approaching of the opposite
areas, namely the temporo-cerebellar and the
frontal ones, with closing of the interposed gaps
(sylvian and temporal valleys). Here, this process
is termed convolution, and it leads to the species-
speciﬁc ‘‘globularity’’ of the ectocranial counter-
part characterising the modern human populations
(Manzi et al., 2000b; Lieberman et al., 2002;
Bruner et al., 2004).
It is worth noting that the previous three-
dimensional analysis of the endocranial extinct
variability was able to characterise the same
patterns, integrating the changes in the parietal
areas with those related to the endocranial widening
(Bruner et al., 2003). The present two-dimensional
approach was necessary to localise and describe the
upper bending of the vault, or conversely the actual
eﬀect of the surface convolution, because of the
lateral view projection associated with the use of
geometry-related type II landmarks.
Occipital area. The occipital lobes have been
hypothesised to show a steady reduction during
human evolution (Holloway, 1983, 1995), changing
from a more posterior location (behind the parietal
areas) to a more advanced position (under the
parietal structures), with the cerebellar poles fol-
lowing the same pattern (Grimaud-Herve´ , 1997).
This process involves a rotation of the posterior
complex forward and under the cerebral mass. The
metric analysis suggests only a size-related vertical
development, while the geometric morphometric
approach conﬁrms the ﬂattening of the occipital
structures onto the developing parieto-temporal
areas. The relative reduction of the most encephal-
ised taxa can explain the greater dominance of the
anterior branches of the middle meningeal vessels
(Grimaud-Herve´ , 1997) compared with the posteri-
or development of the vascular systemin the Middle
Pleistocene Asian hominids.
Human evolution and brain size
Brain size is surely the most well-known subject
in studies of human brain evolution. Presently,
there is no agreement on the dynamics of changes
in cranial capacity during the Middle Pleistocene.
After the evolution of the early Homo morpho-
types, a stasis may have occurred in the enceph-
alisation process, with limited brain size increase
295 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
until after 600 ka (Ruﬀ et al., 1997). The following
brain enlargement in diﬀerent human lineages led
gradually to brain sizes included in the non-
pathological lower values of the modern range
(Conroy et al., 2000). In contrast, although
a gradual increase of the cranial capacity is
reported for the (mostly Asian) Homo erectus
populations, there is some evidence of a discrete
transition to higher cranial capacity values in the
(mostly Afro-European) Homo heidelbergensis
lineage (Rightmire, 2003).
Independently from the degree of encephalisa-
tion as quantitative development of the cranial
capacity, the available data from the present
analyses strengthen and improve the character-
isation of two distinct allometric trajectories
described for the evolution of the human brain
(Bruner et al., 2003). It must stressed here that the
term trajectory is interpreted as a general size-
related shape change. Thus it is a structural
relation between cerebral shape and encephalisa-
tion. It is therefore not assumed to be ‘‘geometric’’
allometry (i.e. the analysis of the departure from
isometric scaling), and inferences concerning the
quantiﬁcation of these trajectories have not been
considered because of the small number of speci-
mens in each operational group. Furthermore,
trajectory is obviously not used here to imply
a progressive evolutionary process.
The vertical endocranial development (proba-
bly stressed at the level of frontal ascending
circumvolution), the frontal and temporal widen-
ing, and the occipital ﬂattening, represent common
size-related consequences shared within the genus
Homo. Conversely, the non-modern taxa are
characterised by a parietal shortening and ﬂatten-
ing, while the modern specimens show a derived
structural conﬁguration based on a parietal hy-
pertrophy involving a convolution of the endo-
Therefore, Neandertals are hypothesised to be
derived on the basis of the allometric expression
and the encephalisation degree (quantity), but
plesiomorphic on the basis of structural and
functional processes (quality). In any case, major
shared allometric trajectories do not exclude the
possibility of minor species-speciﬁc changes. It
must be noted that in Neandertals a certain degree
of parasagittal parietal development has been
described, shifting the tent-like posterior proﬁle
of Homo erectus and Homo heidelbergensis into the
classic en bombe outline (Bruner et al., 2003).
Other diﬀerences have been proposed as endocra-
nial autapomorphic features of the Neandertal
lineage, e.g. the high frequency of a well developed
spheno-parietal sinus (Gracia, 1991; Saban, 1995;
Arsuaga et al., 1997; Grimaud-Herve´ , 1997).
However, considering the presence of this trait in
the Indonesian and Zhoukoudian Homo erectus
(Grimaud-Herve´ , 1997) and the scaling relation-
ship between archaic groups and Neandertals, it
must be veriﬁed whether or not the expression of
this trace could be another result of the allometric
Concerning the variation in Homo sapiens,
some diﬀerences can occur between Late Pleisto-
cene and Holocene populations. Metric analyses
have shown that Upper Paleolithic modern hu-
mans display increased heights and lengths and
decreased widths with respect to recent endocrania
(Grimaud-Herve´ , 1997). These diﬀerences could be
interpreted in terms of the allometric trajectory of
the Holocene gracilisation and decrease of cranial
capacity (Henneberg, 1988; Holloway, 1995; Ruﬀ
et al., 1997), but further analyses must be
addressed to this issue.
Clearly, this study is limited to the endocranial
geometry, and the results must be interpreted in
terms of structural macroscopic pattern. No
information is available on the architecture of
the cerebral tissues, that can be just hypothesised
on neontological bases. For instance, it has been
suggested that hominid evolution may have been
related to a speciﬁc neocortical expansion more
than a general brain size increase, with departure
from the non-human allometric trajectories in
frontal and temporal white-matter development
(Rilling and Insel, 1999; Rilling and Seligman,
Brain evolution and functional morphology
The geometry of the brain should be interpreted
as the functional and structural result of a bio-
mechanical complex. Morphology is the ﬁnal
result of forces and intensities which originate
296 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
from the interactions between genetic programs
and the individual environment. Yet they develop
within a physical medium that is an active part of
the process by means of its mechanical constraints,
leading to the ﬁnal conﬁguration of the structures
(Thompson, 1942; Moss and Young, 1960). This
approach is the basis of a dynamic conception of
cranial morphology, in which evolution and
ontogeny can be interpreted as the products of
structural balances (Sergi, 1934, 1944; Enlow,
The endocranial cavity, formed by the cerebral
capsule, the skull base and the meninges, is
a functional matrix sensitive to the inﬂuence of
the growing soft tissues (Moss and Young, 1960).
The neural mass determines the force and magni-
tude of growth (quantity), while the skull base, the
dural layers and the endocranial tensors (falx
cerebri and tentorium cerebelli) represent vectors of
direction controlling the qualitative result (shape).
The vault bones show a passive growth mecha-
nism, in which bone deposition and resorption are
induced by the soft tissue stimulated by the brain
pressure and bone separation at the sutures
(Enlow, 1990). In contrast, the skull base compo-
nents and the three endocranial fossae grow
actively by drift, displacing the surrounding
splanchnocranial and basicranial structures. These
patterns of growth suggest possible explanations
for the allometric trends hypothesised in this
The frontal lobes seem to be more conservative
during hominid evolution with respect to other
cerebral districts. The vertical development is
limited, with the frontal areas growing mostly
laterally. There are at least two constraints to the
vertical development. First, the maximum loading
of the frontal lobes onto the orbital roofs may be
limited by their structural resistance. Second,
a general vertical development of the anterior
fossa leads to a downward rotation of the orbits,
of the nasomaxillary complex and of the olfactory
bulbs (Enlow, 1990). After a certain degree of
downward pushing, the process may reach a phys-
ical limit beyond which a further displacement of
the facial volume is not achievable. In contrast,
a lateral widening is possible because of the
extreme frontalisation of the genus Homo and
the marked splanchnocranial reduction. The ﬁrst
process advances the temporal fossa (Ross, 1995;
Ravosa et al., 2000), while the second reduces the
volume of the anterior temporal muscle (Cachel,
1978). Interestingly, recent genetic advances on
mutations of the myosin in apes and humans
support a similar evolutionary relationship be-
tween the temporal muscle and the neurocranial
development (Stedman et al., 2004).
As a consequence of the orbital frontalisation
and muzzle reduction, a large lateral volume is
available for frontal broadening of the brain,
presented in archaic hominids as the post-orbital
constriction and reduced in later taxa by widening
of the frontal lobes. Thus, the broadening of the
frontal lobes is the only mechanism that is able to
enlarge allometrically the frontal areas, given the
vertical constraints discussed above. The limits
related to the frontal height development and the
availability of lateral enlargement can thus be
regarded as compensatory processes. Hemispheric
specialisation is related to size via the positive
allometric increase in connectivity (Hofman,
2001). It will be interesting to test whether or not
the rate of the allometric frontal widening could
have represented a pre-adaptation to the hemi-
spheric specialisation at the third frontal circum-
Even if the frontal lobes were not involved in
major volumetric or morphological rearrange-
ments during human evolution, an increased
degree of its gyriﬁcation has been anyway sug-
gested (Rilling and Insel, 1999), and the respective
cognitive consequences are presently not known.
If the anterior endocranial areas may enlarge
mainly through a lateral widening, the posterior
volumes are more easily enlarged by a vertical
development. The maximum breadth of the cranial
base has been suggested to have the greatest
inﬂuence on the main cranial proportions (Lieber-
man et al., 2000). If a variable is associated with
a large number of secondary processes, the
necessity of functional coherence will preserve
the character from large deviations.
The parietal areas seem to have a major role in
the structural network of the human endocranial
system (Fig. 7). It has been suggested that as
cranial capacity increases the parietal areas
297 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
undergo to a relative shortening and ﬂattening,
except when modern humans are compared with
non-modern taxa (this work; Bruner et al., 2003).
The longitudinal main tensor of brain develop-
ment is the falx cerebri, a meningeal process
interposed between the two cerebral hemispheres.
As the brain enlarges, a basic allometric relation
describes a cubic cerebral volume increasing on
the quadratic meningeal sheet of the falx, or
even along its linear chord projection acting as
the real physical vector on the brain surface.
Considering the important structural role of
the falx cerebri, this process may easily involve
a loss of balance and may require some shape
The parietal lobes lie midway between the two
brain extremes, represented by the frontal and
occipital poles. Following the increase in brain
size, the anterior and posterior lobes are free to
rearrange by means of a diﬀerent orientation. In
contrast, the parietal area is constrained by its
middle position and cannot rearrange the allome-
tric pattern by an independent movement. As
a result, while the brain enlarges the falx cerebri
and other tensors cannot keep the pace with the
general growth, inducing a relative midsagittal
reduction. The overall eﬀect could be a parietal
midsagittal shortening and consequent ﬂattening,
with a cerebral upward bending related to the
tension at the frontal and occipital lobes. It must
be stressed that also during ontogeny the frontal,
temporal and inferior parietal areas undergo
a relative increase, while the occipital and superior
parietal districts show a relative stasis (see Pen˜ a-
The role of the cranial base ﬂexion within this
context is of major interest. The cranial base angle
has a determinant role in cerebral spatial packing
(Ross and Ravosa, 1993). Although its function in
human evolution seems to suggest other compen-
satory processes, at least in modern humans (Ross
and Henneberg, 1995; Jeﬀery and Spoor, 2002),
the role of this variable is not completely resolved
(Lieberman et al., 2000; McCarthy, 2001). The
dorsal bending and the parietal convolution pre-
viously described is likely to have some eﬀect on
the cranial base angle, and further analyses are
required to clarify this issue. Both processes should
aﬀect the cranial base variation in opposite
directions, the dorsal bending involving a more
platybasic structure, and the parietal convolution
inducing klinorhynchy. The same convolution
process aﬀected and rearranged the vertical de-
velopment. A similar scenario to this parietal
Fig. 7. Structural hypotheses on two encephalisation trajectories. Endocranial capacity increases independently in modern humans
(top) and Neandertals (bottom). The ﬁrst process is based upon a neomorphic structural change related to a parietal hypertrophy. The
second is largely based upon the quantitative development of an archaic pattern. The distortion grids show the warp from the mean
archaic shape (here represented by the Sale´ endocast) to the mean modern and Neandertal conﬁgurations (x 1.6).
298 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
scaling hypothesis was proposed by Strait (1999)
to be a main factor involved in cranial base ﬂexion,
on the basis of the non-cortical brain properties.
The ‘‘non-cortical scaling hypothesis’’ suggests
a soft tissue constraint related to the negative
allometric pattern of the medullar, mesencephalic
and diencephalic structures, eventually related to
metabolic requirements. Regardless of the causal
nexus between parietal bone development, bio-
mechanical tensors, brain tissues and cranial base
ﬂexion, it is clear that they represent an integrated
system within a functional network.
During anthropoid brain evolution the neo-
cortical white matter has scaled at a higher power
than the grey matter (Rilling and Insel, 1999;
Hofman, 2001). Thus, the number of connections
(axons) outpaced the number of neocortical
neurons as the brain enlarged. Functionally, this
can be interpreted as an increase of information
exchange that is faster than the increase of the
information itself. It is worth noting that the
increased spherical shape in modern populations
further increased the connectivity of the brain’s
neuronal network by the shortening of the
distances between the diﬀerent districts. In a system
that processes thousands of bits of information
every few microseconds, a minor increase in ﬂow
eﬃciency can induce an exponential advantage by
mean of a decrease of the ‘‘wiring length’’ (see also
Parietal development in modern humans must
be integrated within a theory of localised cells
proliferation. According to the radial unit hypoth-
esis (see Rakic and Kornack, 2001) such pro-
liferation is related to an increase of the source
cells at the ventricular zone. Recent advances on
the genetic control of cortical folding have been
based on a group of pathologies generally de-
scribed as polymicrogyria (Rakic, 2004). These
analyses suggest that even single mutations can
involve marked and discrete changes in the
structural organisation of speciﬁc functional areas
of the cortical layers. Consequently, random and
localised genomic changes can induce a regional
cortical development by addition of radial units,
promoting fast and localised evolutionary events.
The development of the parietal areas with
relative adjustment of the overall brain morphol-
ogy and increase of connectivity also ﬁts well
within the tension-based theory of brain morpho-
genesis (Van Essen, 1997). This hypothesis sug-
gests that during neural morphogenesis the
physical tension of the neural structures (axons,
dendrites and glial processes) produces mechanical
forces that guide the shape development and
‘‘compact wiring’’ of the brain. As in the relation-
ship with physical tensors represented by the falx
cerebri and tentorium cerebelli, the magnitude of
the process is again based upon the hydrostatic
pressure produced by brain enlargement. Two
alternative inferences may follow. First, the
modern parietal development and the conse-
quently more spherical brain shape may have
increased the compact wiring eﬃciency. If so, the
parietal functional development should then be
regarded as the major force promoting the change
of brain morphology. On the other hand, some
rearrangements based on the functional biome-
chanics of the neural tensors may have involved
a necessary parietal adjustment. In that case,
parietal development was not a direct adaptation
but a consequence of other changes. According to
either explanation, and considering the multifac-
torial functions related to parietal development, it
is likely that the shift from the non-modern
allometric trajectory and the resulting enhance-
ment of the parietal lobes had cognitive con-
sequences. In other words, results presented here
suggest that the parietal development in modern
humans is the only non-allometric diﬀerence
between Homo sapiens and non-modern taxa,
and this morphological change probably may have
represented a discrete cognitive shift.
The parietal cortex may have had a principal
role during hominid evolution through its direct
relationship with visuospatial integration, sensory
integration, multimodal processing, and social
communication (Holloway, 1995; Faillenot et al.,
1999). The parietal lobes are involved in the
control of ﬁnger movements during spatial anal-
ysis (Shibata and Ioannides, 2001) and in turn act
on cognitive tasks and association processes
(Culham and Kanwisher, 2001). It is interesting
that the parietal districts seem to be crucial in
manipulation and planning of motor sequences
because this suggests a role in tool-making. In this
299 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
perspective, it is likely that the discrete qualitative
development of operational objects displayed in
the Late Pleistocene by modern humans was
related to such a structural transformation. In
addition, hypotheses about the evolution of
language have been based on a comparison
between speech and tool-making activity, both
represented by the modular organisation of motor
sequences (see Bradshaw, 1997). In 1973 Konrad
Lorenz interpreted the roots of the conceptual
thinking by means of ﬁve variables: together with
abstraction, curiosity, voluntary movement, and
imitation, he listed the spatial orientation (Lorenz,
1973). In particular, he referred to the potentiality
to create an ‘‘imagined space’’ interior to the
central nervous system. This space works as
a model to act virtually within an environment
by means of the thought, and it is supposed to
represent a basic foundation of any conceptual
operation, including language. Considering the
hypothesised role of the parietal areas in visuo-
spatial integration as recognition and communi-
cation of the external environment, the evolution
of these structures may be directly related to the
evolution of such ‘‘inner reality’’.
Finally, by means of the parietal expansion the
modern human brain acquired a more globular
shape, and the relative decrease of the cerebral
surface area with respect to brain volume is
directly related to thermoregulation and metabolic
budget, and secondarily to diet and behaviour
(Leonard and Robertson, 1992, 1994, 1997; Aiello
and Wheeler, 1995; Kaplan et al., 2000; Leonard
et al., 2003).
Although the present analysis suggests a major
role of the parietal areas during human brain
evolution, it must be stressed that other cerebral
districts - e.g. the temporal and the cerebellar
structures - are more diﬃcult to consider in the
fossil record but provide interesting perspectives
for future studies (see Semendeferi, 2001; Weaver,
2002). For human brain evolution, the structural
and functional morphology can be interpreted as
a single and complex ‘‘phylogenetic package’’
(Enlow, 1990). The neuro-functional consequences
of the development of speciﬁc cortical areas and
the change in spatial organisation between diﬀer-
ent districts, and possibly of metabolism, suggest
that a discrete cognitive shift between non-modern
and modern humans cannot be excluded.
I am sincerely grateful to Giorgio Manzi, who
was a constant reference during this project. Juan
Luis Arsuaga, Patricio Dominguez, and Ana
Gracia gave me the opportunity to begin this
work with useful suggestions and help. Henry and
Marie-Antoinette de Lumley, and Aldo and
Eugenia Segre, allowed the study of most of the
specimens. Dominique Grimaud-Herve´ was the
precious teacher who introduced me to paleoneur-
ology. Dennis Slice had the patience to help me
every time I got entangled with multivariate
questions. Bernard Wood and Fabio di Vincenzo
furnished interesting cues. Christoph Zollikofer
and Charles Lockwood provided many useful
comments during the review process. Two anon-
ymous reviewers supplied important advice and
helped to consider a wide and varied literature.
Maryanne Tafuri helped in the ﬁnal linguistic
revision. This project was carried out at the
Laboratory of Human Paleontology directed by
P. Passarello at the Universita` ‘‘La Sapienza’’,
Roma. This work was partly supported by the
Italian MIUR/urst (including COFIN grants).
Aboitiz, F., Garcia, R., 1997. The anatomy of language
revisited. Biol. Res. 30, 171e183.
Aiello, L., Wheeler, P., 1995. The expensive-tissue hypothesis.
Curr. Anthrop. 36, 199e221.
Arsuaga, J.L., Martı´ nez, I., Gracia, A., Lorenzo, C., 1997. The
Sima de los Huesos crania (Sierra de Atapuerca, Spain). A
comparative study. J. Hum. Evol. 33, 219e281.
Begun, D., Walker, A., 1993. The endocast. In: Walker, A.,
Leakey, R. (Eds.), The Nariokotome Homo erectus skeleton.
Springer-Verlag, Berlin, pp. 326e358.
Bookstein, F.L., 1989. Principal warps: thin-plate spline and the
decomposition of deformations. I.E.E.E. Trans. Pattern
Anal. Machine Intelligence 11, 567e585.
Bookstein, F.L., 1991. Morphometric tools for landmark data.
Cambridge University Press, Cambridge.
Bookstein, F., Schafer, K., Prossinger, H., Seidler, H., Fieder,
M., Stringer, C., Weber, G.W., Arsuaga, J.L., Slice, D.E.,
300 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
Rohlf, F.J., Recheis, W., Mariam, A.J., Marcus, L.F., 1999.
Comparing frontal cranial proﬁles in archaic and modern
Homo by morphometric analysis. Anat. Rec. 257, 217e224.
Bradshaw, J.L., 1997. Human evolution. A neuropsychological
perspective. Taylor and Francis, London.
Bruner, E., 2003a. Fossil traces of the human thought:
paleoneurology and the evolution of the genus Homo.
Rivista di Antropologia 81, 29e56.
Bruner, E., 2003b. Computer tomography and paleoneurology:
the Saccopastore Neandertals and brain evolution in the
European Middle Pleistocene. PhD Thesis. University La
Bruner, E., Manzi, G., Passarello, P., 2002. The ‘‘Virtual’’ endo-
cast of Saccopastore 1. General morphology and preliminary
comparisons by geometric morphometrics. In: Mafart, B.,
Delingette, H. (Eds.), Three-Dimensional Imaging in Paleo-
anthropology and Prehistoric Archaeology, British Archeol.
Records IS 1049. Archeopress, Oxford, pp. 17e24.
Bruner, E., Manzi, G., Arsuaga, J.L., 2003. Encephalization
and allometric trajectories in the genus Homo: evidence
from the Neandertal and modern lineges. Proc. Natl. Acad.
Sci. USA 100, 15335e15340.
Bruner, E., Saracino, B., Passarello, P., Ricci, F., Tafuri, M.,
Manzi, G., 2004. Midsagittal cranial shape variation in the
genus Homo by geometric morphometrics. Coll. Antropol.
Cachel, S.M., 1978. A functional analysis of the primate
masticatory system and the origin of the anthropid post-
orbital septum. Am. J. Phys. Anthrop. 50, 1e17.
Cantalupo, C., Hopkins, W.D., 2001. Asymmetric Broca’s area
in great apes. Nature 414, 505.
Condemi, S., 1992. Les Hommes Fossiles de Saccopastore et
leur Relations Phyloge´ ne´ tiques. CNRS, Paris.
Conroy, G., Weber, G., Seidler, H., Recheis, W., Zur Nedden,
D., Mariam, J.H., 2000. Endocranial capacity of the Bodo
cranium determined from three-dimensional computed
tomography. Am. J. Phys. Anthrop. 113, 111e118.
Corrain, C., Graziati, G., Leonardi, P., 1976. La sepoltura
epipaleolitica nel riparo di Vatte di Zambana (Trento).
Preistoria Alpina 12, 175e212.
Culham, J.C., Kanwisher, N.G., 2001. Neuroimaging of
cognitive functions in human parietal cortex. Curr. Opin.
Neurobiol. 11, 157e163.
Enlow, D.H., 1990. Facial Growth. WB Saunders Company,
Faillenot, I., Decety, J., Jeannerod, M., 1999. Human brain
activity related to the perception of spatial features of
objects. Neuroimage 10, 114e124.
Falk, D., 1986. Endocranial casts and their signiﬁcance for
primate brain evolution. In: Swindler, D.R., Erwin, J. (Eds.),
Comparative Primate Biology Vol. 1: Systematics, Evolu-
tion, and Anatomy. Alan R. Riss, New York, pp. 477e490.
Falk, D., 1987. Hominid paleoneurology. Ann. Rev. Anthrop.
Falk, D., 1993. Meningeal arterial patterns in great apes:
implications for hominid vascular evolution. Am. J. Phys.
Anthrop. 92, 81e97.
Falk, D., Redmond Jr., J.C., Guyer, J., Conroy, C., Recheis,
W., Weber, G.W., Seidler, H., 2000. Early hominid brain
evolution: a new look at old endocasts. J. Hum. Evol. 38,
Felsenstein, J., 1989. PHYLIP: Phylogeny Inference Package
3.2. Cladistics 5, 164e166.
Free, S.L., O’Higgins, P., Maudgil, D.D., Dryden, I.L.,
Lemieux, L., Fish, D.R., Shorvon, S.D., 2001. Landmark-
based morphometrics of the normal adult brain using MRI.
Neuroimage 13, 801e813.
Gracia, A., 1991. Impresiones endocraneales del hombre de
lbeas. In: Rebato, E., Caldero´ n, R. (Eds.), VI Congreso
de Antropologı´ a. Universidad del Paı´ s Vasco, Bilbao, pp.
Grimaud-Herve´ , D., 1997. L’e´volution de l’enche´phale chez
Homo erectus et Homo sapiens. CNRS Editions, Paris.
Henneberg, M., 1988. Decrease of human skull size in the
Holocene. Hum. Biol. 60, 395e405.
Hofman, M.A., 2001. Brain evolution in hominids: are we at
the end of the road? In: Falk, D., Gibson, K.R. (Eds.),
Evolutionary Anatomy of the Primate Cerebral Cortex.
Cambridge University Press, Cambridge, pp. 113e127.
Holloway, R.L., 1978. The relevance of endocasts for studying
primate brain evolution. In: Noback, C.R. (Ed.), Sensory
Systems of Primates. PlenumPress, NewYork, pp. 181e200.
Holloway, R.L., 1980. Indonesian ‘‘Solo’’ (Ngandong) endo-
cranial reconstructions: some preliminary observations and
comparisons with neandertal and Homo erectus group. Am.
J. Phys. Anthrop. 553, 285e295.
Holloway, R.L., 1981a. Exploring the dorsal surface of
hominoid brain endocasts by stereoplotter and discriminant
analysis. Phil. Trans. R. Soc. Lond. B 393, 155e166.
Holloway, R.L., 1981b. Volumetric and asimmetry determi-
nations on recent hominid endocasts: Spy I and Spy II,
Djebel Ihroud I, and the Sale´ Homo erectus specimen. With
some notes on Neandertal brain size. Am. J. Phys. Anthrop.
Holloway, R.L., 1983. Cerebral brain endocast pattern of
Australopithecus afarensis hominid. Nature 303, 420e422.
Holloway, R.L., 1995. Towarda synthetic theory of humanbrain
evolution. In: Changeaux, J.P., Chavaillon, J. (Eds.), Origins
of the Human Brain. Clarendon Press, Oxford, pp. 42e54.
Holloway, R.L., De La Costelareymondie, M.C., 1982. Brain
endocast asymmetry in pongids and hominids: some
preliminary ﬁndings on the paleontology of cerebral
dominance. Am. J. Phys. Anthrop. 58, 101e110.
Hublin, J.J., 2002. Northwestern African Middle Pleistocene
hominids and their bearing on the emergence of Homo
sapiens. In: Barham, L., Robson-Brown, K. (Eds.), Human
Roots, Africa and Asia in the Middle Pleistocene. CHER-
UB, Bristol, pp. 99e121.
Jeﬀery, N., Spoor, F., 2002. Brain size and the human cranial
base: a prenatal perspective. Am. J. Phys. Anthrop. 118,
Kaplan, H., Hill, K., Lancaster, J., Hurtado, A.M., 2000. A
theory of human life history evolution: diet, intelligence,
and longevity. Evol. Anthropol. 9, 156e183.
301 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
Kimbel, W.H., 1984. Variation in the pattern of cranial venous
sinuses and hominid phylogeny. Am. J. Phys. Anthrop 63,
Legendre, P. (2001). Model II regression. De´ partement de
sciences biologiques, Universite´ de Montre´ al.
Legendre, P., Legendre, L., 1998. Numerical Ecology. Elsevier
Le May, M., 1976. Morphological cerebral asymmetries of
modern man, fossil man, and nonhuman primates. Ann.
NY Acad. Sci. 280, 349e366.
Leonard, W.R., Robertson, M.L., 1992. Nutritional require-
ments and human evolution : a bioenergetics model. Am. J.
Hum. Biol. 4, 179e195.
Leonard, W.R., Robertson, M.L., 1994. Evolutionary perspec-
tive on human nutrition: the inﬂuence of brain and body
size on diet and metabolism. Am. J. Hum. Biol. 6, 77e88.
Leonard, W.R., Robertson, M.L., 1997. Comparative primate
energetics and hominid evolution. Am. J. Phys. Anthrop.
Leonard, W.R., Robertson, M.L., Snodgrass, J.J., Kuzawa,
C.W., 2003. Metabolic correlates of hominid brain evolu-
tion. Comp. Bioch. Physiol. Part A 136, 5e15.
Lieberman, D.E., Pearson, O.M., Mowbray, K.M., 2000.
Basicranial inﬂuence on overall cranial shape. J. Hum.
Evol. 38, 291e315.
Lieberman, D.E., Mc Bratney, B.M., Krovitz, G., 2002. The
evolution and development of cranial form in Homo
sapiens. Proc. Nat. Acad. Sci. USA 99, 1134e1139.
Lorenz, K., 1973. Die Ru¨ ckseite des Spiegels. R. Piper and Co.
Verlag, Mu¨ nchen.
Mannu, A., 1911. A proposito delle variazioni delle doccie dei
seni venosi occipitali. Rivista di Antropologia XVI,
Manzi, G., 2003. ‘‘Epigenetic’’ cranial traits, Neandertals and
the origin of Homo sapiens. Rivista di Antropologia 81,
Manzi, G., Vienna, A., Hauser, G., 1996. Developmental stress
and cranial hypostosis by epigenetic trait occurrence and
distribution: an exploratory study on the Italian Neander-
tals. J. Hum. Evol. 30, 511e527.
Manzi, G., Gracia, A., Arsuaga, J.L., 2000a. Cranial discrete
traits in the Middle Pleistocene humans from Sima de los
Huesos (Sierra de Atapuerca, Spain). Does hypostosis
represent any increase in ‘‘ontogenetic stress’’ along the
Neanderthal lineage? J. Hum. Evol. 38, 425e446.
Manzi, G., Saracino, B., Bruner, E., Passarello, P., 2000b.
Geometric morphometric analysis of mid-sagittal cranial
proﬁles in Neandertals, modern humans, and their ances-
tors. Rivista di Antropologia 78, 193e204.
Marcus, L.F., Bello, E., Garcı` a-Valdecasas, A., 1993. Contri-
bution To Morphometrics. Museo Nacional de Ciencias
Marcus, L.F., Corti, M., Loy, A., Naylor, G.J.P., Slice, D.E.,
1996. Advances in Morphometrics. Plenum Press, New
Martin, R.D., Barbour, A.D., 1989. Aspects of line-ﬁtting in
bivariate allometric analyses. Folia Primatol. 53, 65e81.
McCarthy, R.C., 2001. Anthropoid cranial base architecture
and scaling relationships. Hum. Evol. 40, 41e66.
Moss, M.L., Young, R.W., 1960. A functional approach to
craniology. Am. J. Phys. Anthrop. 18, 281e292.
Newell, R.R., Constandse-Westermann, T.S., Meiklejohn, C.,
1979. The skeletal remains of mesolithic man in western
Europe: an evaluative catalogue. J. Hum. Evol. 8.
Page, R.D.M., 1996. TREEVIEW: an application to display
phylogenetic trees on personal computer. Comput. Appl.
Biosci. 12, 357e358.
Penin, X. (2000). Applied Procrustes Software 2.3.
Pen˜ a-Melian, A., 2000. Development of human brain. Hum.
Evol. 15, 99e112.
Ponce de Leo` n, M.S., Zollikofer, C.P.E., 2001. Neanderthal
cranial ontogeny and its implications for late hominid
diversity. Nature 412, 534e538.
Rakic, P., Kornack, D.R., 2001. Neocortical expansion and
elaboration during primate evolution: a view from neuro-
embriology. In: Falk, D., Gibson, K.R. (Eds.), Evolution-
ary Anatomy of the Primate Cerebral Cortex. Cambridge
University Press, Cambridge, pp. 30e56.
Rakic, P., 2004. Genetic control of cortical convolutions.
Science 303, 1983e1984.
Ravosa, M.J., Noble, V.E., Hylander, W.L., Johnson, K.R.,
Kowalski, E.M., 2000. Masticatory stress, orbital orienta-
tion and the evolution of the primate postorbital bar.
J. Hum. Evol. 38, 667e693.
Richtsmeier, J.T., Deleon, V.B., Lele, S.R., 2002. The promise
of geometric morphometrics. Y. Phys. Anthropol. 45,
Rightmire, G.P., 2003. Brain size and encephalization in early
to Mid-Pleistocene Homo. Am. J. Phys. Anthrop. (in press).
Rilling, J.K., Insel, T.R., 1999. The primate neocortex in
comparative perspective using magnetic resonance imaging.
J. Hum. Evol. 37, 191e223.
Rilling, J.K., Seligman, R.A., 2002. A quantitative morpho-
metric comparative analysis of the primate temporal lobe. J.
Hum. Evol. 42, 505e533.
Rohlf, F.J., 1998a. tpsDig 1.2. Ecology and Evolution. SUNY
at Stony Brook, NY.
Rohlf, F.J., 1998b. tpsRelw 1.18. Ecology and Evolution.
SUNY at Stony Brook, NY.
Rohlf, F.J., 1998c. tpsSmall 1.19. Ecology and Evolution.
SUNY at Stony Brook, NY.
Rohlf, F.J., Bookstein, F.L. (Eds.), 1990. Proceedings of the
Michigan Morphometrics Workshop. University of Michigan
Museum of Zoology.
Rohlf, F.J., 2003. Bias and error in estimates of mean shape in
geometric morphometrics. J. Hum. Evol. 44, 665e683.
Rohlf, F.J., Marcus, L.F., 1993. A revolution in morphomet-
rics. Trends Ecol. Evol. 8, 129e132.
Ross, C.F., 1995. Allometric and functional inﬂuences on
primate orbit orientation and the origins of the Anthro-
poidea. J. Hum. Evol. 29, 201e227.
Ross, C.F., Ravosa, M.J., 1993. Basicranial ﬂexion, relative
brain size and facial kyphosis in nonhuman primates. Am. J.
Phys. Anthrop. 91, 305e324.
302 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
Ross, C., Henneberg, M., 1995. Basicranial ﬂexion, relative
brain size, and facial kyphosis in Homo sapiens and some
fossil hominids. Am. J. Phys. Anthrop. 98, 575e593.
Ruﬀ, C.B., Trinkaus, E., Holliday, T.W., 1997. Body mass
and encephalization in Pleistocene Homo. Nature 387,
Saban, R., 1995. Image of the human fossil brain: endocranial
casts and meningeal vessels in young and adult subjects. In:
Changeaux, P., Chavaillon, J. (Eds.), Origins of the Human
Brain. Clarendon Press, Oxford, pp. 11e38.
Seidler, H., Falk, D., Stringer, C., Wilﬁng, H., Muller, G.B.,
zur Nedden, D., Weber, G.W., Reicheis, W., Arsuaga, J.L.,
1997. A comparative study of stereolithographically mod-
elled skulls of Petralona and Broken Hill: implications for
future studies of Middle Pleistocene hominid evolution. J.
Hum. Evol. 33, 691e703.
Semendeferi, K., 2001. Advances in the study of hominoid
brain evolution: magnetic resonance imaging (MRI)
and 3-D reconstruction. In: Falk, D., Gibson, K.R.
(Eds.), Evolutionary Anatomy of the Primate Cerebral
Cortex. Cambridge University Press, Cambridge, pp.
Semendeferi, K., Damasio, H., Frank, R., Van Hoesen, G.W.,
1997. The evolution of the frontal lobes: a volumetric
analysis based on three-dimensional reconstructions of
magnetic resonance scans of human and ape brains.
J. Hum. Evol. 32, 375e388.
Semendeferi, K., Damasio, H., 2000. The brain and its main
anatomical subdivisions in living hominoids using magnetic
resonance imaging. J. Hum. Evol. 38, 317e332.
Sergi, S., 1934. Ossicini fontanellari della regione del lambda nel
cranio di Saccopastore e nei crani neandertaliani. Rivista di
Antropologia 30, 101e112.
Sergi, S., 1944. Craniometria e craniograﬁa del primo
paleantropo di Saccopastore. Ricerche di Morfologia 20-
Sergi, S., 1948. L’uomo di Saccopastore. Paleontographia
Italica XLII, 25e164.
Shibata, T., Ioannides, A.A., 2001. Contribution of the human
superior parietal lobule to spatial selection process: an
MEG study. Brain Res. 897, 164e168.
Slice, D., 2000. Morpheus et al. Ecology and Evolution. SUNY
at Stony Brook, NY.
Smith, G.R., 1990. Homology in morphometrics and phyloge-
netics. In: Rohlf, F.J., Bookstein, F.L. (Eds.), Proceedings
of the Michigan Morphometrics Workshop. University of
Michigan Museum of Zoology, pp. 325e338.
Stedman, H.H., Kozyak, B.W., Nelson, A., Thesier, D.M., Su,
L.T., Low, D.W., Bridges, C.R., Shrager, J.B., Minugh-
Purvis, N., Mitchell, M.A., 2004. Myosin gene mutation
correlates with anatomical changes in the human lineage.
Nature 428, 415e418.
Strait, D.S., 1999. The scaling of basicranial ﬂexion and length.
J. Hum. Evol. 37, 701e719.
Thompson, D’A.W., 1942. On Growth and Form. Cambridge
University Press, Cambridge.
Tobias, P.V., 1995. The brain of the ﬁrst hominids. In:
Changeaux, J.P., Chavaillon, J. (Eds.), Origins of the
Human Brain. Clarendon Press, Oxford, pp. 61e83.
Valeri, C.J., Cole 3rd, T.M., Lele, S., Richtsmeier, J.T., 1998.
Capturing data from three-dimensional surfaces using fuzzy
landmarks. Am. J. Phys. Anthrop. 107, 113e124.
Van Essen, D.C., 1997. A tension-based theory of morphogen-
esis and compact wiring in the central nervous system.
Nature 385, 313e318.
Weaver, A., 2002. Relative cerebellar and cerebral hemisphere
volume in Pliocene and Pleistocene Homo: a complex
trajectory. J. Hum. Evol. 42, A38.
Zollikofer, C.P.E., Ponce de Leo´ n, M.S., 2000. The brain and
its case: computer based case studies on the relation between
software and hardware in living and fossil hominid skulls.
In: Tobias, P.V., Raath, M.A., Moggi-Cecchi, J., Doyle,
G.A. (Eds.), Humanity from African Naissance to
Coming Millenia. Firenze University Press e Witwaters-
rand University Press, Firenze and Johannesburg, pp.
303 E. Bruner / Journal of Human Evolution 47 (2004) 279e303
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