Journal of Human Evolution 126 (2019) 112e123
Contents lists available at ScienceDirect
Journal of Human Evolution
journal homepage: www.elsevier.com/locate/jhevol
The endocast of StW 573 (“Little Foot”) and hominin brain evolution
lie Beaudet a, b, *, Ronald J. Clarke c, Edwin J. de Jager b, Laurent Bruxelles a, d, e,
Ame
Kristian J. Carlson c, f, Robin Crompton g, h, Frikkie de Beer i, Jelle Dhaene j,
Jason L. Heaton c, k, Kudakwashe Jakata c, Tea Jashashvili c, l, m, Kathleen Kuman a,
Juliet McClymont n, Travis R. Pickering c, o, Dominic Stratford a
a
School of Geography, Archaeology and Environmental Studies, University of the Witwatersrand, Private Bag 3, Johannesburg, WITS 2050, South Africa
Department of Anatomy, University of Pretoria, PO Box 2034, Pretoria 0001, South Africa
Evolutionary Studies Institute, University of the Witwatersrand, Private Bag 3, Johannesburg, WITS 2050, South Africa
d
French National Institute for Preventive Archaeological Researches (INRAP), Nîmes, France
e
French Institute of South Africa (IFAS), USR 3336 CNRS, Johannesburg 2001, South Africa
f
Department of Integrative Anatomical Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, United States
g
Department of Musculoskeletal Biology, Institute of Ageing and Chronic Disease, University of Liverpool, Liverpool L7 8TX, United Kingdom
h
Department of Rheumatology, Aintree University NHS Trust, Liverpool L9 7AL, UK
i
South African Nuclear Energy Corporation SOC Ltd. (Necsa), Pelindaba, North West Province, South Africa
j
UGCT Department of Physics and Astronomy, Ghent University, Proeftuinstraat 86/N12, B-9000 Gent, Belgium
k
Department of Biology, Birmingham-Southern College, Birmingham, AL, 35254, United States
l
Molecular Imaging Center, Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, United States
m
Department of Geology and Paleontology, Georgian National Museum, Tbilisi 0105, Georgia
n
School of Health Sciences, Aldro Building, University of Brighton, Eastbourne, United Kingdom
o
Department of Anthropology, University of Wisconsin, Madison, WI, 53706, USA
b
c
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 7 August 2018
Accepted 12 November 2018
One of the most crucial debates in human paleoneurology concerns the timing and mode of the
emergence of the derived cerebral features in the hominin fossil record. Given its exceptional degree
of preservation and geological age (i.e., 3.67 Ma), StW 573 (‘Little Foot’) has the potential to shed new
light on hominin brain evolution. Here we present the first detailed comparative description of the
external neuroanatomy of StW 573. The endocast was virtually reconstructed and compared to ten
southern African hominin specimens from Makapansgat, Malapa, Sterkfontein and Swartkrans
attributed to Australopithecus and Paranthropus. We apply an automatic method for the detection of
sulcal and vascular imprints. The endocranial surface of StW 573 is crushed and plastically deformed
in a number of locations. The uncorrected and therefore minimum cranial capacity estimate is
408 cm3 and plots at the lower end of Australopithecus variation. The endocast of StW 573 approximates the rostrocaudally elongated and dorsoventrally flattened endocranial shape seen in
Australopithecus and displays a distinct left occipital petalia. StW 573 and the comparative early
hominin specimens share a similar sulcal pattern in the inferior region of the frontal lobes that also
resembles the pattern observed in extant chimpanzees. The presumed lunate sulcus in StW 573 is
located above the sigmoid sinus, as in extant chimpanzees, while it is more caudally positioned in SK
1585 and StW 505. The middle branch of the middle meningeal vessels derives from the anterior
branch, as in MH 1, MLD 37/38, StW 578. Overall, the cortical anatomy of StW 573 displays a less
derived condition compared to the late Pliocene/early Pleistocene southern African hominins (e.g.,
StW 505, SK 1585).
© 2018 Elsevier Ltd. All rights reserved.
Keywords:
Australopithecus
sulcal pattern
Middle meningeal vessels
Pliocene
Sterkfontein
* Corresponding author.
E-mail address: beaudet.amelie@gmail.com (A. Beaudet).
https://doi.org/10.1016/j.jhevol.2018.11.009
0047-2484/© 2018 Elsevier Ltd. All rights reserved.
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
1. Introduction
One of the most critical questions in human paleoneurology
concerns the timing of the emergence of derived cerebral features
within the hominin1 clade. The assessment of a reliable chronological framework for the evolution of the human brain is essential
for discussing the process of cerebral changes. In particular, investigations of the palaeontological record, comparative neuroanatomy of extant mammals, and quantitative genetic analyses
have converged on two distinct models, i.e., mosaic-like, and
concerted evolution models (Finlay and Darlington, 1995; Barton
and Harvey, 2000; de Winter and Oxnard, 2001; Holloway, 2001;
Oxnard, 2004; Falk, 2009; Hager et al., 2012; Smaers and Soligo,
mez-Robles et al., 2014). While the mosaic-like pattern
2013; Go
of evolution suggests independent evolutionary trajectories of cerebral structures (e.g., Barton and Harvey, 2000; de Winter and
Oxnard, 2001; Holloway, 2001; Oxnard, 2004; Smaers and Soligo,
2013), a concerted pattern of evolution involves a global reorganization of the brain (e.g., Finlay and Darlington, 1995; Falk, 2009).
As the earliest representatives of Homo have been suggested to
display neuroanatomical structural features commonly regarded as
typical of extant humans (e.g., Tobias, 1987; Falk, 1983a;
Schoenemann, 2013 [in spite of later changes in morphology of
the human endocast, Neubauer et al., 2018]), evidence for such
changes in the brain and associated evolutionary patterns must be
sought earlier in the hominin fossil record.
In particular, three cerebral regions have been the focus of major
interest for addressing the question of timing and process of
evolutionary changes in the early hominin cerebrum (see review in
de Sousa and Cunha [2012]). Because of its roles in executive
functions and language (e.g., Kringelbach and Rolls, 2004; Keller
et al., 2009), the prefrontal cortex has been extensively investigated in human paleoneurology. Indeed, the inferior frontal gyrus
in Australopithecus has long been suggested to be similar to that
seen in extant chimpanzees because of the presence of a frontoorbital sulcus (see review in Falk, 2014). However, the possibility
that early structural changes in this region may be perceptible in
the 1.9 Ma Australopithecus sediba holotype adds further
complexity to our understanding of the evolution of the frontal
lobes (Carlson et al., 2011; Falk, 2014; Falk et al., 2018). Furthermore, the morphology of the occipital lobes in Australopithecus has
been proposed to reflect potential topographical reduction of the
visual cortex, which is likely to indicate an expansion of the parietal
association cortex. This hypothesis is based on a presumed caudal
position of the lunate sulcus in early hominins, which forms the
anterolateral boundary of the primary visual cortex in apes (e.g., the
Taung child, StW 505; Dart, 1925; Holloway, 1981, Holloway et al.,
2004a). However, identification of the lunate sulcus in fossil hominins remains highly controversial (e.g., Falk, 1980; Holloway, 1981;
Falk, 1983b; Holloway et al., 2004a; Falk, 2009). Finally, besides
being involved in critical functions in the extant human brain (e.g.,
association of the precuneus with tasks integrating spatial, chronological and social relationships [Bruner et al., 2017]), the parietal
region has played a fundamental role in the emergence of the
characteristic globular shape of the modern human brain (Bruner
et al., 2003a; Neubauer et al., 2018). However, because this region
is rarely preserved in early hominins, little is known about early
hominin parietal organization and morphology (Beaudet et al.,
1
There is no universal agreement as to whether the separation of humans and
their kin from great apes and their kin should be recognized at family level
(Hominidae) or tribe level (Hominini) or subtribe level (Hominina). Contributors to
this volume have agreed, while choosing their own term, to recognize that
disagreement by inserting this footnote.
113
2018a). Despite an unknown degree of correspondence between
the cerebral and endocranial sulcal patterns (Le Gros Clark et al.,
1936, but see Dumoncel et al., 2018), the relevance of the frontoorbital and lunate sulci, as well as to a lesser extent the parietal
sulci (see for example Tobias [1987] with regard to the inferior
parietal lobule), exemplifies the pivotal role of sulcal patterns in
detecting potential indications of cortical reorganization.
Besides sulcal imprints, endocasts may preserve traces of the
, 1997). Because of its
vascular system (Saban, 1983; Grimaud-Herve
role in the metabolism and thermoregulation of the brain, the
endocranial vascular system might be considered a relevant proxy
for analysis of fundamental changes in the hominin brain (see review in Bruner, 2017). Our knowledge of the endocranial vascular
system in fossil hominin taxa relies mainly on imprints of the
venous sinuses and of the middle meningeal vessels on the inner
surface of the braincase, but also on the preservation of the diploic
channels within diploic bone (Schepers, 1946; Saban, 1983; Falk
and Conroy, 1983; Conroy et al., 1990; Falk, 1990; Tobias, 1991;
Bruner et al., 2003b; Holloway et al., 2004b; Bruner et al., 2005;
Bruner and Sherkat, 2008; Bruner et al., 2011; Rangel de L
azaro
et al., 2016; Beaudet et al., 2018b). Extracranial venous foramina
represent an additional source of evidence for reconstructing the
cranial blood flow in fossils (e.g., Braga and Boesch, 1997; Seymour
et al., 2016). Comparison of the venous sinus systems and the
middle meningeal vessel pattern in early hominins reveals substantial differences between Australopithecus and Paranthropus
(Saban, 1983; Falk and Conroy, 1983; Conroy et al., 1990; Falk, 1990;
Tobias, 1991). More specifically, an enlarged occipitalemarginal
sinus is more commonly found in Paranthropus than in Australopithecus (except for the Hadar hominins) and the middle branch of
the middle meningeal vessels is virtually absent in Australopithecus
(Saban, 1983; Falk and Conroy, 1983; Conroy et al., 1990; Falk, 1990;
Tobias, 1991). For now, there is no consensus over the physiological
implications of the organization of the middle meningeal vessels in
the fossil hominin record (Bruner et al., 2003b, 2011), even if the
thermoregulation hypothesis has been largely favoured (e.g., Falk,
1990). Interpreting structural changes in the endocranial vascular
system in the light of cerebral reorganization is therefore of interest
for developing physiological hypotheses and investigating the potential coevolution of the brain and the vascular network.
The early hominin fossil record is highly fragmentary and rarely
preserves complete crania or natural endocasts (Holloway et al.,
2004b). Consequently, our knowledge of early hominin brain evolution primarily derives from partial endocasts, usually documenting
one of the three aforementioned key regions in the brain (e.g., frontal
lobes in KNM-ER 1470, MH 1, and Sts 60; occipital lobes in AL 162-28,
SK 1585 and StW 505; and the parietal lobe in Sts 1017 [Schepers,1946;
Holloway, 1972; Falk, 1979; Holloway, 1983; Falk, 1983a; Holloway
et al., 2004a; Carlson et al., 2011, Falk, 2014]) and traces of the
vascular system (e.g., KNM-ER 1470, SK 1585, Sts 60, and Sts 1017
[Schepers,1946; Holloway,1972; Falk,1979; Saban,1983]). Considering
these constraints, falsification of the hypotheses of a mosaic versus a
concerted evolution of cortical areas, and direct comparison of the
evolutionary trajectories of cortical folding and the vascular system
might be hampered by the quality of the early hominin fossil record.
In this regard, the ‘Little Foot’ cranium represents a unique opportunity to provide additional evidence of Pliocene hominin
neuroanatomy and to discuss potential evolutionary scenarios.
Indeed, besides its exceptional degree of preservation and
completeness (Clarke and Tobias, 1995; Clarke, 1998; Clarke and
Kuman, Submitted for publication), the Australopithecus specimen
StW 573 (‘Little Foot’), discovered in 1994 and 1997 in Member 2 of
the Sterkfontein Formation, is remarkable for its geological age of
3.67 Ma (Bruxelles et al., 2014; Granger et al., 2015; Kramers and
Dirks, 2017a,b; Stratford et al., 2017; Bruxelles et al., Submitted
114
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
for publication). Therefore, our study aims to: (i) provide the first
description of the StW 573 endocast (including general
morphology, structural asymmetries and cranial capacity), (ii)
detect, identify and comparatively describe the sulcal and vascular
pattern and (iii) discuss the significance of our findings for the
evolution of the hominin brain.
Table 2
Cranial capacity (ECV, cm3) of StW 573 compared with ECVs of Australopithecus and
Paranthropus published in Du et al. (2018).a
Specimen/taxa
2. Materials and methods
2.1. Comparative material
Information on fossil and extant specimens examined in the
present study is summarized in Table 1. We included ten fossil
hominins currently housed in the Evolutionary Studies Institute at
the University of the Witwatersrand in Johannesburg and the Ditsong National Museum of Natural History in Pretoria (South Africa;
Table 1). These are from Makapansgat (n ¼ 1), Malapa (n ¼ 1),
Sterkfontein (n ¼ 7) and Swartkrans (n ¼ 1). We use endocranial
volumes (ECV) of Australopithecus (afarensis, africanus, sediba and
garhi) and Paranthropus (aethiopicus, robustus and boisei) published
in Du et al. (2018) (Table 2). As we need to take into consideration the
hypothesis of a third Australopithecus species in southern Africa, the
Australopithecus africanus group is split into A. africanus (MLD 37/38,
Sts 19/58, Sts 5, Sts 60 and Taung) and Australopithecus prometheus
(MLD 1, Sts 71 and StW 505 [Clarke, 2008]). For our extant comparative sample, we selected one adult human and one adult common
chimpanzee individual curated in the Pretoria Bone Collection
et al., 2005) at the University of Pretoria (South Africa) and in
(L'Abbe
the Royal Museum for Central Africa in Tervuren (Belgium) respectively, and we also referred to available atlases and publications
documenting variation in the extant human and chimpanzee brain
(namely Connolly, 1950; Ono et al., 1990; Falk et al., 2018).
ECV
StW 573
Australopithecus prometheus (n ¼ 3)b
Mean
Range
Australopithecus afarensis (n ¼ 6)
Mean
Range
Australopithecus africanus (n ¼ 5)
Mean
Range
Australopithecus garhi (n ¼ 1)
Australopithecus sediba (n ¼ 1)
Paranthropus aethiopicus (n ¼ 3)
Mean
Range
Paranthropus robustus (n ¼ 3)c
Mean
Range
Paranthropus boisei (n ¼ 8)
Mean
Range
Date (Ma)
408
3.67
503
442e558
2.01e2.85
2.95e3.24
428
372e550
2.01e3.03
455
414e508
450
420
2.45e2.50
1.95
1.7e2.41
443
410e491
1.6e2.36
486
465e500c
1.41e1.93
492
430e545
a
Date ranges are from Du et al. (2018) except for Australopithecus prometheus: for
Sterkfontein Member 2 and StW 573, we use Granger et al., 2015, and for Member 4
Pickering and Kramers (2010) minimum age of 2.01. We note, however, that the
stratigraphic association of the flowstones used to date the upper limit of Member 4
is more complex than proposed in Pickering and Kramers (2010) and older dates for
Member 4 should not be discarded; for example, the faunal age estimate for that
member is between 2.4 to 2.8 Ma (Vrba, 1985).
b
Following Clarke (2008).
c
The ECV values for TM 1517, SK 48 and SK 46 listed by Du et al. (2018) are not
used here because RJC notes that these were only rough visual estimates published
in brief by Schepers (1946) and Broom and Robinson (1952) based on partial and
deformed specimens. We therefore use only the P. robustus specimens published by
Holloway et al. (2004a,b).
Table 1
Comparative sample used for analyzing and comparing the endocranial sulcal and vascular imprints.
Specimen/sample
Site/provenance
Taxonomic attribution
Sex
StW 505
Sterkfontein Member 4
Australopithecus
africanus/prometheus
M
StW 578
Jacovec Cavern
Australopithecus sp.
?
Sts 5
Sterkfontein Member 4
Australopithecus africanus
F/M
Sts 25
Sterkfontein Member 4
Australopithecus sp.
?
Sts 60
Sterkfontein Member 4
Australopithecus africanus
M
Sts 1017
Sts 1960b
SK 1585
MH 1
Sterkfontein Member 4
Sterkfontein Member 4
Dump Swartkrans
Malapa
?
Australopithecus africanus
Paranthropus robustus
Australopithecus sediba
?
?
?
M
MLD 37/38
Makapansgat
Member 4
South Africa
Congo
Australopithecus africanus
F
Homo sapiens
Pan troglodytes
F
M
Extant human (n ¼ 1)
Extant chimpanzee (n ¼ 1)
a
b
c
d
e
f
g
h
Evolutionary Studies Institute;
Ditsong National Museum of Natural History, Pretoria;
Pretoria Bone Collection, University of Pretoria;
Royal Museum for Central Africa.
Palaeosciences Centre, University of the Witwatersrand, Johannesburg;
South African Nuclear Energy Corporation, Pretoria (Hoffman and de Beer, 2012);
European Synchrotron Radiation Facility, Grenoble;
Centre for X-ray Tomography of Ghent University, Gent (Masschaele et al., 2013).
References
Lockwood and Tobias
(1999, 2002); Clarke
(2008)
Partridge et al. (2003);
Clarke (2013)
Broom (1947); Broom
and Robinson (1950);
Broom et al. (1950);
Clarke (2008); Grine et
al. (2012)
Brain (1981); Wolpoff
and Lee (2006); Grine
(2013)
Broom and Schepers
(1946)
Falk (1979)
de Ruiter (2004)
Holloway (1972)
Berger et al. (2010);
Carlson et al. (2011)
Dart (1959, 1962);
Conroy et al. (1990)
et al. (2005)
L'Abbe
Stored at
Imaging facility
ESIa
Pal. Centree
90.8
ESIa
Pal. Centree
66.6
e
75.0
b
Voxel size*
(isotropic; mm)
DNMNH
Pal. Centre
DNMNHb
Necsaf
64.9
DNMNHb
Necsaf
59.7
DNMNHb
DNMNHb
DNMNHb
ESIa
Necsaf
Necsaf
Necsaf
ESRFg
42.8
63.5
65.5
91.42
ESIa
Pal. Centree
80.8
PBCc
RMCAd
Necsaf
UGCTh
114.1
85.0
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
Sterkfontein StW 505 is an incomplete cranium preserving the
splanchnocranium and most of the left side of the neurocranium
(Lockwood and Tobias,1999) and is variably attributed to A. africanus
(Lockwood and Tobias, 1999, 2002) or A. prometheus (Clarke, 2008).
All of these studies regard StW 505 as an adult male specimen. This
specimen was recovered in Member 4 of the Sterkfontein Formation
during excavation of the type locality breccia where most of the
Australopithecus remains were recovered from 1936 by R. Broom and
later by J. Robinson (Lockwood and Tobias, 1999). The endocast
preserves the left hemisphere and the right frontal lobe (Falk et al.,
2000; Holloway et al., 2004a,b; Neubauer et al., 2012).
StW 578 is a calotte assigned to Australopithecus sp. and
discovered by R.J. Clarke and M. Makgothokgo in situ in the Jacovec
Cavern (Partridge et al., 2003; Beaudet et al., 2018b). The endocast
preserves the right parietal lobe, the posterior portion of the left
parietal lobe and part of the frontal area.
Sts 5 (‘Mrs Ples’) is the most complete and well-preserved cranium attributed to A. africanus (Broom, 1947; Broom et al., 1950). Sts
5 has been variably described as an adult female (Broom, 1947;
Broom and Robinson, 1950; Broom et al., 1950; Clarke, 2008;
Grine et al., 2012) or an adolescent male (Thackeray et al., 2002;
see review in Grine, 2013). Sts 5 was found in Member 4 of the
Sterkfontein Formation (Broom, 1947). The braincase lacks a strip of
bone running across the frontal and left side that was physically
filled using reconstruction material (see Clarke, 1990; Robinson,
1997 for comments on later damage).
Sts 25 is an isolated neurocranium filled by calcified sediment
found in Member 4 of the Sterkfontein Formation (Brain, 1981;
Holloway et al., 2004b). There is no definite taxonomic diagnosis
of Sts 25 (review in Beaudet et al., 2018b; Brain, 1981; Wolpoff and
Lee, 2006). Sts 25 has been suggested to be an adult (Brain, 1981;
Grine, 2013) or a young individual (Wolpoff and Lee, 2006). Sts
25 preserves the caudal part of the right frontal lobe, a portion of
the right parietal lobe, most of the left parietal and occipital lobes.
Sts 60 is a natural partial endocast found in Member 4 of the
Sterkfontein Formation (Broom and Schepers, 1946). Sts 60 is
associated with TM 1511, the holotype of Plesianthropus transvaalensis, which is now considered a junior synonym of A. africanus
(Clarke, 1994). TM 1511 is an adult male (Clarke, 2008). The endocast
preserves most of the left side while the right side is represented
only by the frontal lobe and a limited part of the parietal lobe.
Sts 1017 is a portion of a natural partial endocast from Member 4
of the Sterkfontein Formation initially identified as a cercopithecoid
and subsequently as a hominin (Falk, 1979). The species and sex are
unknown. Sts 1017 provides a portion of the right parietal, temporal
and frontal lobes (Falk, 1979).
Sts 1960b is a natural partial endocast embedded in a block of
breccia from Sterkfontein Member 4 attributed to A. africanus based
on comparisons with Sts 60 (de Ruiter, 2004). The visible surface of
the endocast consists mostly of the right frontal lobe and a portion
of the superior part of the left frontal lobe.
Swartkrans SK 1585 is a natural partial endocast from the lime
miners' hillside rubble dump at Swartkrans (Brain, 1970) and
consists of the right hemisphere and a very small portion of the left
occipital lobe (Holloway, 1972; Falk, 1980; Falk et al., 2000;
Holloway et al., 2004b). So far, this is the only natural endocast
known for Paranthropus robustus (Holloway et al., 2004b). This
specimen has been tentatively identified as a P. robustus by
Holloway (1972).
Malapa The partial cranium of the holotype juvenile male from
A. sediba (MH 1) was found in the 1.977 Ma deposits of Malapa
(Berger et al., 2010). The endocast of MH 1 is missing the entire
right hemisphere posterior to the coronal suture, posterior portions
of the left occipital and temporal lobes, and the cerebellum (Carlson
et al., 2011).
115
Makapansgat MLD 37/38 is a partial cranium attributed to an
adult female A. africanus from Makapansgat (Dart, 1959, 1962). The
endocast lacks most of the frontal area rostral to bregma (to the
exception of the caudal portion of the right inferior frontal area) as
well as the rostral part of the left temporal lobe (Conroy et al., 1990;
Neubauer et al., 2004, 2012).
2.2. Scanning protocol and endocast reconstruction
The skull of StW 573 was scanned at the microfocus X-ray tomography facility of the Palaeosciences Centre at the University of
the Witwatersrand, in Johannesburg (South Africa), at a spatial
resolution of 88 mm (isotropic voxel size). All of the comparative
specimens investigated in this study have been similarly imaged by
microfocus X-ray tomography using the various systems available
at the Centre for X-ray Tomography of Ghent University (UGCT) in
Ghent (Belgium; Masschaele et al., 2013), the Palaeosciences Centre
at the University of the Witwatersrand in Johannesburg (South
Africa) and the South African Nuclear Energy Corporation in Pelindaba (South Africa; Hoffman and de Beer, 2012, Table 1).
The sediments filling the endocranial cavity in StW 573 and the
comparative fossil specimens were digitally separated from the
bony remains by combining a region-based segmentation approach
and manual corrections via Avizo v9.0 software (Visualization Sciences Group Inc.; Meyer and Beucher, 1990; Roerdink and Meijster,
2001). The virtual endocranial volumes were extracted from the
extant human and chimpanzee individuals by using Endex software (Subsol et al., 2010; http://liris.cnrs.fr/gilles.gesquiere/wiki/
doku.php?id¼endex). The cranial capacity of StW 573 was
computed using Avizo v9.0.
2.3. Detection and identification of sulcal and vascular imprints
We used an automatic method for the detection of cortical relief in
endocasts based on the algorithm presented by Yoshizawa et al.
(2007, 2008) for the detection of topographical variation in threedimensional (3D) meshes (see Beaudet et al., 2016 and Beaudet and
Gilissen, 2018 for further technical details). Sulcal and vascular (i.e.,
middle meningeal vessels) imprints were detected via a geometrybased method using curvature lines computed from the surface. We
manually corrected detection by removing non-anatomical features,
mostly related to diagenetic processes, through a customized script
written in MATLAB R2013a (Mathworks, https://www.mathworks.
com/products/matlab.html). For reference for identification, we use
human and chimpanzee brains (Connolly, 1950; Ono et al., 1990; Falk
et al., 2018) and endocast (de Jager et al., 2018) atlases.
We followed the nomenclature detailed in Connolly (1950) and
Falk et al. (2018) and summarized in Table 3 for describing the
sulcal patterns. With respect to the middle meningeal vessels
(MMV), we referred to anterior (i.e., bregmatic), middle (i.e., obelic)
and posterior (i.e., lambdatic) branches (Schepers, 1946; Saban,
1983; Falk, 1993; Bruner et al., 2003b, 2005; Bruner and Sherkat,
2008). Additionally, we applied the scoring system introduced by
Adachi (1928) for the branching pattern of the middle branch of the
MMV that includes type I (i.e., the middle ramus branches from the
anterior ramus), type II (the middle ramus branches from the
posterior ramus) and type III (the middle ramus branches from both
rami) as illustrated in Falk (1993, Figure 3).
3. Results
3.1. General description
Preservation: Preservation of the cranium of StW 573 is
described in Clarke and Kuman, (Submitted for publication). A
116
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
Table 3
Abbreviations of features identified on endocasts.
Abbreviation
Sulci
ar
c
h
hr
fi
fm
fo
fs
ip
L
lc
pci
pcm
pcs
pl
pti
r
S
sca
scp
tm
ts
W
Middle meningeal vessels
ab
fb
mb
pb
Definition
Ascending ramus of lateral fissure
Central sulcus
Horizontal ramus of inferior precentral sulcus
Horizontal ramus of lateral fissure
Inferior frontal sulcus
Middle frontal sulcus
Fronto-orbital sulcus
Superior frontal sulcus
Intraparietal sulcus
Lunate sulcus
Calcarine sulcus
Inferior precentral sulcus
Middle precentral sulcus
Superior precentral sulcus
Prelunate sulcus
Inferior postcentral sulcus
Rectus sulcus
Lateral fissure
Subcentral anterior sulcus
Subcentral posterior sulcus
Middle temporal sulcus
Superior temporal sulcus
Fronto-marginal sulcus
Anterior branch
Frontal branch
Middle branch
Posterior branch
virtual rendering of the endocast is shown in Figure 1. A fracture
runs along the coronal suture and the frontal region has collapsed.
At the left side, a transverse break has induced a slight gap in the
middle part of the frontal lobe. The orbital surfaces, the frontal
poles, the inferior part of the frontal lobes and the left temporal
pole are not preserved. The superior parts of the frontal and parietal
lobes are damaged and distorted. An oblique crack runs from the
superior part of the caudal portion of the left parietal lobe to the
right sigmoid sinus, with some slight displacement. The left occipital and cerebellar lobes, and the portion of the occipital region
in-between the two cerebella are damaged. The region of the
basicranium surrounding the foramen magnum is crushed.
Morphology: The general shape of the unreconstructed endocast of StW 573 is compared with a number of southern African
Plio-Pleistocene hominins in Figure 2. The endocast of StW 573
approximates the rostrocaudally elongated and dorsoventrally
flattened endocranial shape seen in Australopithecus (Fig. 2;
Neubauer et al., 2012; Beaudet, 2018a). Even though the frontal
pole is missing, the frontal lobes seem to be more acutely angled
than in other Australopithecus, and we may hypothesize that the
beak-shaped rostral orbital area that is found in extant great apes
and Paranthropus may have been present in StW 573 (Fig. 2; Falk
et al., 2000). However, the fracture along the sagittal plane may
be responsible for the narrowing of the frontal area (Clarke and
Kuman, Submitted for publication). On the other hand, unlike
Paranthropus, the nearly complete right temporal lobe is anteriorly
extended and laterally projected, as in other Australopithecus
specimens (Fig. 2; Falk et al., 2000). The occipital poles in StW 573
are more pointed than in the Australopithecus comparative specimens and closely resemble the occipital morphology seen in SK
1585 and the extant human individual (Fig. 2). However, as for the
frontal lobes, this protrusion might be related to the crack that runs
along the occipital region. The cerebellar lobes are projected posteriorly, as in other Australopithecus, while in Paranthropus they are
placed under the cerebrum (Fig. 2; Holloway, 1972; Falk, 1985;
Holloway and Yuan, 2004).
Structural asymmetries: In terms of structural asymmetries,
StW 573 displays a left occipital petalia (i.e., protrusion of the left
occipital lobe beyond the right occipital lobe) that is also found in
Sts 5 and SK 1585 as well as in most fossil hominins, extant great
apes and humans (Fig. 2; Holloway et al., 2004b; Balzeau et al.,
2012). It is noteworthy that in MLD 37/38 the right occipital lobe
protrudes beyond the left occipital lobe (Fig. 2).
Cranial capacity StW 573 has an unreconstructed cranial capacity estimate of 408 cm3. We compiled the cranial capacity estimates of Australopithecus (afarensis, africanus, sediba and garhi)
and Paranthropus (aethiopicus, robustus and boisei) from Du et al.
(2018) in Table 2. The estimate for StW 573 falls within the range
Figure 1. Original skull (left), virtual skull (light grey) showing the endocast in semi-transparency (middle) and virtual endocast (dark blue, right) of StW 573 (A). Oblique view of
the virtual endocast of StW 573 showing the main cerebral imprints (B). Standard views (anterior, right, posterior, left, superior and inferior) of the endocast of StW 573 (C). Photo of
the original skull by M. Lotter and R.J. Clarke. Scale bars: 2 cm.
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
117
Figure 2. Virtual endocast of StW 573 and of six Australopithecus (StW 505, StW 578, Sts 5, Sts 60, MH 1, MLD 37/38), one Paranthropus (SK 1585), one extant human (EH) and one
extant chimpanzee (EC) specimens in lateral right (top row), dorsal (middle row) and rostral (bottom row) views. The left side of StW 505, Sts 60 and MH 1 are shown as right.
Images not to scale.
of Australopithecus afarensis but is slightly lower than the range of
southern African Australopithecus as well as the eastern and
southern African Paranthropus. This value is probably an underestimation thereof, because of the frontal region that has collapsed
and the plastic deformation that has affected the cranium (Clarke
and Kuman, Sumbitted). After correction of cranial capacity, StW
573 has the potential to fit within the range of southern African
Australopithecus and eastern African Paranthropus. In any case, the
cranial capacity of StW 573 would plot at the lower end of the
Australopithecus variation.
Additional identifiable features: On the top of the right parietal
lobe, there is a distinct granular fovea produced by the protrusion
of the arachnoid (Fig. 1 and Supplementary Online Material [SOM]).
The size of the fovea is less than 10 mm in diameter and is located
close to the sagittal plane at the top of the parietal lobe.
3.2. Sulcal imprints
Frontal lobes: A remnant of the superior frontal sulcus is identifiable on the rostral part of the right hemisphere (Fig. 3 and SOM).
The sulcus rectus makes an incision in the orbital margin. Caudal to
the sulcus rectus are a series of rostrocaudally-oriented furrows,
which correspond to the middle frontal sulcus. In the inferior part
of the frontal lobe, two grooves are perceptible that could not be
clearly identified (but see Discussion). The vertical sulcus detected
in the caudal portion of the frontal area is identified as the inferior
precentral sulcus.
On the most superior aspect of the left frontal lobe, a series of
sulci course from the anterior border close to the frontal pole towards the vertical crack delimiting approximately the transition to
the parietal lobe. We identify the most rostral sulcus among these as
the sulcus rectus, the intermediate furrows as part of the middle
frontal sulcus and the most caudal imprints as part of the horizontal
ramus of the inferior precentral sulcus. These three sulci could have
been continuous in the brain (Connolly, 1950; Falk et al., 2018). The
vertical sulcus transecting the middle frontal sulcus may correspond
to an element of the superior frontal sulcus (Ono et al., 1990; Falk
et al., 2018). The fronto-orbital sulcus incises the lateral margin of
the inferior frontal convolutions. Two sulci are detected superior to
the fronto-orbital sulcus in a position analogous to the unidentified
sulci detected in the right hemisphere. Given their respective position, we consider the following hypotheses: (i) the two furrows
may correspond to two rami of the fronto-orbital sulcus, (ii) the
posterior furrow may correspond to the inferior frontal sulcus
(Connolly, 1950; Ono et al., 1990; Falk et al., 2018). An additional
sulcus is detected close to the fronto-orbital sulcus, which could not
be identified. The vertical groove posterior to the fronto-orbital
Figure 3. Sulcal pattern in StW 573 and in five Australopithecus (StW 505, StW 578, Sts
5, Sts 25, Sts 60) specimens in lateral views. Only sulci mentioned in the text are
labelled. The right view of StW 505, the left view of StW 578 and both views of Sts 25
show the inner surface(s) of the opposite side(s) of the endocast. Question marks
indicate uncertain sulcal identifications. Abbreviations are detailed in Table 3. Labels
are placed at one of the extremities of the corresponding sulci. Images not to scale.
118
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
sulcus corresponds to the inferior precentral sulcus. The horizontal
ramus of the inferior precentral sulcus may have been confluent
with the inferior precentral sulcus.
In StW 573, Sts 5, Sts 25, SK 1585, MH 1, MLD 37/38 and to a
lesser extent in Sts 60 and Sts 1960b, the inferior region of the
frontal lobes is similarly convoluted (Figs. 3, 4, and SOM). In all of
these endocasts, the inferior region is incised by three vertical clefts
(which may correspond to the inferior precentral sulcus, the frontoorbital sulcus and the inferior frontal sulcus) bordering distinct
bulges (particularly prominent in Sts 5, MH 1 and MLD 37/38). The
pattern detected differs from the one reported in the human brain,
where the horizontal and ascending rami of the lateral fissure are
visible, and approximates more closely the pattern documented in
the chimpanzee brain, even if the configuration of the inferior
frontal sulcus could be extremely variable in the latter (Fig. 4,
Connolly, 1950; Falk et al., 2018). The middle frontal sulcus is
detected in StW 573, StW 505, Sts 60, Sts 1960b, and probably Sts 5.
This sulcus runs relatively straight from the frontal pole towards
the parietal area and is connected (or at least topographically close
to) the sulcus rectus, as in the chimpanzee brain (Falk et al., 2018).
In both StW 573 and Sts 60 the caudal end of the middle frontal
sulcus curves to form the horizontal ramus of the precentral sulcus,
which might also be observed in the human and chimpanzee brain
(Connolly, 1950; Ono et al., 1990; Falk et al., 2018).
Parietal lobes: In both hemispheres, the central sulcus in StW 573
runs along the main fracture approximately delimiting the frontal
lobe (Fig. 3, and SOM). The inferior end of the central sulcus is
slightly convex in both hemispheres. A remnant of a vertical sulcus
is detected caudal to the central sulcus on both sides. Because of its
close topographical proximity with the central sulcus, we suggest
that this furrow may correspond to the inferior postcentral sulcus. In
both hemispheres, a short vertical sulcus transects the lateral fissure
near the inferior end of the presumed inferior postcentral sulcus.
We identify this imprint as the subcentral posterior sulcus.
The central sulcus in StW 573, Sts 60 and SK 1585 is relatively
straight as compared to the hook-like inferior end of the central
sulcus in Sts 1017 (Figs. 3-4, and SOM). In both StW 573 and Sts
1017, the posterior subcentral sulcus intersects the lateral fissure
and it is topographically close to the postcentral sulcus, which is
also found in the human and chimpanzee brain (Connolly, 1950;
Ono et al., 1990; Falk et al., 2018).
Temporal lobes: The lateral fissure as well as the superior
temporal sulcus are clearly visible on the right temporal lobe of StW
573 (Fig. 3, SOM). Imprints of the superior temporal sulcus run
caudally towards the occipital lobe. Fragmentary furrows in the
inferior part of the right and left temporal lobes are tentatively
identified as remnants of the middle temporal sulcus.
In StW 573, Sts 5, Sts 60 and Sts 1017 the superior and middle
temporal sulci are parallel, as in extant chimpanzees, while in SK
1585 (and maybe MLD 37/38) they intersect (Figs. 3-4, and SOM). In
all of the fossil specimens considered in this study, the temporal
sulci are relatively continuous, as in extant chimpanzees, whereas
in extant humans the middle temporal sulcus is often subdivided
(Connolly, 1950; Falk et al., 2018).
Occipital lobes: Only one sulcus could be unambiguously
detected in the occipital part of the endocast. This crescent-shaped
sulcus is tentatively identified as the lateral edge of the lunate
sulcus. However, as StW 573 lacks any clear imprints of other occipital sulci and the bordering parietal sulci, our identification has
to be considered speculative. A faint sulcus was detected on the
right occipital lobe of the StW 573 endocast, but is difficult to
assign.
3.3. Vascular imprints
Figure 4. Sulcal patterns in four Australopithecus (Sts 1017, Sts 1960b, MH 1, MLD 37/
38), one Paranthropus (SK 1585), one extant human (EH) and one extant chimpanzee
(EC) specimens in lateral views. Only sulci mentioned in the text are labelled. The right
view of MH 1 shows the inner surface of the left side of the endocast. Question marks
indicate uncertain sulcal identifications. Abbreviations are detailed in Table 3. Labels
are placed at one of the extremities of the corresponding sulci. Images not to scale.
Traces of the middle meningeal vessels (MMV) are clearly visible
on both hemispheres of StW 573 (Fig. 5). On the right side, the
anterior branch of the MMV extends from the temporo-orbital
notch to the parietal lobe and bifurcates into two ramifications.
The middle branch of the MMV is connected to the anterior branch
and runs along the Sylvian fissure. The posterior branch derives
from the branch connected to the sigmoid sinus in the inferior part
of the temporal lobe (tentatively interpreted as the superior
petrosal sinus) and is parallel to the anterior and middle branches.
The meningeal vessel pattern on the left side is similar to the right
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
119
patterns that differ in the branching of the middle branch of the
MMV. The first pattern includes MLD 37/38, the extant human
endocast, and probably StW 578 and MH 1, depicting a middle
branch deriving from the anterior branch of the MMV (type I in Falk
[1993] adapted from the classification of Adachi [1928]). The second pattern includes SK 1585 and corresponds to a middle branch
deriving from the posterior branch of the MMV (type II in Falk
[1993] adapted from the classification of Adachi [1928]). The degree of ramification varies from a very simple pattern (e.g., StW 578,
Sts 60) to a more complex organization (left hemisphere of Sts 1017,
SK 1585, MLD 37/38, extant human and chimpanzee). In this
comparative context, StW 573 is similar to MLD 37/38, StW 578, MH
1 and extant humans in terms of branching pattern (i.e., type I).
4. Discussion
4.1. General aspects
Figure 5. Vascular patterns in StW 573 and in five Australopithecus (StW 578, Sts 60,
Sts 1017, MH 1, MLD 37/38), one Paranthropus (SK 1585), one extant human (EH) and
one extant chimpanzee (EC) specimens in lateral views. Only vessels mentioned in the
text are labelled. Abbreviations are detailed in Table 3. Images not to scale.
Despite a number of fractures and potential plastic deformation,
the endocast of StW 573 represents one of the most complete and
well-preserved early hominin endocasts currently available in the
fossil record (Holloway et al., 2004b). In terms of overall
morphology, the unreconstructed endocast is similar to the typical
shape described in early hominins (Falk et al., 2000; Neubauer
et al., 2012; Beaudet et al., 2018a) with some intriguing similarities with Paranthropus in the frontal and occipital lobes that need
to be confirmed by virtual reconstruction of the endocast and
quantitative morphometric analyses. The presence of occipital
petalias in Australopithecus specimens has been reported previously (e.g., Sts 5, Holloway et al., 2004b). This pattern of structural
asymmetry has been suggested to be shared by extant non-human
great apes and fossil hominins and to have been inherited from the
last common ancestor (Balzeau et al., 2012). In this regard, StW 573
confirms that occipital petalias were present in the hominin clade
more than three million years ago. The StW 573 estimated unreconstructed cranial capacity plots at the lower end of the Australopithecus range, which is consistent with its old geological age and
the hypothesis of a gradual increase in brain size within the hominin clade (but see Du et al., 2018). However, since the frontal region
has collapsed and plastic deformation has probably affected the
cranium (Clarke and Kuman, Submitted for publication), this volume is likely underestimated. Accordingly, the corrected volume
will likely fit within the A. africanus and/or the A. prometheus range,
and also within A. afarensis variation. Interestingly, StW 573 shows
traces of an arachnoid granulation. In extant humans, arachnoid
granulations are usually found adjacent to the superior sagittal sinus and are suggested to be involved in the drainage of the cerebrospinal fluid (Ikushima et al., 1999). Even if possible correlations
between size and frequency of arachnoid granulations and age are
disputed (e.g., Ikushima et al., 1999; Bayrak et al., 2009), the presence of this trace in StW 573 may be explained by the advanced age
of the specimen (i.e., the teeth are heavily worn and the absence of
internal signs of fused sutures [Clarke and Kuman, Submitted for
publication]) and related erosion/calcification of bone.
4.2. Sulcal pattern
counterpart, except ramification of the anterior and middle
branches is missing. Moreover, the anterior and middle branches
are more reticulated than in the right hemisphere. Unfortunately,
the occipital part is damaged and nothing can be said about the
configuration of the transverse-sigmoid system and, in particular,
about the presence/absence of an enlarged occipitalemarginal sinus (Falk and Conroy, 1983; Conroy et al., 1990; Tobias, 1991).
Within the fossil hominin specimens, the middle meningeal
branch is absent from Sts 60 and probably Sts 1017. We identify two
The inferior frontal circumvolutions and occipital sulci in early
hominins have played a central role in the debate dealing with the
timing and mode of brain evolutionary history (e.g., Falk, 1980;
Holloway, 1981; Holloway et al., 2004a; Falk, 2014). In particular,
the human-like configuration of the inferior frontal gyri (i.e.,
presence of the horizontal and ascending branches of the lateral
fissure) has long been acknowledged to emerge concomitantly with
the emergence of genus Homo (Falk, 1983a; Tobias, 1987). However,
120
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
the combination of a chimpanzee-like sulcal pattern (i.e., presence
of a fronto-orbital sulcus) with evidence of shape reorganization in
the A. sediba endocast (MH 1) adds further complexity to the
controversial evolutionary history of this cortical region (Carlson
et al., 2011; Falk, 2014). The description of the endocast of StW
573 and our comparative sample have the potential to provide
additional evidence of variation of the configuration of the early
hominin inferior frontal area. In our study, StW 573 and the Australopithecus and Paranthropus specimens show nearly systematically the same chimpanzee-like sulcal pattern combining three
vertical furrows, which encompass prominent bulges. However, the
degree of protrusion of the inferior frontal bulges is particularly
high in Sts 5, Sts 25, SK 1585 and MH 1 (but not to the same degree),
especially as compared to StW 573, which might suggest early
shape reorganization prior to changes in the sulcal pattern in this
region (Carlson et al., 2011; but see; Falk et al., 2018).
If our identification of the lunate sulcus in StW 573 is correct,
then it would be placed nearly above the sigmoid sinus, as in extant
chimpanzees, while in StW 505, SK 1585 and in extant humans the
lunate sulcus is found more caudally (Figs. 3, 4). Thus, its rostral
position would suggest an ancestral organization of the visual
cortex in Pliocene southern African hominins. In this regard, our
results cannot falsify either of the two competing hypotheses,
arguing for a human-like caudal (Dart, 1925; Holloway, 1972, 1981;
Holloway et al., 2004a) or chimpanzee-like rostral (Falk, 1980,
1983b, 2009) position of the lunate sulcus in the geologically
younger southern African hominin endocasts (e.g., Taung, StW 505,
SK 1585). On the contrary, if we consider the condition reported for
contemporaneous eastern African hominins, the StW 573 endocast
might provide crucial evidence for discussing evolutionary scenarios. Indeed, for southern African hominins, the A. afarensis
specimen AL 162-28 has been suggested to show either a humanlike (Holloway, 1983; Holloway and Kimbel, 1986) or chimpanzeelike (Falk, 1985) lunate sulcus. If AL 162-28 shows a human-like
lunate sulcus, it would mean that the derived organization of this
region occurred in eastern African Australopithecus, and that this
population was probably ancestral to the southern African hominins displaying similar organisation, or that this trait emerged in
different localities in Africa as a result of convergent evolution. On
the other hand, if AL 162-28 is similar to StW 573 in terms of occipital organization, the origins of a derived occipital organization
would postdate those two specimens. If “Little Foot” is significantly
geologically younger than 3.67 Ma (Kramers and Dirks, 2017a,b; but
see Stratford et al., 2017; Bruxelles et al., Submitted for publication),
it might indicate a high degree of variation of the lunate sulcus
within Pleistocene hominins. However, our identification of the
lunate sulcus in StW 573 needs to be confirmed through the
application of quantitative methods (e.g., Holloway, 1981; Beaudet,
2017). Moreover, variation of the lunate sulcus has been revealed to
be particularly high in the extant human brain (e.g., in Allen et al.,
[2006], a continuous lunate sulcus could only be identified in 1.4%
of the hemispheres observed), which may raise some concerns
about the identification of this structure in fossil hominin
endocasts.
The parietal lobes contributed significantly to the emergence of
globular shape of the modern human brain (Bruner et al., 2003a).
This region is also of interest due to the association of particular
neural districts with functions, such as the angular and supramarginal gyri for language (Tobias, 1987). In our sample, ramifications of the caudal portion of the superior temporal sulcus are
perceptible in Sts 1017 and the inferior part of the parieto-occipital
region are well-convoluted (e.g., StW 578 and StW 505). Moreover,
the posterior subcentral sulcus is present in StW 573, a region not
often preserved in early hominin endocasts (but see Sts 1017). This
sulcus forms the caudal boundary of Brodmann's area 43, which is
related to primary gustatory cortex, but also has implications for
language and digit stimulation (Trans Cranial Technologies, 2012).
Similarly, the superior temporal gyrus is involved in a number of
critical functions (notably as part of Wernicke's area) (Trans Cranial
Technologies, 2012). Interestingly, in all of the specimens preserving temporal sulci, the superior and middle temporal sulci are
parallel, with the exception of the Paranthropus specimen SK 1585,
and probably the Australopithecus specimen from Makapansgat,
MLD 37/38, in which the two sulci intersect. This observation might
be consistent with the differences reported in the morphology of
the temporal lobe between Australopithecus and Paranthropus (Falk
et al., 2000), and could be of interest considering the combination
of Australopithecus- and Paranthropus-like traits previously pointed
out in MLD 37/38 (Aguirre, 1970; Tobias, 1980).
4.3. Vascular pattern
The endocast of StW 573 reveals a complex organization of the
vascular system including ramifications of the anterior branch and
the presence of a middle branch of the MMV. Saban (1983, 1984)
described two patterns of the MMV within early hominins taxa,
with Paranthropus (SK 1585, KNM-ER 407, KNM-ER 1813) displaying a middle branch that is virtually absent in Australopithecus
(Taung, Sts 60, Omo 338 Y). Within our sample, we detected the
presence of a middle branch of the MMV in Australopithecus specimens, including in StW 573. Accordingly, our study suggests that
the middle meningeal vascular system in early hominins may have
been more complex and variable than previously thought. Moreover, within the limit of our sample (i.e., SK 1585 being the unique
representative of the Paranthropus genus), we found distinct patterns in terms of branching of the middle branch of the MMV between Australopithecus (type I) and Paranthropus (type II). Similarly,
Schepers (1946) identified various patterns in the southern African
early hominins depending on the dominance or codominance of
the anterior or posterior branches. Nonetheless, as previously
pointed out in great apes, the branching patterns of the middle
meningeal vessels variy substantially within a species (Falk, 1993),
and thus could be expected to vary as well within hominin taxa.
Interestingly, the middle meningeal vessels supply both the
diploic vessels in the cranial vault, and the dura mater (see review in
Bruner and Sherkat, 2008). Even if the extent of the diploic channels
housing diploic vessels has not been estimated yet in early hominins, a recent study revealed a large proportion of diploic bone in
the cranial vault of southern African Australopithecus as compared to
the relatively thin diploic layer in Paranthropus (Beaudet et al.,
2018b). Together with the typical enlarged occipitalemarginal sinus (Falk and Conroy, 1983; Conroy et al., 1990), those features tend
to support different cranial venous outflow in Paranthropus and,
possibly, a different metabolic rate (Seymour et al., 2016). This might
be consistent with the hypothesis of enlarged sinuses for Paranthropus and reliance of A. africanus on a different vascular system
involving the veins (Falk, 1990).
5. Conclusion
StW 573 provides a unique opportunity to investigate the
neuroanatomy of a Pliocene Australopithecus specimen and offers
fresh evidence for discussing the timing and mode of early hominin
brain evolution. While the degree of cortical folding and reticulation of the middle meningeal vessels in early hominin adult endocasts was previously known mainly from partial endocasts
(Schepers, 1946; Holloway, 1972; Falk, 1979; Holloway, 1983; Saban,
1984; Holloway et al., 2004a,b; Carlson et al., 2011; Falk, 2014), the
nearly complete endocast of StW 573 preserves a large extent of the
sulcal and vascular imprints.
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
Consistent with its geological age, StW 573 shows a minimum
cranial capacity estimate (pending the results of ongoing work in
producing a reconstructed endocast) that fits near the lower end of
observed Australopithecus variation and exhibits an overall cortical
folding pattern that is potentially less derived than in late Pliocene/
early Pleistocene southern African hominins (i.e., protrusion of the
inferior frontal convolutions in particular compared to MH 1, caudal
position of the presumed lunate sulcus compared to SK 1585 or StW
505). As previously predicted (Balzeau et al., 2012), the endocast of
StW 573 suggests that the left occipital petalia is already present in
Pliocene hominins. The exceptional preservation of StW 573 allows
the identification of very fine neuroanatomical details, such as an
arachnoid granulation, which opens new perspectives for our understanding of Australopithecus palaeobiology. Moreover, our
description of StW 573, together with our revision of the hominin
fossil record in southern Africa, suggests a complex organization of
the vascular system involving various branching patterns of the
middle meningeal arteries.
As the 3.67 Ma StW 573 specimen differs from the late Pliocene/
early Pleistocene southern African hominin specimens in key cerebral areas (e.g., inferior frontal gyri, visual cortex), we may hypothesize that environmental and biological changes that occurred
during the Plio-Pleistocene transition were probably selective
pressures on the cortical reorganisation of early hominins. More
specifically, a significant environmental shift took place during the
Plio-Pleistocene transition along with faunal turnovers in mammal
communities (Vrba, 1992; Bobe et al., 2002; deMenocal, 2004;
Robinson et al., 2017). Accordingly, this transition may have
involved substantial changes in primate ecological niches (e.g.,
Elton, 2001) and group size (e.g., Bettridge and Dunbar, 2012),
which may in turn be responsible for critical reorganization in the
brain (e.g., Aiello and Wheeler, 1995; Dunbar, 2009; Holloway et al.,
2004b). The virtual reconstruction of the skull of StW 573 will be
crucial for comparatively and quantitatively assessing the global
and local endocranial morphology of this unique specimen and
identifying potential early morphological changes within the
hominin clade.
Acknowledgements
We are indebted to E. Gillisen and W. Wendelen (Tervuren), G.
(Pretoria), L. Kgasi, H. Fourie, S. Potze and M.
Krüger and E. L'Abbe
Tawane (Pretoria), and B. Zipfel (Johannesburg) for having granted
access to fossil and comparative material under their care. We also
thank L. Bam and J. Hoffman (Pelindaba), M. Dierick (Ghent) for Xray microtomographic acquisitions. We are grateful to the Ditsong
National Museum of Natural History and the University of the
Witwatersrand for loaning hominin crania in their collections.
Permission for fossil access granted by H. Fourie, S. Potze and M.
Tawane (Ditsong National Museum of Natural History) and B. Zipfel
(Evolutionary Studies Institute). For technical and/or scientific
discussion/collaboration we are grateful to: M. Carmen Arriaza
(Pretoria) and J.F.
(Johannesburg), J. Dumoncel (Toulouse), A. Oettle
Thackeray (Johannesburg). We thank the DST-NRF for sponsoring
the Micro-XCT facility at Necsa, and the DST-NRF and Wits University for funding the microfocus X-ray CT facility in the ESI (www.
wits.ac.za/microct). The support of the AESOPþ program, the
Claude Leon Foundation, the DST-NRF Center of Excellence in
Palaeosciences (CoE-Pal), The Palaeontological Scientific Trust
(PAST) and the French Institute of South Africa towards this
research is hereby acknowledged. Major funding for the Sterkfontein excavations and MicroCT scanning work have been provided by
National Research Foundation grants to KK (#82591 and 82611)
and to DS (#98808) and by PAST, without whose support this
research could not have been able to continue. We thank Andrea
121
Leenen and Robert Blumenschine for their help in securing major
corporate funding, including sustained support from Standard Bank
and JP Morgan. Opinions expressed and conclusions arrived at are
those of the authors and are not necessarily to be attributed to the
Center of Excellence in Palaeosciences. We thank S. Elton as well as
thre anonymous reviewers for their comments, which contributed
to improve the original version of this manuscript. Ethical clearance
for the use of extant human crania was obtained from the Main
Research Ethics committee of the Faculty of Health Sciences, University of Pretoria in February 2016.
Supplementary online material
Supplementary online material related to this article can be
found at https://doi.org/10.1016/j.jhevol.2018.11.009.
References
Adachi, B., 1928. Das Arteriensystem der Japaner. Band 1. Kyoto. Verlag der
Kaiserlich-Japanischen Universitatzu Kyoto.
n de “Paranthropus” en Makapansgat. In: Cro
nica del
Aguirre, E., 1970. Identificacio
rida, pp. 98e124.
XI Congreso Nacional de Arqueología, Me
Aiello, L.C., Wheeler, P., 1995. The expensive-tissue hypothesis: the brain and the
digestive system in human and primate evolution. Current Anthropology 36,
199e221.
Allen, J.S., Bruss, J., Damasio, H., 2006. Looking for the lunate sulcus: a magnetic
resonance imaging study in modern humans. Anatomical Record 288, 867e876.
, D., 2012. Shared pattern of endocranial
Balzeau, A., Gilissen, E., Grimaud-Herve
shape asymmetries among great apes, anatomically modern humans, and fossil
hominins. PLOs ONE 7, e29581.
Barton, R.A., Harvey, P.H., 2000. Mosaic evolution of brain structure in mammals.
Nature 405, 1055e1058.
Bayrak, A.H., Akay, H.O., Ozmen, C.A., Senturk, S., 2009. Arachnoid granulations:
frequency and distribution in multi-detector row CT of dural sinuses. Biotechnology & Biotechnological Equipment 23, 1255e1258.
Beaudet, A., 2017. The emergence of language in the hominin lineage: perspectives
from fossil endocasts. Frontiers in Human Neuroscience 11, 427.
Beaudet, A., Gilissen, E., 2018. Fossil primate endocasts: perspectives from advanced
imaging techniques. In: Bruner, E., Ogihara, N., Tanabe, H. (Eds.), Digital Endocasts: from Skulls to Brains. Springer, Nagoya, pp. 47e58.
Beaudet, A., Dumoncel, J., de Beer, F., Duployer, B., Durrleman, S., Gilissen, E.,
Hoffman, J., Tenailleau, C., Thackeray, J.F., Braga, J., 2016. Morphoarchitectural
variation in South African fossil cercopithecoid endocasts. Journal of Human
Evolution 101, 65e78.
Beaudet, A., Dumoncel, J., de Beer, F., Durrleman, S., Gilissen, E., Oettle, A., Subsol, G.,
Thackeray, J.F., Braga, J., 2018a. The endocranial shape of Australopithecus africanus: surface analysis of the endocasts of Sts 5 and Sts 60. Journal of Anatomy
232, 296e303.
Beaudet, A., Carlson, K.J., Clarke, R.J., de Beer, F., Dhaene, J., Heaton, J., Pickering, T.R.,
Stratford, D., 2018b. Cranial vault thickness variation and inner structural organization in the StW 578 hominin cranium from Jacovec Cavern, South Africa.
Journal of Human Evolution 121, 204e220.
Bettridge, C.M., Dunbar, R.I.M., 2012. Modeling the biogeography of fossil baboons.
International Journal of Primatology 33, 1278e1308.
Berger, L.R., de Ruiter, D., Churchill, S.E., Schmid, P., Carlson, K.J., Dirks, P.H.G.M.,
Kibii, J.B., 2010. Australopithecus sediba: a new species of Homo-like australopith
from South Africa. Science 328, 195e204.
Bobe, R., Behrensmeyer, A.K., Chapman, R.E., 2002. Faunal change, environmental
variability and late Pliocene hominin evolution. Journal of Human Evolution 42,
475e497.
Braga, J., Boesch, C., 1997. Further data about venous channels in South African PlioPleistocene hominids. Journal of Human Evolution 33, 423e447.
Brain, C.K., 1970. New finds at the Swartkrans australopithecine site. Nature 225,
1112e1119.
Brain, C.K., 1981. The Hunters of the Hunted? An Introduction to African Cave
taphonomy. University of Chicago Press, Chicago.
Broom, R., 1947. Discovery of a new skull of the South African ape-man, Plesianthropus. Nature 159, 672.
Broom, R., Robinson, J.T., 1950. Further evidence of the structure of the Sterkfontein
ape-man Plesianthropus. Transvaal Museum Memoirs 4, 7e83.
Broom, R., Robinson, J.T., 1952. Swartkrans Ape-Man, Paranthropus crassidens.
Transvaal Museum, Pretoria.
Broom, R., Schepers, G.W.H., 1946. The South African Fossil Ape-men: the Australopithecinae. In: Transvaal Museum Memoirs, vol. 2. AMS Press, New York.
Broom, R., Robinson, J.T., Schepers, G.W.H., 1950. Sterkfontein ape-man. In: Plesianthropus. Transv. Transvaal Museum Memoirs, vol. 4. Pretoria, Transvaal
Museum.
Bruner, E., 2017. The fossil evidence of human brain evolution. In: Kaas, J. (Ed.),
Evolution of nervous systems, vol. 4. Elsevier, Oxford, pp. 63e92.
122
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
Bruner, E., Sherkat, S., 2008. The middle meningeal artery: from clinics to fossils.
Child’s Nervous System 24, 1289e1298.
Bruner, E., Manzi, G., Arsuaga, J.L., 2003a. Encephalization and allometric trajectories in the genus Homo: evidence from the Neandertal and modern lineages.
Proceedings of the National Academy of Sciences U.S.A. 100, 15335e15340.
Bruner, E., Averini, M., Manzi, G., 2003b. Endocranial traits. Prevalence and distribution in a recent human population. European Journal of Anatomy 7, 23e33.
Bruner, E., Mantini, S., Perna, A., Maffei, C., Manzi, G., 2005. Fractal dimension of the
middle meningeal vessels: variation and evolution in Homo erectus, Neanderthals, and modern humans. European Journal of Morphology 42, 217e224.
tara, J.M., Ripani, M., Sherkat, S., 2011. The
Bruner, E., Mantini, S., Musso, F., De La Cue
evolution of the meningeal vascular system in the human genus: From brain
shape to thermoregulation. American Journal of Human Biology 23, 35e43.
Bruner, E., Preuss, T.M., Chen, X., Rilling, J.K., 2017. Evidence for expansion of the
precuneus inhuman evolution. Brain Structure and Function 222, 1053e1060.
Bruxelles, L., Clarke, R.J., Maire, R., Ortega, R., Stratford, D., 2014. Stratigraphic
analysis of the Sterkfontein StW 573 Australopithecus skeleton and implications
for its age. Journal of Human Evolution 70, 36e48.
Carlson, K.J., Stout, D., Jashashvili, T., de Ruiter, D.J., Tafforeau, P., Carlson, K.,
Berger, L.R., 2011. The endocast of MH1, Australopithecus sediba. Science 333,
1402.
Clarke, R.J., 1990. Observations on some restored hominid specimens in the
Transvaal Museum, Pretoria. In: Sperber, G.H. (Ed.), From Apes to Angels: Essays
in Anthropology in Honor of Philip V. Tobias. Wiley-Liss, New-York,
pp. 135e151.
Clarke, R.J., 1994. Advances in understanding the craniofacial anatomy of South
African early hominids. In: Corruccini, R.S., Ciochon, R.L. (Eds.), Integrative Paths
to the Past: Essays in Honor of F. Clark Howell. Prentice-Hall, New Jersey,
pp. 205e222.
Clarke, R.J., 1998. First ever discovery of a well-preserved skull and associated
skeleton of Australopithecus. South African Journal of Science 94, 460e463.
Clarke, R.J., 2008. Latest information on Sterkfontein's Australopithecus skeleton and
a new look at Australopithecus. South African Journal of Science 104, 443e449.
Clarke, R.J., 2013. Australopithecus from Sterkfontein Caves, South Africa. In:
Reed, K., Fleagle, J.G., Leakey, R.E. (Eds.), The Paleobiology of Australopithecus.
Springer, Dordrecht, pp. 105e123.
Clarke, R.J., Tobias, P.V., 1995. Sterkfontein member 2 foot bones of the oldest South
African hominid. Science 269, 521e524.
Connolly, C.J., 1950. External Morphology of the Primate Brain. C.C. Thomas,
Springfield.
Conroy, G.C., Vannier, M.W., Tobias, P.V., 1990. Endocranial features of Australopithecus africanus revealed by 2- and 3-D computed tomography. Science 247,
838e841.
Dart, R.A., 1925. Australopithecus africanus: the man-ape of South Africa. Nature 115,
195e199.
Dart, R.A., 1959. The first Australopithecus cranium from the pink breccia at Makapansgat. American Journal of Physical Anthropology 17, 77e82.
Dart, R.A., 1962. The Makapansgat pink breccia australopithecine skull. American
Journal of Physical Anthropology 20, 119e126.
deMenocal, P.B., 2004. African climate change and faunal evolution during the
Pliocene-Pleistocene. Earth and Planetary Science Letters 220, 3e24.
, A.C., Fonta, C., Beaudet, A., 2018.
de Jager, E., Van Schoor, A.N., Hoffman, J.W., Oettle
Sulcal pattern variation in extant human endocasts. American Journal of
Physical Anthropology 165(Suppl. 66), 63 (abstract).
de Ruiter, D.J., 2004. Undescribed hominin fossils from the Transvaal Museum
faunal collections. Annals of the Transvaal Museum 41, 29e40.
de Sousa, A., Cunha, E., 2012. Hominins and the emergence of the modern human
brain. In: Hofman, M.A., Falk, D. (Eds.), Evolution of the Primate Brain: From
Neuron to Behavior. Elsevier, New York, pp. 293e322.
de Winter, W., Oxnard, C.E., 2001. Evolutionary radiations and convergences in the
structural organization of mammalian brains. Nature 409, 710e714.
Du, A., Zipkin, A.M., Hatala, K.G., Renner, E., Baker, J.L., Bianchi, S., Bernal, K.H.,
Wood, B.A., 2018. Pattern and process in hominin brain size evolution are scaledependent. Proceedings of the Royal Society B 285, 20172738.
, A.C., Lockhat, Z., Suleman, F.E., de
Dumoncel, J., Subsol, G., Durrleman, S., Oettle
Jager, E., Beaudet, A., 2018. A Quantitative Comparison of the Brain and the
me Symposium national de Morphome
trie et
Inner Surface of the Cranium, 10ie
Evolution des Formes (abstract).
Dunbar, R.I., 2009. The social brain hypothesis and its implications for social evolution. Annals of Human Biology 36, 562e572.
Elton, S., 2001. Locomotor and habitat classification of cercopithecoid postcranial
material from Sterkfontein Member 4, Bolt's Farm and Swartkrans Members 1
and 2, South Africa. Palaeontologia Africana 37, 115e126.
Falk, D., 1979. On a new australopithecine partial endocast. American Journal of
Physical Anthropology 50, 610e614.
Falk, D., 1980. A reanalysis of the South African australopithecine natural endocasts.
American Journal of Physical Anthropology 53, 525e539.
Falk, D., 1983a. Cerebral cortices of East African early hominids. Science 221,
1072e1074.
Falk, D., 1983b. The Taung endocast: a reply to Holloway. American Journal of
Physical Anthropology 60, 479e489.
Falk, D., 1985. Hadar AL 162-28 endocast as evidence that brain enlargement preceded cortical reorganization in hominid evolution. Nature 313, 45e47.
Falk, D., 1990. Brain evolution in Homo: The “radiator” theory. Behavioral and Brain
Sciences 13, 333e381.
Falk, D., 1993. Meningeal arterial patterns in great apes: implications for hominid
vascular evolution. American Journal of Physical Anthropology 92, 81e97.
Falk, D., 2009. The natural endocast of Taung (Australopithecus africanus): insights
from the unpublished papers of Raymond Arthur Dart. American Journal of
Physical Anthropology 49, 49e65.
Falk, D., 2014. Interpreting sulci on hominin endocasts: old hypotheses and new
findings. Frontiers in Human Neuroscience 8, 134.
Falk, D., Conroy, G.C., 1983. The cranial venous sinus system in Australopithecus
afarensis. Nature 306, 779e781.
Falk, D., Redmond Jr., J.C., Guyer, J., Conroy, G.C., Recheis, W., Weber, G.W., Seidler, H.,
2000. Early hominid brain evolution: a new look at old endocasts. Journal of
Human Evolution 38, 695e717.
n, M., Semendeferi, K., Alatorre Warren, J.L.,
Falk, D., Zollikofer, C.P.E., Ponce de Leo
Hopkins, W.D., 2018. Identification of in vivo sulci on the external surface of
eight adult chimpanzee brains: implications for interpreting early hominin
endocasts. Brain, Behavior and Evolution 91, 45e58.
Finlay, B.L., Darlington, R.B., 1995. Linked regularities in the development and
evolution of mammalian brains. Science 268, 1578e1584.
mez-Robles, A., Hopkins, D., Sherwood, C.C., 2014. Modular structure facilitates
Go
mosaic evolution of the brain in chimpanzees and humans. Nature Communication 5, 4469.
Granger, D.E., Gibbon, R.J., Kuman, K., Clarke, R.J., Bruxelles, L., Caffee, M.W., 2015.
New cosmogenic burial ages for Sterkfontein Member 2 Australopithecus and
Member 5 Oldowan. Nature 522, 85e88.
Grine, F.E., 2013. The alpha taxonomy of Australopithecus africanus. In: Reed, K.E.,
Fleagle, J.G., Leakey, R.E. (Eds.), The Paleobiology of Australopithecus. Springer,
Dordrecht, pp. 74e104.
Grine, F.E., Weber, G.W., Plavcan, J.M., Benazzi, S., 2012. Sex at Sterkfontein: ‘Mrs.
Ples’ is still an adult female. Journal of Human Evolution 62, 593e604.
, D., 1997. L'e
volution de l'ence
phale chez Homo erectus et Homo
Grimaud-Herve
sapiens. Exemples de l'Asie et de l'Europe. CNRS, Paris.
Hager, R., Lu, L., Rosen, G.D., Williams, R.W., 2012. Genetic architecture supports
mosaic brain evolution and independent brain-body size regulation. Nature
Communication 3, 1079.
Hoffman, J.W., de Beer, F.C., 2012. Characteristics of the micro-focus X-ray tomography facility (MIXRAD) at Necsa in South Africa. In: 18th World Conference of
Nondestructive Testing, Durban, South Africa.
Holloway, R.L., 1972. New australopithecine endocast, SK 1585, from Swartkrans,
South Africa. American Journal of Physical Anthropology 37, 173e186.
Holloway, R.L., 1981. Revisiting the South African Taung australopithecine endocast:
The position of the lunate sulcus as determined by the stereoplotting technique.
American Journal of Physical Anthropology 56, 43e58.
Holloway, R.L., 1983. Cerebral brain endocast pattern of Australopithecus afarensis
hominid. Nautre 303, 420e422.
Holloway, R.L., 2001. Does allometry mask important brain structure residuals
relevant to species-specific behavioural evolution? Behavioral and Brain Sciences 24, 286e287.
Holloway, R.L., Kimbel, W.H., 1986. Endocast morphology of Hadar hominid AL 16228. Nature 321, 536e537.
Holloway, R.L., Yuan, M.S., 2004. Endocranial morphology of A.L. 444-2. In:
Kimbel, W.H., Rak, Y., Johanson, D.C. (Eds.), The Skull of Australopithecus afarensis. Oxford University Press, Oxford, pp. 123e135.
Holloway, R.L., Clarke, R.J., Tobias, P.V., 2004a. Posterior lunate sulcus in Australopithecus africanus: was Dart right? Comptes Rendus Palevol 3, 1e7.
Holloway, R.L., Broadfield, D.C., Yuan, M.S., 2004b. The Human Fossil Record: Brain
Endocasts, the Paleoneurological Evidence. Wiley-Liss, Hoboken.
Ikushima, I., Korogi, Y., Makita, O., Yamura, M., Kawano, H., Kohama, M.,
Arikawa, K., Takahashi, M., 1999. MRI of arachnoid granulations within the
dural sinuses using a FLAIR pulse sequence. The British Journal of Radiology 72,
1046e1051.
Keller, S.S., Crow, T., Foundas, A., Amunts, K., Roberts, N., 2009. Broca's area: nomenclature, anatomy, typology and asymmetry. Brain and Language 109, 29e48.
Kramers, J.D., Dirks, P.H.G.M., 2017a. The age of fossil StW573 (‘little foot’): an
alternative interpretation of 26Al/10Be burial data. South African Journal of
Science 113, 1e8.
Kramers, J.D., Dirks, P.H.G.M., 2017b. The Age of Fossil StW573 (‘little foot’): reply to
comments by Stratford et al. South African Journal of Science 113, 1e3.
Kringelbach, M.L., Rolls, E.T., 2004. The functional neuroanatomy of the human
orbitofrontal cortex: evidence from neuroimaging and neuropsychology.
Progress in Neurobiology 72, 341e372.
, E.N., Loots, M., Meiring, J.H., 2005. The pretoria bone collection: a modern
L'Abbe
South African skeletal sample. Homo 56, 197e205.
Le Gros Clark, W.E., Cooper, D.M., Zuckerman, S., 1936. The endocranial cast of the
Chimpanzee. Journal of the Royal Anthropological Institute 66, 249e268.
Lockwood, C.A., Tobias, P.V., 1999. A large male hominid cranium from Sterkfontein,
South Africa, and the status of Australopithecus africanus. Journal of Human
Evolution 36, 637e685.
Lockwood, C.A., Tobias, P.V., 2002. Morphology and affinities of new hominid cranial
remains from Member 4 of the Sterkfontein Formation, Gauteng Province,
South Africa. Journal of Human Evolution 42, 389e450.
Masschaele, B., Dierick, M., Van Loo, D., Boone, M.N., Brabant, L., Pauwels, E.,
Cnudde, V., Van Hoorebeke, L., 2013. HECTOR: A 240kV micro-CT setup optimized for research. Journal of Physics: Conference Series 463, 012012.
Meyer, F., Beucher, S., 1990. Morphological segmentation. Journal of Visual
Communication and Image Representation 1, 21e46.
A. Beaudet et al. / Journal of Human Evolution 126 (2019) 112e123
Neubauer, S., Gunz, P., Mitteroecker, P., Weber, G.W., 2004. Three-dimensional
digital imaging of the partial Australopithecus africanus endocranium MLD 37/
38. Canadian Association of Radiologists Journal 55, 271e278.
Neubauer, S., Gunz, P., Weber, G.W., Hublin, J.-J., 2012. Endocranial volume of Australopithecus africanus: New CT-based estimates and the effects of missing data
and small sample size. Journal of Human Evolution 62, 498e510.
Neubauer, S., Hublin, J.-J., Gunz, P., 2018. The evolution of modern human brain
shape. Science Advances 4, eaao5961.
Ono, M., Kubik, S., Abernathey, C.D., 1990. Atlas of the Cerebral Sulci. Thieme
Publishing Group, Stuttgart.
Oxnard, C.E., 2004. Brain evolution: mammals, primates, chimpanzees, and
humans. International Journal of Primatology 25, 1127e1158.
Partridge, T.C., Granger, D.E., Caffee, M.W., Clarke, R.J., 2003. Lower Pliocene hominid remains from Sterkfontein. Science 300, 607e612.
Pickering, R., Kramers, J.D., 2010. Re-appraisal of the stratigraphy and determination
of new U-Pb dates for the Sterkfontein hominid site, South Africa. Journal of
Human Evolution 59, 70e86.
tara, J.M., Písova
, H., Lorenzo, C., Bruner, E., 2016.
Rangel de L
azaro, G., de la Cue
Diploic vessels and computed tomography: segmentation and comparison in
modern humans and fossil hominids. American Journal of Physical Anthropology 159, 313e324.
Robinson, J.T., 1997. The discovery of the Mrs Ples skull specimen. South African
Journal of Science 93, 164e165.
Robinson, J.R., Rowan, J., Campisano, C.J., Wynn, J.G., Reed, K.E., 2017. Late Pliocene
environmental change during the transition from Australopithecus to Homo.
Nature Ecology & Evolution 1, 159.
Roerdink, J.B.T.M., Meijster, A., 2001. The watershed transform: definitions, algorithms and parallelization strategies. Fundamenta Informaticae 41, 187e228.
ninge
es moyennes des Australopithe
ques. Bulletins et
Saban, R., 1983. Les veines me
moires de la Socie
te
d'Anthropologie de Paris 10, 313e323.
Me
volution des veines me
ninge
es chez Les Hommes
Saban, R., 1984. Anatomie et e
des travaux historiques et scientifiques, Paris.
fossiles. Comite
Schepers, G.W.H., 1946. The endocranial casts of the South African ape-men. In:
Broom, R., Schepers, G.W.H. (Eds.), The South African Fossil Ape-men: the
Australopithecinae. Transvaal Museum, Johannesburg, pp. 155e272.
Schoenemann, P.T., 2013. Hominid brain evolution. In: Begun, D. (Ed.), A Companion
to Paleoanthropology. Wiley-Blackwell, Chichester, pp. 136e164.
123
Seymour, R.S., Bosiocic, V., Snelling, E.P., 2016. Fossil skulls reveal that blood flow
rate to the brain increased faster than brain volume during human evolution.
Royal Society Open Science 3, 160305.
Smaers, J.B., Soligo, C., 2013. Brain reorganization, not relative brain size, primarily
characterizes anthropoid brain evolution. Proceedings of the Royal Society B
280, 20130269.
Stratford, D.J., Granger, D.E., Bruxelles, J., Clarke, R.J., Kuman, K., Gibbon, R.J., 2017.
Comments on ‘The Age of Fossil StW573 (‘Little Foot’): an alternative interpretation of 26Al/10Be burial data’. South African Journal of Science 113, 1e3.
re, G., Braga, J., Thackeray, F., 2010. 3D automatic methods to
Subsol, G., Gesquie
segment “virtual” endocasts: state of the art and future directions. American
Journal of Physical Anthropology 141(Suppl. 50), 226e227 (abstract).
Thackeray, J.F., Braga, J., Treil, J., Niksch, N., Labuschagne, J.H., 2002. ‘Mrs Ples’ (Sts 5)
from sterkfontein: an adolescent male? South African Journal of Science 98,
21e22.
Tobias, P.V., 1980. “Australopithecus afarensis” and A. africanus: critique and an
alternative hypothesis. Palaeontologia Africana 23, 1e17.
Tobias, P.V., 1987. The brain of Homo habilis: a new level of organization in cerebral
evolution. Journal of Human Evolution 16, 741e761.
Tobias, P.V., 1991. Olduvai Gorge. In: The Skulls, Endocasts and Teeth of Homo
habilis, vol. 4. Cambridge University Press, Cambridge.
Trans Cranial Technologies, 2012. Cortical Functions. Wanchai, Hong Kong.
Vrba, E.S., 1985. Early hominids in southern Africa: updated observations on
chronological and ecological background. In: Tobias, P.V. (Ed.), Hominid Evolution. Past, Present and Future. Alan R. Liss, New York, pp. 195e200.
Vrba, E.S., 1992. Mammals as a key to evolutionary theory. Journal of Mammalogy
73, 1e28.
Wolpoff, M.H., Lee, S.H., 2006. Variation in the habiline crania e Must it be taxonomic? Human Evolution 21, 71e84.
Yoshizawa, S., Belyaev, A., Yokota, H., Seidel, H.-P., 2007. Fast and faithful
geometric algorithm for detecting crest lines on meshes. In: Proceedings of the
15th Pacific Conference on Computer Graphics and Applications, pp. 231e237.
Yoshizawa, S., Belyaev, A., Yokota, H., Seidel, H.P., 2008. Fast, robust, and faithful
methods for detecting crest lines on meshes. Computer Aided Geometry Design
25, 545e560.