Brain, Calvarium, Cladistics A New Approach To An Old Question, Who Are Modern Humans and Neandertals - Journal of Human Evolution - 201

Journal of Human Evolution 92 (2016) 22e36
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Journal of Human Evolution

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Brain, calvarium, cladistics: A new approach to an old question, who

are modern humans and Neandertals?
lien Mounier a, b, *, Antoine Balzeau c, d, Miguel Caparros c,
Aure
Dominique Grimaud-Herve c
a
The Leverhulme Centre for Human Evolutionary Studies, Biological Anthropology Division, Department of Archaeology and Anthropology, University of
Cambridge, Fitzwilliam Street, Cambridge CB2 1QH, United Kingdom
b
UMR 7268 ADES, Aix-Marseille Universite/EFS/CNRS, Facult
e de Medecine e Secteur Nord Aix-Marseille Universit
e, CS80011, Bd Pierre Dramard, 13344
Marseille, France
c
Equipe de Pal
eontologie Humaine, UMR 7194 du CNRS, D epartement de Prehistoire du Museum national d'Histoire naturelle, Paris, France
d
Department of African Zoology, Royal Museum for Central Africa, B-3080 Tervuren, Belgium
a r t i c l e i n f o a b s t r a c t
Article history: The evolutionary history of the genus Homo is the focus of major research efforts in palaeoanthropology.
Received 13 April 2015 However, the use of palaeoneurology to infer phylogenies of our genus is rare. Here we use cladistics to
Accepted 16 December 2015 test the importance of the brain in differentiating and defining Neandertals and modern humans. The
Available online xxx
analysis is based on morphological data from the calvarium and endocast of Pleistocene fossils and re-
sults in a single most parsimonious cladogram.
Keywords:
We demonstrate that the joint use of endocranial and calvarial features with cladistics provides a
Palaeoneurology
unique means to understand the evolution of the genus Homo. The main results of this study indicate
Cladistics
Genus Homo
that: (i) the endocranial features are more phylogenetically informative than the characters from the
Homo neanderthalensis calvarium; (ii) the specific differentiation of Neandertals and modern humans is mostly supported by
Homo sapiens well-known calvarial autapomorphies; (iii) the endocranial anatomy of modern humans and Neandertals
show strong similarities, which appeared in the fossil record with the last common ancestor of both
species; and (iv) apart from encephalisation, human endocranial anatomy changed tremendously during
the end of the Middle Pleistocene. This may be linked to major cultural and technological novelties that
had happened by the end of the Middle Pleistocene (e.g., expansion of the Middle Stone Age (MSA) in
Africa and Mousterian in Europe). The combined study of endocranial and exocranial anatomy offers
opportunities to further understand human evolution and the implication for the phylogeny of our
genus.
© 2015 Elsevier Ltd. All rights reserved.
1. Introduction Significant work has been done on analysing the endocast shape
using comparative anatomy or geometric morphometric tech-
The evolution of the genus Homo is the focus of major research niques (Grimaud-Herve , 1997; Bruner, 2004, 2015; Neubauer et al.,
efforts in palaeoanthropology. From comparative anatomy to 2010; Bienvenu et al., 2011; Balzeau et al., 2014), leading to the
genomic studies, many different approaches are available to identification of different trends in the evolution of the brain in the
palaeoanthropologists to provide interpretations of the evolu- human lineage. For example, an increase in brain size during
tionary history of our genus. One of these methods, palae- hominin evolution is well-documented and established (Leakey
oneurology, involves studying the morphology of endocasts in et al., 1964; Sousa de and Wood, 2007; Rightmire, 2013) as is a
order to document the evolution of the hominin brain (Grimaud- reduction in brain size during the late evolution of Homo sapiens
Herve, 1997; Holloway et al., 2004; Sousa de and Wood, 2007). (Martin, 1983; Henneberg, 1998; Balzeau et al., 2013). Reorganisa-
tional changes have also been observed throughout human evo-
lution, such as the variations in sulcal patterning and gyral
extension (Tobias, 1971; Grimaud-Herve , 1997; Holloway, 2008;
* Corresponding author. Balzeau et al., 2012, 2013) and in meningeal patterns
E-mail address: am2099@cam.ac.uk (A. Mounier).
http://dx.doi.org/10.1016/j.jhevol.2015.12.006
0047-2484/© 2015 Elsevier Ltd. All rights reserved.
A. Mounier et al. / Journal of Human Evolution 92 (2016) 22e36 23
(Weidenreich, 1938; Saban, 1995; Grimaud-Herve , 2004b). In Nevertheless, many aspects concerning the definition of the
addition, recent works have been focussing on the ontogenetic Neandertal and AMH groups, their possible interaction and evolu-
development of the brain in humans and other hominids (Gunz tionary relationship, remain obscure. In particular, over the past 30
et al., 2012) in order to address evolutionary questions such as years much attention has been paid to the identification and the
the demise of Homo neanderthalensis. definition of their last common ancestor (LCA; Stringer, 1983, 2012;
However, with the exception of brain size variation, researchers Rightmire, 2008; Mounier et al., 2009; Endicott et al., 2010) through
tend to overlook palaeoneurological evidence when building the debate regarding the species Homo heidelbergensis
evolutionary hypotheses and theories. This apparent lack of (Schoetensack, 1908).
consideration may be partially explained by the peculiarity of the In the present study, we will answer the following questions:
material studied in palaeoneurology (i.e., the endocranial surface e
the endocast; see Grimaud-Herve , 1997; Holloway et al., 2004). 1) Are endocranial morphological features useful to assess phy-
More specifically, the study of the endocast as a surrogate for the logenies in the genus Homo when compared to ‘classic’ calvarial
study of the brain implies in-depth understanding of the complex anatomical traits?
relationships between brain shape and endocranial shape (Fournier 2) Can the definition of H. neanderthalensis and H. sapiens be
et al., 2011). In other words, to what extent does the endocast improved by the cladistic analysis of calvarial and endocranial
adequately reflect the shape of the brain? This difficult issue can be morphologies?
only partly addressed, as a major part of the morphological varia- 3) Can we propose hypotheses regarding the likely endocranial
tion observed on the brain is not preserved on the endocranial morphological pattern of the last common ancestor between
surface. However, the use of endocasts to study the fossil record H. sapiens and H. neanderthalensis?
also has advantages over the use of other anatomical parts. For
instance, a number of studies have demonstrated a significant age-
related reduction in total brain volume (Resnick et al., 2003; 2. Materials and methods
Kochunov et al., 2005; Rettmann et al., 2006), suggesting that the
shape of the endocranial cast reflects the shape of the brain of a 2.1. Materials
fully grown adult. Therefore, comparative morphological studies of
adult fossil endocasts compare specimens of the same develop- The fossil sample was selected in order to reflect the Middle and
mental stage, which corresponds to normal brain growth comple- Late Pleistocene fossil record morphological variability, with a
tion. This is not the case in comparative studies focusing on other particular focus on the species H. neanderthalensis and H. sapiens.
anatomical parts of fossils of unknown age of different hominin We included Early Pleistocene specimens as an outgroup to the
species, for which the pattern of development and aging might be cladistic analysis. We analysed the calvarium and the endocranium
different (Balzeau et al., 2012). Additionally, the observation of morphology without taking the upper face into account; this was
morphological features on endocasts may be difficult (Grimaud- due to the paucity of preserved faces among hominins in the
Herve , 1997). This can be, in part at least, addressed through the Pleistocene fossil record. We selected 28 fossil specimens from
use of well-defined coded endocranial anatomical traits. Africa and Eurasia, consisting of four Early Pleistocene specimens,
These limitations may be responsible for the lack of studies six Middle Pleistocene specimens and 18 Late Pleistocene fossils
(Falk, 1979) that address the systematics of hominins through nu- representing H. sapiens (n ¼ 9) and H. neanderthalensis (n ¼ 9;
merical analyses (either phenetic or cladistics) of endocranial Table 1). No juveniles were included in the study. We analysed the
morphological features, whilst cladistic principles and terminology original specimens (with the exception of Ehringsdorf 9 and
are regularly used in studies analysing endocast morphology Predmostí 3) and their endocranial casts or virtual replicas of the
(Semendeferi et al., 2010; Falk, 2012). For instance, Falk (1979) endocasts obtained from imaging methodologies. 3D volume
warns that the use of cladistics with neurological features must rendering was obtained from medical computed tomographic
be conducted cautiously since parallel evolution, and not ances- scans (voxel size between 0.449219 and 0.488281 mm). The
traledescendent relationships, might better explain the endocast boundary between bone and air, as well as the limits of the
morphological pattern among primates. And yet, cladistics is different structures analysed, were identified by manual segmen-
designed to distinguish between inherited similarities (homol- tation. This protocol required the use of multiple threshold values
ogies) and convergent morphologies (homoplasies) in order to as a function of variations in bone mineralisation. These settings
reconstruct phylogenetic relationships among taxa (Simpson, 1961; enabled us to obtain precise outlines and limits of the endocranial
Hennig, 1966). cavity, leading to the production of accurate 3D reconstructions.
In past palaeoneurological studies, some of us (AB and DGH) Computation of the virtual endocasts and evaluation of the
have identified trends in brain evolution among hominids and anatomical features were performed with Avizo 7 (VGS, ©2015 FEI
particularly in hominins, including apomorphic traits (Grimaud- Company).
Herve , 1997; Balzeau et al., 2012, 2013). Therefore, we believe Seventy coded morphological features (34 on the endocast and
that the combination of cladistics and palaeoneurology provides 36 on the calvarium, Tables 2 and 3) were observed on the speci-
yet underexploited possibilities to further understand the human mens. Coded observations on the calvaria were made by AM while
fossil record. The present study attempts to reconsider the evolu- observations on the endocasts were made by DGH. A full descrip-
tion of the genus Homo phylogenetically through cladistic analyses tion of the morphological features is available in Mounier (2009)
using coded morphological features from both the calvarium for the calvarium and in Grimaud-Herve (1997) for the endocast
(Mounier, 2009; Mounier et al., 2011) and the endocast (Grimaud- (see also Supplementary Online Material [SOM] A).
Herve , 1997; Grimaud-Herve and Lordkipanidze, 2010). This paper
is mainly focused on the phylogenetic relationship between 2.2. Methods
anatomically modern humans (AMHs) and Neandertals, since the
classification of these two taxa as H. sapiens and H. neanderthalensis, 2.2.1. Cladistic classification method The aim of the cladistic
while not completely settled (Hublin, 1998; Ovchinnikov et al., classification is to discover hierarchical relationships between ter-
2000; Condemi, 2001; Stringer, 2006; Wolpoff, 2009; Reich et al., minal taxa and to identify sister groups (monophyletic groups)
2011), is mostly accepted in the scientific community. among them on the basis of two fundamental principles: the
24 A. Mounier et al. / Journal of Human Evolution 92 (2016) 22e36
Table 1
Specimens included in the study.a
Specimens Chronology Site Chronology references
Early Pleistocene
KNM-ER 1470 ~1.8 Ma Koobi Fora, Kenya (Gathogo and Brown, 2006)
OH9 >1.47 Ma Olduvai Gorge, Tanzania (Tamrat et al., 1995)
Middle Pleistocene
Petralona* 150e250 ka Petralona, Greece (Grün, 1996)
Ehringsdorf 9 230 ka Ehringsdorf, Germany (Blackwell and Schwarcz, 1986)
Kabwe 1 >125 ka Kabwe, Zambia (Stringer, 2011)
Jebel Irhoud 1 130e190 ka Jebel Irhoud, Morocco (Grün and Stringer, 1991)
Jebel Irhoud 2 90e125 ka Jebel Irhoud, Morocco (Grün and Stringer, 1991)
LH 18 129e108 ka Laetoli, Tanzania (Manega, 1995)
Late Pleistocene
H. neanderthalensis
Saccopastore 1 100e130 ka Saccopastore, Italy (Bruner and Manzi, 2006)
Gibraltar 1 45e70 ka Forbe's Quarry, Gibraltar (Oakley, 1964)
La Ferrassie 1 53e66 ka La Ferrassie, France (Blackwell et al., 2007)
La Quina H5 ~65 ka La Quina, France (Mellars, 1996)
La Chapelle-aux-Saints ~50 ka La Chapelle-aux-Saints, France (Boule, 1911e1913)
Neanderthal 1 40 ka Feldhoffer Grotte, Germany (Schmitz et al., 2002)
Guattari 1 52 ± 12 ka Monte-Circeo, Italy (Grün and Stringer, 1991)
Spy 1 >36 ka Spy, Belgium (Toussaint and Pirson, 2006)
Spy 10 >36 ka Spy, Belgium (Toussaint and Pirson, 2006)
H. sapiens
Mlade c1 31 ka Mlade c, Czech Republic (Bra€uer et al., 2006)
Cro-Magnon 1* 28 ka Les Eyzies, France (Henry-Gambier, 2002)
Cro-Magnon 3 28 ka Les Eyzies, France (Henry-Gambier, 2002)
Predmostí 3 ~26 ka Chromeck, Czech Republic (Jelinek, 1991)
Abri Pataud 1* 22 ka Les Eyzies, France (Bricker and Mellars, 1987)
Qafzeh 6 90e130 ka Qafzeh, Israel (Valladas et al., 1988)
Skhu l V 66e102 ka Skhu l, Israel (Grün et al., 2005)
Nazlet Khater 2* 38 ± 6 ka Nazlet Khater, Egypt (Crevecoeur, 2006)
Hofmeyr* 36.2 ± 3.3 ka Hofmeyr, South Africa (Grine et al., 2007)
a
Bold type indicates that original specimens were examined (calvaria) and * indicates that virtual endocasts were studied.
concept of relative close relatedness (morphological similarity) and fossils (e.g., Blackwell and Schwarcz, 1986; Rak et al., 2002; Hublin,
the concept of similarity inherited from a common ancestor 2009; Mounier et al., 2011), we chose to run this analysis at the sub-
(sharing a recent common ancestor; Simpson, 1961). To do this, it is species level (see Caparros, 1997; Zeitoun, 2000, 2001; Asfaw et al.,
necessary to identify at least one similarity from a common 2002; Gilbert et al., 2003; Mallegni et al., 2003; Prat, 2004; Argue
ancestor (homology) that represents the appearance of an et al., 2009; Mounier and Caparros, 2015), with each fossil homi-
evolutionary novelty (synapomorphy). The identification of nin representing the population from which it is randomly drawn.
synapomorphies between sister taxa defines monophyletic
2.2.2. Parsimony analysis The parsimony analysis conducted in
groups from which a phylogeny and a classification may be
the present study follows the three step conceptual approach (see
inferred (Hennig, 1966; Caparros, 1997). Some authors consider
Caparros, 1997) presented by Mounier and Caparros (2015). It aims
cladistics as an inappropriate methodology in palaeoanthropology
to obtain the best-fit solution to explain the database of a given
(Trinkaus, 1992). However, its principal numerical classification
cladistic analysis by taking the phylogenetic information content
rival, the phenetic method, also presents a number of difficulties.
of the characters into account before running the proper cladistic
In contrast to cladistics, phenetics does not allow the recognition
analysis that will determine the evolutionary relationships
of homologies to identify taxa, and phenetic classifications are
between the terminal taxa (see below and Farris, 1969; Goloboff,
based solely on the general morphological resemblance between
1993). The first step of the protocol (low-level analysis) tests the
specimens (Darlu and Tassy, 1993). The results of phenetic
characters by congruence, i.e., parsimony principle (see Wiley,
analyses summarized in clustering dendograms does not provide
1981; de Pinna, 1991), ascertaining the phylogenetic information
the supporting evidence related to character states at the nodes
content of the characters as exemplified by their retention index
which define the morphotypes of common hypothetical ancestors
(RI, see below). The second step (high-level analysis) infers the
of terminal taxa and, consequently, the necessary information
hierarchical relationships between the terminal taxa using the
relevant to ancestor-descendant scenarios.
reweighted characters; in other words taking into account the
The aim of the present analysis is to test whether endocranial
phylogenetic information content of each character. Finally, the
synapomorphies supporting the accepted classification of the
last step is character state optimisation (Farris, 1970; Swofford
specimens included in this study may be identified. As proposed by
and Maddison, 1987) for identifying the morphology of the
Darlu and Tassy (1993), we consider that cladistic analyses below
hypothetical ancestors at the nodes of the cladogram. Paup (v.4.0)
the species level can be appropriate as long as terminal taxa (1) can
was used to perform the analysis and MacClade (v.4.08a) was
be recognized as possessing at least one unique attribute and, (2)
used for graphical illustration of supporting characters at the
should, in principal, be monophyletic groups; they further argue
hypothetical ancestors' nodes.
that populations meet these requirements. Due to the uncertainty
The low-level analysis uses a heuristic search by random step-
concerning the taxonomic classification of numerous hominin
wise addition to test by congruence the information content of each
of the 70 unweighted characters as reflected in the character occipitalis and #60 outline of the superior border of the temporal
retention index RI (Farris, 1989; Caparros, 1997; SOM squama). Additionally, 29 characters show a RI value inferior to 1
Tables B.1eB.5). If RI ¼ 1 the character represents a synapomor- but greater or equal to 0.667, and 13 present a RI of between 0.667
phy and if 0 RI < 1 the index represents the percentage of syn- and 0.5. It is interesting to note that the endocast shows a slightly
apomorphy of the character reflected in the most parsimonious higher percentage of phylogenetically informative characters
tree. If RI ¼ 0, the character expresses the maximum degree of (73.54%) compared with the calvarium (66.67%, SOM Table B.2). The
homoplasy and is therefore irrelevant to the branching of the discussion of the results is based on the 49 characters with RI 0.50
cladogram. The character RIs are discussed when reviewing the and special attention will be given to the features with a RI 0.667
supporting characters at the cladogram's nodes. (Table 4). The heuristic search found only one most parsimonious
The high-level analysis consists of running a branch-and-band tree (MPT) with the following tree fit statistics: tree length ¼ 49.56,
numerical analysis after reweighting the characters. As is com- CI ¼ 0.49, HI ¼ 0.51, RI ¼ 0.82 and RC ¼ 0.40 (SOM D). These tree fit
mon in all cladistic analyses, the first run shows that the statistics are relatively good, especially considering the high RI.
morphological features contribute differently to the fit of the best They are similar to the values obtained after the reweighting of the
trees according to their respective RI, some characters being more characters. Accordingly, the obtained classification (SOM C) is
homoplastic than others. Therefore, and as has been argued pre- similar to the one obtained after the reweighting of the characters
viously (Farris, 1969; Goloboff, 1993), in a parsimony analysis one (see below and Figs. 1 and 2), with the exception of the Neandertal
should always take the weights attributed to each character by the specimens, La Chapelle-aux-Saints and Neanderthal 1, which swap
congruence test into account in order to obtain the evolutionary positions. These low-level analysis results indicate that the data-
history which best explains the variation observed in the data. In base presents a strong phylogenetic signal.
the present study, we reweighted the data using the rescale con-
sistency index (RC ¼ CI (consistency index) RI (retention index)) 3.2. Parsimony analysis of reweighted characters
which is the most efficient way of weighting the data (Farris, 1989).
In order to further asses the robustness of our most parsimonious We used a branch-and-bound algorithm to analyse the
tree, we performed a bootstrap analysis (Felsenstein, 1985) of reweighted characters by respective RCs (Methods and Table 4). The
10,000 replicates on the reweighted data using heuristic searches. result is a single most parsimonious cladogram (Fig. 1) with overall
The results with the confidence in percentages for each branch of tree fit statistics as follows: tree length ¼ 50.21894, CI ¼ 0.50,
the tree are displayed in Figure 2 and SOM D. HI ¼ 0.50, RI ¼ 0.82 and RC ¼ 0.41. The CI value of the cladogram
The last step of the study is to analyse the apomorphic charac- corresponds to the traditionally admitted threshold of significance
ters that come in support of the branches of the cladogram. How- (i.e., 0.5) and might be considered as low; however, it should be
ever, in a given cladogram there are ambiguities regarding the noted that the CI is negatively correlated with the number of taxa
possible assignment of character states at various nodes of a given (Sanderson and Donoghue, 1989). Using Sanderson and Donoghue's
most parsimonious tree. These ambiguities may be assigned either (1989) formula to estimate the expected CI value given a number of
by a process of selective arguments about what the most likely taxa (i.e., CI ¼ 0.900.022 (number of taxa) þ 0.000213 (number of
character states possessed by the hypothetical ancestor at a node taxa)2), we obtain a predictive CI of 0.46 which is lower than the
could have been, or by one of the two accepted methods of actual CI value of the present study (i.e., 0.50). Therefore, the tree is
resolving ambiguities: ACCTRAN and DELTRAN (Farris, 1970; robust, particularly considering the RI of 0.82.
Swofford and Maddison, 1987). In the ACCTRAN method of accel- Three well-recognized clades can be identified on the cladogram
erated transformation, changes are assigned along the branches of (Fig. 1). The Early Pleistocene fossils comprise the outgroup (KNM-
a phylogenetic tree as close to the root as possible. This method ER 1470, KNM-ER 3733, KNM-ER 3883, OH 9) while the Neandertal
minimizes hypotheses of parallel origins of traits and favors re- and AMH specimens form two monophyletic groups:
versals. In the DELTRAN method, the delayed transformation H. neanderthalensis from node 40 to 32, and H. sapiens from node 50
changes are assigned along branches as close to the tips as possible to 41. The H. neanderthalensis clade includes ‘classic’ Western Eu-
and parallelisms are favored. However, Agnarsson and Miller ropeans (La Chapelle-aux-Saints, La Ferrassie 1, Neandertal, La
(2008) suggest that neither ACCTRAN nor DELTRAN consistently Quina H5, Spy 1 and 10), Southern Europeans (Guattari I, Sacco-
minimize parallelism. In the present study, we tested both opti- pastore 1 and Gibraltar 1) and one Late Middle Pleistocene fossil,
misation methods and we decided to use the DELTRAN method Ehringsdorf 9, which is often considered as an ‘early Neandertal’
since it enhances the proportion of unambiguous informative (Dean et al., 1998; Condemi, 2001). The AMHs sister group is
characters (see Results and SOM Table B.6). composed of upper Palaeolithic specimens (Predmostí 3, Mlade c 1,
Hofmeyr, Nalzet Khather 2, Abri Pataud 1, Cro-Magnon 1 and 3)
3. Results associated with Qafzeh 6 and Skhu l V, which are well-positioned
inside the clade despite their robust morphologies
3.1. Characters' phylogenetic information content analysis (Vandermeersch, 1981a; Grimaud-Herve , 1997; Balzeau et al.,
2013). Finally, the Jebel Irhoud specimens are also part of the
Out of the 70 characters (Tables 2 and 3), the first step of the clade showing strong similarities with Qafzeh and Skhu l (Hublin,
analysis (low-level analysis) identified 49 morphological features 2001). These three groups show a high degree of cohesiveness,
(Table 4) with appreciable phylogenetic information content especially within the AMH and Neandertal clades which are sup-
(RI 0.5), while 21 characters show a high homoplasic informative ported by numerous highly synapomorphic character changes (see
content level (RI < 0.5; Caparros, 1997). Among the 49 phyloge- infra).
netically informative characters, seven are synapomorphies (CI, RI Three Middle Pleistocene fossils stand between the outgroup
and RC ¼ 1, HI ¼ 0): five endocranial features (#1 cranial capacity, and the two monophyletic sister groups: Petralona, Kabwe and LH
#7 number of ramifications of the middle meningeal system, #16 18. The significance of this arrangement is unclear. Petralona and
orientation of the anterior and posterior ramus of the Sylvian valley Kabwe are often included in the hypodigm of H. heidelbergensis s.l.,
in norma lateralis, #22 definition and projection of the supra- the possible ancestral species to Neandertals and AMHs (Rightmire,
marginal gyrus and #30 position of the occipital lobes); and two 2008; Mounier et al., 2011; Stringer, 2012); their positioning in the
calvarial characters (#55 outline of the planum occipitale in norma cladogram might support this statement. LH 18's position is more
Table 2
Morphological features.a
Morphological features Character states Morphological features (endocast) Character states

(endocast)
Cranial capacity #1 0 <1200 Maximum length position between pars 19 0 Posterior

1 1200 triangularis 1 Medial
Spheno-parietal sinus 2 0 Absent or weakly-marked Position of the base of the pars triangularis 20 0 In front of the pole
1 Bulky relative to the temporal pole 1 On top of the temporal pole
Petro-squamous sinus 3 0 Absent 2 Join the temporal pole
1 Present Development of the relief of the foot of the 21 0 Weakly defined, not projecting
second parietal convolution
Development of the 4 0 Posterior system dominant, 1 Well-defined, slightly projecting
middle meningeal vessel developed obelic ramus
system 1 Anterior system dominant, Definition and projection of the supra- 22 0 Weakly-defined, weakly-projecting
well-ramified obelic ramus marginal gyrus
Development of the 5 0 From posterior frontal 1 Well-defined
anterior branch of the convolutions to anterior
middle meningeal system parietal convolutions or to
medial supra-marginal gyrus
1 Expands until the medial region Form of the supra-marginal gyrus 23 0 Weakly delineated
of the angular gyrus
Development of the 6 0 From medial region of supra- 1 Rounded
posterior branch of the marginal gyrus to posterior part
middle meningeal system of angular gyrus
1 Unique vessel with very few 2 Ovoid
ramifications
Number of ramifications 7 0 Few ramifications with few or Lobule of the angular gyrus 24 0 Non-discernible
of the middle meningeal no anastomoses
system 1 Dense network of anastomoses 1 Present
Orientation of the 8 0 Posterior branch parallel to the Orientation of the temporal sulcus 25 0 Converging frontward
branches of the middle bregmatic trunk
meningeal system 1 Posterior branches are oblique 1 Parallel
backward
Surface development 9 0 <14% of the hemispheres Orientation of the anterior part of the 26 0 Converging frontward
occipital lobe/ surface temporal lobes
hemispheres 1 14% of the hemispheres 1 Parallel
surface
Surface development 10 0 <50% of the hemispheres Position of the maximum endocranial width 27 0 Second temporal convolution
parieto-temporal lobe/ surface
hemispheres 1 50% of the hemispheres 1 First temporal convolution
surface
Form of the encephalic 11 0 Long, relatively narrow Position of the endo-vertex 28 0 Near endobregma or between bregma and Rolando
rostrum sulcus
1 Short and wide 1 Superior extremity of Rolando sulcus
General form of the 12 0 Regular curve Projection of the occipital lobes 29 0 Weak
encephalic rostrum and 1 Curve formed by two 1 Important
of the frontal lobes in disconnected parts between the
norma facialis orbital lobe and the encephalic
rostrum planes
Configuration of the 13 0 Large sulcus Position of the occipital lobes 30 0 Posterior continuing parietal and temporal lobes
interhemispheric fissure 1 Narrow and deep sulcus 1 Anterior under parietal and temporal lobes
Relief of the head of the 14 0 Weak and poorly delineated Position of the cerebellar lobes 31 0 Under occipital lobes or in intermediate position
third frontal convolution under temporal and occipital lobes
1 Well-developed, well- 1 Anterior under temporal lobes
delineated
Relief of the foot of the 15 0 Weak and poorly delineated Width of interhemispheric space between 32 0 Wide
third frontal convolution 1 Well-delineated, projecting the occipital lobes 1 Narrow, limited to diameter of superior sagittal
sinus
Anterior and posterior 16 0 Opening orientated backward Width of the sulcus separating the 33 0 Large
ramus of Sylvian valley: 1 Opening orientated upward cerebellar lobes 1 Narrow
orientation and frontward
Lateral development of 17 0 Weak lateral projection Form of the cerebellar lobes in norma 34 0 Triangular
the pars triangularis 1 Projecting laterally occipitalis 1 Ovoid
Sagittal development of 18 0 Weakly-developed downward
the pars triangularis 1 Developed downward
Table 2 (continued)
Morphological features Character states Morphological features (calvarium) Character states

(calvarium)
Outline of the calvarium, norma 35 0 Triangular Occipital bun 53 0 Absent

occipitalis 1 Circular 1 Present
2 Pentagonal Opisthocranion relative position/inion 54 0 Same position
Frontal cord length (M29)/parietal 36 0 M29/M30 < 1 1 Different position
cord length (M30) 1 M29/M30 1 Outline of the planum occipitale, norma 55 0 Triangular
Outline of the supra-orbital region, 37 0 Straight occipitalis 1 Circular
norma facialis 1 Convex 2 Pentagonal
Supra-orbital region: sulcus 38 0 Complete Suprainiac fossa 56 0 Absent or weakly-delineated
supraorbitalis 1 Incomplete 1 Present, well-delineated
2 Absent: arcus superciliaris- Torus occipitalis transversus 57 0 Absent
supraorbitalis merged
Projection of the supra-orbital 39 0 Not projecting or arcus 1 Present: medially protruding
region superciliairis only
1 Whole supra-orbital region 2 Present: bilaterally protruding
Post-orbital constriction 40 0 Important (Ipc 0.75) Protuberantia occipitalis externa 58 0 Absent
(Ipc ¼ M9/M43) 1 Absent (Ipc>0.85) 1 Present
Outline of the supra-orbital 41 0 Straight Tuberculum linearum 59 0 Absent
region, norma verticalis 1 Convex 1 Present
Sulcus postorbitalis 42 0 Absent Outline of the superior border of the 60 0 Curved or sinuous
1 Medially present temporal squama 1 Straight
2 Present continue Crista supramastoidea/processus 61 0 Not lined up
Tuber frontale 43 0 Absent zygomaticus temporalis 1 Lined up
1 Defined, medially shifted Tuberculum supramastoideum anterius 62 0 Absent
2 Present 1 Present
Sagittal keel on the frontal 44 0 Absent Position of the auditory meatus/processus 63 0 Below
1 Present zygomaticus temporalis 1 Intermediate
Bregmatic eminence 45 0 Absent 2 Aligned
1 Present Tuberculum mastoideum anterior 64 0 Absent
Thickening on the superior part 46 0 Absent 1 Present
of the coronal sutures 1 Present Processus mastoidus: downward 65 0 No protrusion
Pre-lambdatic hollowing on the 47 0 Absent development/basicranium 1 Protrusion
bregma-lambda arch 1 Present Glenoid cavity depth/articular tubercle 66 0 Shallow (<0.9 mm)
Linea temporalis width of the 48 0 Absent lowest point 1 Deep (>0.9 mm)
temporal band 1 Narrow (20 mm) Petro-tympanic crest orientation in relation 67 0 Perpendicular or frontward
2 Wide (>20 mm) to the sagittal plan 1 Backward
Torus angularis parietalis 49 0 Absent Articular tubercle configuration 68 0 Medio-lateral concavity
1 Present 1 Antero-posterior convexity
Tuber parietale 50 0 Absent 2 Medio-lateral convexity and vertical
1 Present, medially shifted Tuberculum zygomaticum posterius (post 69 0 Absent to weakly-marked
2 Present, high position glenoid process) 1 Marked
Outline of the occipital, norma 51 0 Rounded profile Tympanal contribution to the posterior wall 70 0 Weak
lateralis 1 Sharply angled of the glenoid cavity 1 Important
Outline of the planum 52 0 No convexity
occipitale, norma lateralis 1 Convexity
a (1997) and Mounier (2009).
Morphological features and character states description. For more details see SOM A, Grimaud-Herve
surprising as the fossil has been described as an early H. sapiens Methods). Very few changes can be observed in the assignment of
(Bra€uer, 2008). character states at nodes when using one or the other method
These polygenetic trends are corroborated by the 50% majority- (SOM Table B6). We used the DELTRAN resolution method to
rule bootstrapped consensus tree (Fig. 2, SOM D). In particular, the discuss the characters supporting the clades (Fig. 1) since DELTRAN
classification of the Homo erectus and of the three Middle Pleisto- identifies a slightly larger percentage of characters with a signifi-
cene specimens, as well as the integrity of the Neandertal clade, is cant RI value (i.e., RI 0.5, 72.22% against 71.43% for ACCTRAN) and,
confirmed with high confidence. However, the modern human in particular, a larger percentage of unambiguous characters
sister group fails to be identified and its terminal taxa are rooted in (69.44% instead of 59.66% for ACCTRAN, SOM Table B.6).
a polytomy at the ancestral node of Neandertal and modern The sister group of H. neanderthalensis is supported by six un-
humans. This may indicate larger morphological variation within ambiguous character state changes at node 40; all of them show a
the modern human fossils. high RI value (SOM Table B.3). Four of them are well-identified
To further assess the phylogenetic relationships that are not features specific to Neandertals: bilaterally protruding torus occi-
revealed by the most parsimonious tree, we analyse the suites of pitalis transversus (Hublin, 1988; #57, RI ¼ 0.933), well-delineated
synapomorphic characters that occur in support of the branches suprainiac fossa (Balzeau and Rougier, 2010, 2013; #56, RI ¼ 0.909),
and clades of the cladogram. circular calvarium in norma occipitalis (Condemi, 1992; #35,
RI ¼ 0.875) and medio-lateral concavity of the articular tubercle
3.3. Analysis of supporting characters of each clade (Elyaqtine, 2001; #68, RI ¼ 0.8), and can be considered as syna-
pomorphic inside the Neandertal clade (Fig. 1). Along with those
We tested the two accepted methods of resolving ambiguities calvarial features, the only endocranial character state change that
associated with the possible assignment of character states at phylogenetically supports the clade, a bulky spheno-parietal sinus
nodes: ACCTRAN and DELTRAN (Agnarsson and Miller, 2008; see (Grimaud-Herve , 1997; #2, RI ¼ 0.75), could be considered to be
Table 3
28
Character states of morphological features of fossil specimens.a
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34
KNM-ER 1470 0 0 1 0 0 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
KNM-ER 3733 0 0 e e e e e e 1 0 e e 1 0 e e 0 0 0 0 0 0 0 e 1 0 e 0 0 0 0 0 0 0
KNM-ER 3883 0 0 0 1 1 1 0 e 0 1 0 0 1 e e e 0 0 0 0 0 0 0 e 1 e 0 0 0 0 0 0 e e
OH9 0 0 0 e e 0 0 0 0 1 0 0 0 0 0 0 0 0 e 0 0 0 0 0 0 0 0 e 0 0 0 0 0 0
Petralona 1 e e e e e e e 1 1 0 e 0 1 1 0 1 0 0 0 0 0 1 0 1 0 0 0 1 0 0 0 0 0
Ehringsdorf 9 1 1 1 1 1 1 0 1 1 0 e e 1 e e e e e e e 1 1 e 1 e e 1 1 1 1 1 1 0 e
Kabwe 1 1 0 e e e e e e 1 1 1 0 0 1 0 1 1 0 0 1 0 0 1 0 1 0 0 1 1 0 1 0 0 1
Jebel Irhoud 1 1 e 0 1 1 1 0 1 1 0 1 1 1 1 e 1 1 1 1 2 0 1 2 1 1 e 0 1 0 1 1 1 1 e
Jebel Irhoud 2 1 0 e 1 1 1 0 1 1 0 1 1 1 1 1 1 1 1 1 2 0 1 2 1 1 1 0 1 0 1 1 e e 1
LH18 1 0 0 1 0 0 0 1 1 0 1 e 0 1 e e e e e e 0 0 0 0 0 0 0 1 1 0 0 0 0 0
Saccopastore 1 1 e e e e e e 0 1 1 0 0 0 1 0 1 1 1 1 1 0 1 2 0 0 0 0 0 1 1 0 1 0 0
Gibraltar 1 1 e e e e e e 0 e e 1 1 0 0 0 e 1 0 1 1 0 1 e e 1 1 1 e 1 1 0 1 e 1
La Ferrassie 1 1 1 1 1 1 1 0 0 0 0 e e 1 1 1 1 1 1 1 1 1 1 2 1 1 0 0 1 1 1 0 1 0 1
La Quina H5 1 1 e 1 1 1 0 1 1 0 e 1 e 1 1 1 1 1 1 e 0 1 2 1 1 e 0 1 1 1 1 1 1 1
La Chapelle-aux-Saints 1 1 1 1 0 0 0 0 1 0 0 1 1 1 1 1 1 1 1 1 1 1 2 1 1 e 0 0 1 1 1 1 0 1
Neanderthal 1 1 1 e 0 0 0 0 0 0 0 1 1 0 1 1 1 1 1 1 e 1 1 2 1 e e 0 0 0 1 e 0 e e
A. Mounier et al. / Journal of Human Evolution 92 (2016) 22e36

Guattari I 1 e e e e e e 1 e e 0 1 1 1 e 1 1 0 1 1 0 1 0 1 1 0 1 1 1 1 0 1 0 e
Spy 1 1 1 1 1 0 0 0 0 1 0 1 1 1 e e 1 0 e e e 1 1 e 1 e e 1 1 0 1 0 1 e e
Spy 10 1 1 1 1 0 0 0 0 1 0 e e e 1 e e 1 e 1 e 1 1 2 1 e e 1 1 1 1 0 1 e e
Mlade c1 1 e 0 e e e e 1 0 1 1 0 0 1 e 1 1 1 1 2 e 1 1 1 1 1 1 1 1 1 0 1 1 0
Cro-Magnon 1 1 0 0 1 1 1 1 1 0 0 1 1 1 1 1 1 1 1 1 2 1 1 1 1 1 1 1 1 1 1 1 1 1 1
Cro-Magnon 3 1 1 e 1 1 1 1 1 1 0 1 1 1 1 1 1 1 1 1 e 1 1 1 1 e e 1 1 1 1 1 1 e e
Predmostí 3 1 0 1 1 1 0 1 1 0 1 1 1 1 1 e e 1 1 1 2 1 1 1 1 1 1 0 1 1 1 1 1 1 1
Abri Pataud 1 1 0 e 1 1 1 e e 0 1 1 1 1 1 1 1 1 1 1 2 1 1 1 1 1 1 1 1 0 1 0 1 1 1
Qafzeh 6 1 0 1 1 1 1 0 1 e e 1 1 1 e 1 1 1 1 1 e e 1 1 1 e e 1 1 0 1 1 1 1 e
Skhul V 1 0 1 1 1 1 0 1 0 1 1 e 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 0 1 1 1
Hofmeyr 1 1 1 1 1 0 1 1 e e 1 1 1 1 e 1 1 1 0 1 1 1 1 1 e 1 1 e e e e e e e
Nazlet Khater 2 1 e e e e e e 1 0 1 1 1 1 1 1 1 1 0 1 1 0 1 1 1 1 1 0 1 0 1 0 1 1 1
35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 % Missing
KNM-ER 1470 0 2 1 2 2 0 1 0 0 0 0 0 0 2 0 0 1 1 0 0 0 0 1 0 e 1 1 1 0 1 e 0 2 0 0 1 2.9

KNM-ER 3733 0 2 1 1 2 0 1 2 1 1 1 1 1 2 0 0 1 0 0 1 0 0 1 0 1 0 1 1 0 0 0 1 0 0 0 1 17.1
KNM-ER 3883 0 2 1 2 2 0 2 2 1 0 0 0 1 2 0 0 1 0 0 0 0 0 1 1 e 0 1 1 0 0 1 1 2 0 1 1 12.9
OH9 0 e 1 2 1 0 1 1 1 0 e e e 1 0 0 1 1 0 0 e 0 1 1 1 1 1 0 0 1 1 1 1 2 0 1 12.9
Petralona 0 1 1 1 1 1 1 1 1 0 0 1 1 2 1 0 1 1 1 0 0 0 1 0 1 0 0 0 1 e 1 1 1 0 1 0 22.9
Ehringsdorf 9 1 1 1 1 1 1 1 1 2 0 0 0 1 1 0 0 1 1 1 1 e 1 2 0 1 0 1 1 1 0 e 0 0 0 0 e 22.9
Kabwe 1 0 1 1 1 1 0 1 1 1 1 0 1 1 1 1 0 1 1 1 1 2 0 1 1 e 0 1 1 0 0 1 1 0 1 1 0 10.0
Jebel Irhoud 1 2 0 0 0 1 1 1 1 2 0 0 0 1 1 0 2 0 1 0 1 2 0 0 0 0 0 0 1 0 0 1 1 0 1 0 0 5.7
Jebel Irhoud 2 0 1 1 1 0 1 1 1 2 0 0 0 1 1 0 1 0 1 0 1 2 0 0 1 1 0 0 0 e 0 1 1 0 1 1 0 5.7
LH18 2 1 1 0 1 0 1 0 2 0 0 0 1 1 0 2 0 1 0 1 2 0 0 0 1 0 0 0 0 0 0 1 0 1 0 1 10.0
Saccopastore 1 1 1 e e 1 1 e e 2 0 0 0 0 1 1 0 1 1 0 1 1 1 2 0 0 0 0 1 e 1 0 1 0 0 1 0 15.7
Gibraltar 1 1 0 1 1 1 1 1 1 2 0 e 0 e 1 0 0 1 1 1 1 1 1 2 0 0 0 1 1 0 0 0 0 0 0 1 0 21.4
La Ferrassie 1 1 1 1 2 1 1 1 1 2 0 0 0 1 1 0 0 1 1 1 1 1 1 2 0 0 0 0 1 2 1 0 0 0 0 1 0 2.9
La Quina H5 1 e 1 1 1 1 1 1 2 0 0 0 0 0 0 0 1 1 1 1 1 1 2 0 0 0 0 1 2 1 0 0 0 0 1 1 8.6
La Chapelle-aux-Saints 1 0 1 2 1 1 1 1 2 0 0 0 1 1 0 0 1 1 1 1 1 1 2 0 0 0 0 1 2 1 0 0 0 0 1 0 1.4
Neanderthal 1 1 1 1 2 1 1 1 1 2 0 0 1 1 1 0 0 e 1 1 1 1 1 2 e e e e e e e e e e e e e 30.0
Guattari I 1 1 1 2 1 1 1 1 2 0 0 0 1 2 0 0 1 1 1 1 1 1 2 0 0 0 0 0 2 1 0 0 0 0 0 0 14.3
Spy 1 1 0 1 2 1 1 1 1 2 0 0 1 1 2 0 0 1 1 1 1 1 1 2 0 0 0 1 1 2 1 0 1 0 0 0 1 14.3
Spy 10 1 e 1 2 1 1 1 1 2 0 0 1 0 2 0 0 1 1 1 1 1 1 2 0 0 0 1 1 2 1 0 1 0 0 0 1 17.1
Mlade c1 2 1 1 0 0 1 1 0 2 0 0 0 1 0 0 2 0 1 1 1 2 1 1 1 1 0 0 0 1 1 1 1 1 1 0 1 10.0
Cro-Magnon 1 2 0 1 0 0 1 1 0 2 0 0 0 1 2 0 2 0 0 0 1 2 0 0 1 1 0 1 0 0 1 1 1 0 1 0 1 0.0
Cro-Magnon 3 2 e 1 0 0 1 1 0 2 0 0 1 1 1 0 2 0 1 1 1 2 0 0 e e e e e e e e e e e e e 28.6
Predmostí 3 0 1 1 0 0 0 1 0 1 1 0 0 0 2 0 2 0 1 1 1 2 1 0 1 1 0 0 0 0 0 1 1 0 1 1 0 2.9
Abri Pataud 1 2 1 1 0 0 1 1 0 2 0 0 0 0 1 0 2 0 1 0 1 2 0 0 1 0 0 0 0 0 0 1 1 0 1 0 1 4.3
Qafzeh 6 2 1 1 0 1 1 1 0 2 0 0 0 1 1 0 2 0 1 0 1 2 0 0 1 0 0 0 0 0 0 e 1 0 1 0 1 12.9
Skhul V 2 0 0 1 1 0 1 1 2 0 0 0 1 1 0 1 0 1 0 1 2 0 0 1 1 0 1 0 0 0 1 1 0 1 0 1 1.4
Hofmeyr 2 e 1 1 1 1 1 0 2 0 1 0 0 2 0 2 e e e e 2 e e e e 0 0 0 0 1 e 1 0 1 1 0 30.0
Nazlet Khater 2 2 1 1 0 0 1 1 0 e e 0 0 0 1 0 2 0 1 0 1 2 0 0 1 1 0 1 0 0 1 1 1 0 0 1 0 11.4
a
Morphological features of each specimen included in the analysis.
A. Mounier et al. / Journal of Human Evolution 92 (2016) 22e36
Figure 1. Most parsimonious cladogram from high level analysis (tree length ¼ 51.63029, CI ¼ 0.46, HI ¼ 0.54, RI ¼ 0.80 and RC ¼ 0.37) with unambiguous supporting characters.
29
Figure 2. Bootstrap 50% majority-rule consensus tree with associated percentages on each branch. The 10,000 heuristic searches based on the reweighted data yield a similar
cladogram to the most parsimonious one (Fig. 1) with the exception of the H. sapiens clade.
specific to the Neandertals. However, this change appears inde- bulky spheno-parietal sinus (#2) could be considered as a proper
pendently in Cro-Magnon 3 and Hofmeyr (Fig. 1, SOM Table B.4). At H. neanderthalensis synapomorphy but it is also present in two
nodes 39 and 38, additional unambiguous changes with relevant RI upper Palaeolithic AMHs (Cro-Magnon 3 and Hofmeyr). No other
values (0.5) occur in support of the Neandertal clade. At node 38, endocranial feature seems to help further define the species but
two are identified Neandertal features: auditory meatus aligned they contribute to underlining important temporal differences
with the processus zygomaticus temporalis (Condemi, 1988; #63, (with Late Middle Pleistocene specimens), which may be useful in
RI ¼ 0.714) and present tuberculum mastoideum anterior the evaluation of the inter-population variation among the species
(Condemi, 1988; #64, RI ¼ 0.727), while at node 39 the presence of (Dean et al., 1998).
a tuberculum linearum (#59, RI ¼ 0.8) appears independently in The sister group of H. sapiens is supported at node 50 by four
the AMHs' sister group (SOM Table B.4; Fig. 1). From node 37 to 35, unambiguous character state changes with relevant RI values (0.5;
the clade is composed of only Western European ‘classic’ Nean- SOM Table B.4). Two are calvarial features: medially shifted tuber
dertals with the exception of Saccopastore 1 (Condemi, 1992). It is parietale (#50, RI ¼ 0.9) and present protuberantia occipitalis
worth noting that all of the unambiguous character state changes externalis (#58, RI ¼ 0.6), and two are endocranial features: narrow
identified at these nodes concern endocranial features (SOM sulcus separating the cerebellar lobes (#33, RI ¼ 0.857) and down-
Table B.3; Fig. 1). At node 37, the downward development of the ward development of the pars triangularis (#18, RI ¼ 0.75). Both
pars triangularis (#18, RI ¼ 0.75) is common to AMHs (node 50) and calvarial and endocranial features are quite homoplasic as they are
Western ‘classic’ Neandertals (Grimaud-Herve , 1997). From node found in other clades of the cladogram. However, the endocranial
36, the clade is further supported by the oblique and backward features may be of more interest for explaining the clustering: the
orientation of the posterior branch of the middle meningeal system narrow sulcus separating the cerebellar lobes should be considered
(#8, RI ¼ 0.75). This feature has been identified as being charac- to be fairly specific to the clade although this character is present in
teristic of Late Pleistocene hominins (Grimaud-Herve , 1997). the Neandertal sister group (i.e., La Quina H5, but to a lesser degree
However, in our sample, it is mostly present among AMHs (Table 3). compared to the conditions seen in AMHs) and is thus a parallel
A similar situation occurs at node 35 where the development of the evolution with, nevertheless, clear differences in shape and dispo-
posterior (#5 RI ¼ 0.6) and anterior (#6, RI ¼ 0.625) meningeal sition of the cerebellar lobes in H. neanderthalensis and H. sapiens
systems revert to their ancestral states (Grimaud-Herve , 2004b; (Grimaud-Herve , 1997; Weaver, 2005; Balzeau et al., 2011). A
Grimaud-Herve and Holloway, 2009) for Spy 1 and 10, Saccopas- downward development of the pars triangularis is also character-
tore 1, Neandertal and La Chapelle-aux-Saints. Considering the Late istic of the Western Neandertals (node 37 and see Grimaud-Herve ,
Middle Pleistocene fossil Ehringsdorf 9, we note that its position in 1997) and undergoes a reversion with Nazlet Khater 2. Among the
the Neandertal clade is well-supported by informative character four unambiguous character state changes identified at node 49,
state changes (node 40, SOM Table B.3; Fig. 1) some of which are three do not present a RI value greater or equal to 0.5: crista
well-known Neandertal features (see supra). The specimen has supramastoidea not lined up with processus zygomaticus tempo-
been described as an ‘early Neandertal’ (Dean et al., 1998; Condemi, ralis (#61, RI ¼ 0.455), occipital lobes weakly projecting (#29,
2001) or as being closer to AMHs (Vl cek, 1993). However, the results RI ¼ 0.4) and anteriorly positioned cerebellar lobes (#31, RI ¼ 0.222).
of this analysis would advocate for a full inclusion of this specimen Only the pars triangularis base joined with the temporal pole (#20,
into the H. neanderthalensis hypodigm. RI ¼ 0.889) could be considered to be more specific to the clade, it is
In summary, the H. neanderthalensis clade is phylogenetically however also found in the Neandertal (Grimaud-Herve , 1997) sister
well-supported by informative synapomorphous characters, most group and is undergoing a reversion with Nazlet Khater 2. Upstream
of which are known specific Neandertal calvarial features (#35, 56, from node 49, support for the AMHs' sister group is stronger. First, at
57 and 68). Considering endocranial features, as noted before, a node 48, a high-positioned tuber parietale (#50, RI ¼ 0.9) should be
Table 4
Most informative characters in decreasing order of RI.a
Morphological features # RI CI RC HI
True apomorphies RI ¼ 1: 6#
Cranial capacity 1 1 1 1 0
Number of ramifications of the middle meningeal system 7 1 1 1 0
Orientation of the anterior and posterior ramus of the Sylvian valley in norma lateralis 16 1 1 1 0
Definition and projection of the supra-marginal gyrus 22 1 1 1 0
Position of the occipital lobes 30 1 1 1 0
Outline of the planum occipitale, norma occipitalis 55 1 1 1 0
Outline of the superior border of the temporal squama 60 1 1 1 0
1 < RI ≤ 0.8: 15#
Torus occipitalis transversus 57 0.933 0.667 0.622 0.333
Suprainiac fossa 56 0.909 0.5 0.455 0.5
Tuber parietale 50 0.9 0.667 0.6 0.333
Outline of the occipital, norma lateralis 51 0.9 0.5 0.45 0.5
Position of the pars triangularis relative to the temporal pole 20 0.889 0.667 0.593 0.333
Orientation of the anterior part of the temporal lobes 26 0.875 0.5 0.438 0.5
Width of the sulcus separating the cerebellar lobes 33 0.875 0.5 0.438 0.5
Outline of the calvarium, norma occipitalis 35 0.875 0.5 0.438 0.5
Width of the interhemispheric space between the occipital lobes 32 0.857 0.5 0.429 0.5
Position of the endo-vertex 28 0.833 0.5 0.417 0.5
Position of the maximum length between the pars triangularis 19 0.8 0.5 0.4 0.5
Lobule of the angular gyrus 24 0.8 0.5 0.4 0.5
Tuber frontale 43 0.8 0.667 0.533 0.333
Tuberculum linearum 59 0.8 0.333 0.267 0.667
Articular tubercle configuration 68 0.8 0.5 0.4 0.5
0.8 < RI ≤ 0.6: 18#
Sulcus postorbitalis 42 0.778 0.333 0.259 0.667
Processus mastoidus: downward development/basicranium 65 0.778 0.333 0.259 0.667
Spheno-parietal sinus 2 0.75 0.333 0.25 0.667
Orientation of the branches of the middle meningeal system 8 0.75 0.333 0.25 0.667
Lateral development of the pars triangularis 17 0.75 0.5 0.375 0.5
Sagittal development of the pars triangularis 18 0.75 0.333 0.25 0.667
Tuberculum mastoideum anterior 64 0.727 0.25 0.182 0.75
Position of the auditory meatus/processus zygomaticus temporalis 63 0.714 0.5 0.357 0.5
Supra-orbital region: sulcus supraorbitalis 38 0.688 0.286 0.196 0.714
Form of the encephalic rostrum 11 0.667 0.333 0.222 0.667
Relief of the head of the third frontal convolution 14 0.667 0.5 0.333 0.5
Form of the supra-marginal gyrus 23 0.667 0.333 0.222 0.667
Projection of the supra-orbital region 39 0.667 0.333 0.222 0.667
Opisthocranion relative position/inion 54 0.667 0.5 0.333 0.5
Development of the posterior branch of the middle meningeal system 6 0.625 0.25 0.156 0.75
Development of the anterior branch of the middle meningeal system 5 0.6 0.333 0.2 0.667
General form of the encephalic rostrum and of the frontal lobes in norma facialis 12 0.6 0.333 0.2 0.667
Protuberantia occipitalis externa 58 0.6 0.2 0.12 0.8
RI < 0.6: 11#
Occipital bun 53 0.583 0.167 0.097 0.833
Tuberculum supramastoideum anterius 62 0.583 0.167 0.097 0.833
Post-orbital constriction (Ipc ¼ M9/M43) 40 0.571 0.25 0.143 0.75
Development of the relief of the foot of the second parietal convolution 21 0.545 0.167 0.091 0.833
Surface development parieto-temporal lobe/hemispheres 10 0.5 0.167 0.083 0.833
Form of the cerebellar lobes in norma occipitalis 34 0.5 0.25 0.125 0.75
Outline of the planum occipitale, norma lateralis 52 0.5 0.5 0.25 0.5
Glenoid cavity depth/articular tubercle lowest point 66 0.5 0.2 0.1 0.8
Petro-tympanic crest orientation in relation to the sagittal plan 67 0.5 0.333 0.167 0.667
a
Characters with RI 0.5 show a higher percentage contribution of synapomorphy than homoplasy in the most parsimonious tree and therefore are the most phyloge-
netically informative.
considered to be specific to the clade. It is however present in the orbital region (#39) as indicated by its RI value (0.575) is variable in
Late Middle Pleistocene specimen LH 18 and is considered to be a the cladogram. Upstream from node 45, the specimens' arrange-
reversion. The two other unambiguous character state changes ment is the expression of cumulative morphological variability with
(tuberculum linearum present, #59, RI ¼ 0.8 and sulcus supra- relatively low synapomorphic value as expressed by the RIs values
orbitalis complete, #38, RI ¼ 0.688) can be observed in Middle (i.e., #9 occipital lobe weakly developed, RI ¼ 0.444 and #48 wide
Pleistocene specimens and undergo reversion upstream in the linea temporalis band, RI ¼ 0.4). Characters #53 (occipital bun pre-
group. Then, the absence of sulcus supraorbitalis (#42, RI ¼ 0.788) sent) and #56 (suprainiac fossa present) seem to be more important
supports quite strongly the sister group from node 47. This change is since they are traditional Neandertal specific features and they
not specific to the group since it is also observable in the outgroup separate Predmostí 3 and Mlade c 1 from the other AMHs. The
(KNM-ER 1470) and in LH 18. Finally, at node 46, among the two presence of such features on these Eastern European AMHs has been
unambiguous character state changes with relevant RI values, a proposed to reflect a certain degree of admixture with Neandertal in
dense network of anastomoses in the middle meningeal system (#7, early European AMHs as advocated by certain authors (Rougier et al.,
RI ¼ 1) is a true synapomorphy for the rest of the AMH clade 2007; Trinkaus, 2007). However, one should keep in mind that the
(Grimaud-Herve , 1997). On the contrary, a non-projecting supra- definition of the suprainiac fossa has been the subject of
controversies (Hublin, 1978; Lieberman, 1995; Smith et al., 2005) Finally, node 51 represents the hypothetical ancestor to AMHs
and one of us has demonstrated that the depression observed on and Neandertals. The analysis identifies six unambiguous character
AMH fossils should not be considered homologous with the well- state changes among which two are true synapomorphies (RI ¼ 1):
known Neandertal morphology that is apomorphic for its external well-defined supra-marginal gyrus (#22) and occipital lobes posi-
particularities and its underlying structural bone composition tioned under the parietal and temporal lobes (#30), and two pre-
(Balzeau and Rougier, 2010, 2013). sent relatively high RI values: narrow interhemispheric space
The AMHs form a clade well-supported by both calvarial and between occipital lobes (#32, RI ¼ 0.857) and angular gyrus present
endocranial features. It is however, less cohesive than the Nean- (#24, RI ¼ 0.8). It is worth noting that all of the features identified at
dertal sister group due to the inclusion of two Late Middle Pleis- node 51 concern endocranial morphology (SOM Table B.5).
tocene fossils (Jebel Irhoud 1 and 2) and of Qafzeh 6 and Skhu l V. Despite the small size of the Middle Pleistocene sample in this
Those fossils are slightly separated from the main AMH clade and analysis, we observe a few evolutionary trends: Kabwe and Petra-
they lack the first synapomorphy of the sister group which ap- lona, which are often grouped in an Afro-European Middle Pleis-
pears at node 46 (dense network of anastomoses in the middle tocene population (Rightmire, 2008; Mounier et al., 2011; Stringer,
meningeal system, #7, RI ¼ 1; Fig. 1). Such a classification of the 2012), are differentiated by numerous character state changes on
Jebel Irhoud, Qafzeh and Skhu l specimens reflects their morpho- the endocranium. Additionally, LH 18, which is generally consid-
logical pattern: the combination of a relatively robust morphology ered as an early AMH (Bra €uer, 2008), fails to be classified as
associated with the presence of key morphological features (e.g., a H. sapiens on the basis of its brain morphology, which is more
narrow sulcus separating the cerebellar lobes #33, and presence of similar to Middle Pleistocene fossils. Finally, the morphological
tuber parietale #50) that are part of the definition of the H. sapiens changes which define the ancestor to the two monophyletic clades
species (Vandermeersch, 1981a; Grimaud-Herve , 1997, 2005). (AMH and Neandertal) concern only endocranial features.
The three Middle Pleistocene fossils, Petralona, Kabwe and LH
18, are positioned just before node 51 which represents the hypo-
thetical last common ancestor between AMHs and Neandertals. 4. Discussion
Node 54 separates the Middle Pleistocene fossils from the out-
group. Five unambiguous character state changes can be identified The results of this cladistic analysis show that the combined use
(SOM Table B.5), among which a cranial capacity superior to of cladistics and palaeoneurology is a powerful and promising
1200 cc is a true synapomorphy for the rest of the cladogram (#1, approach. The inclusion of calvarial and endocranial features allows
RI ¼ 1). Two other features present valuable synapomorphic con- us to investigate the anatomy of fossil specimens in considerably
tent (RI 0.5): pars triangularis projecting laterally (#17, RI ¼ 0.75), greater detail. This study is therefore the most complete investi-
and well-developed head of the third frontal convolution (#14, gation to date on the anatomy of the calvarium and of the endocast,
RI ¼ 0.667). One should note that all these features concern and provides an in-depth view of the Neandertal/modern human
endocranial morphology. The European Middle Pleistocene spec- dichotomy.
imen Petralona is then separated from the main branch due to its The obtained phylogeny, based on both exocranial and endo-
low degree of post-orbital constriction (#40, RI ¼ 0.571) and the cranial characters, corresponds to the major consensus concerning
intermediate position of its auditory meatus in relation to the classification of the genus Homo. Nevertheless, the present study
processus zygomaticus temporalis (#63, RI ¼ 0.714). Upstream of underlines the phylogenetic importance of endocast morphology,
node 53, nine unambiguous changes can be noted, two of which are as the endocranial characters are more phylogenetically informa-
synapomorphies (RI ¼ 1): opening of the Sylvian valley facing up- tive than the calvarial features (SOM Table B.2) generally used to
ward and frontward (#16) and pentagonal planum occipitale in produce phylogenies in human evolution. However, it is important
norma occipitalis (#55), while six show relevant RI values (0.5): to keep in mind that the exact nature of the developmental cor-
pars triangularis positioned on top of the temporal pole (#20, relation that likely exists between the phylogenetically relevant
RI ¼ 0.889), endo-vertex positioned at the superior extremity of the endocranial characters identified in the present study remains
central sulcus (#28, RI ¼ 0.833), antero-posterior convexity of the largely unknown (e.g., see Neubauer, 2015). As a result, further
articular tubercle (#68, RI ¼ 0.8), opisthocranion separated from research is needed to meliorate our understanding of the relative
inion (#54, RI ¼ 0.667), short and wide encephalic rostrum (#11, importance and evolutionary significance of the well-known
RI ¼ 0.667) and petro-tympanic crest perpendicular to the sagittal endocranial morphological features highlighted in this study.
plane (#67, RI ¼ 0.5). The changes at node 53 are important in the Nevertheless, and in spite of this important reservation, the five
building of the current phylogeny. In particular, one true synapo- endocranial synapormorphies identified by the first part of the
morphy (#16 the orientation of the Sylvian valley opening does not present analysis correspond to important evolutionary steps in the
change anywhere else in the cladogram; Fig. 1 and Grimaud-Herve , cladogram (Fig. 3): a large brain size (#1) separates early Homo
1997) separates the early Homo specimens and Petralona from Af- specimens from the rest of the sample; the upward and frontward
rican Middle Pleistocene fossils (i.e., Kabwe and LH 18) and the two opening orientation of the Sylvian valley (#16) isolates Petralona
monophyletic clades Neandertal and AMH. Kabwe is then segre- from more recent fossils; a well-defined supra-marginal gyrus
gated due to the presence of a protuberantia occipitalis externa (#22) as well as occipital lobes positioned under the parietal and
(#58, RI ¼ 0.6). At node 52, we note four unambiguous characters temporal lobes (#30) are synapomorphies of the possible LCA of
with relevant RI values (0.5): absence of a torus occipitalis H. sapiens and H. neanderthalensis and, as such, are common to all
transversus (#57, RI ¼ 0.933), pentagonal calvarium in norma AMH and Neandertal specimens, and finally, a dense network of
occipitalis (#35, RI ¼ 0.875), present tuber frontale (#43, RI ¼ 0.8) anastomoses for the middle meningeal system (#7) distinguishes
and weakly developed parieto-temporal lobe (#10, RI ¼ 0.5). The the upper Palaeolithic H. sapiens from the more archaic AMHs Jebel
separation of LH 18 from the rest of the specimens is due to its Irhoud 1 and 2, Qafzeh 6 and Skhu l V.
developed tuber parietale (#50, RI ¼ 0.9), the absence of sulcus Both monophyletic sister groups, H. sapiens and
postorbitalis (#42, RI ¼ 0.778), the presence of a complete sulcus H. neanderthalensis, are well-supported in the cladogram, but the
supraorbitalis (#38, RI ¼ 0.688) and its relatively low cranial ca- cohesiveness of their clade is mostly supported by characters of the
pacity (#1, RI ¼ 0.6). calvarium and the contribution of endocranial features is different
for each clade.
Figure 3. Simplified cladogram with most important character state changes. Only apomorphies with RI 0.9 are represented.
The Neandertals are mainly defined by calvarial features which Qafzeh 6 and Skhu l V) in the present study. A dense network of
correspond to the known definition of H. neanderthalensis: well- anastomoses indicates improved blood circulation (see Bruner and
delineated suprainiac fossa (Balzeau and Rougier, 2010; #56), Sherkat, 2008; Bruner et al., 2011), which is linked to the oxygen-
bilaterally protruding torus occipitalis transversus (Hublin, 1988; ation of the brain and of the neurons. In neuroscience studies,
#57), circular calvarium in norma occipitalis (Boule, 1911e1913; increased blood flow in some areas of the braincase is commonly
Vandermeersch, 1981b; Condemi, 1992; #35) and auditory used as a proxy to study neuronal activation, in other words the
meatus aligned with processus zygomaticus temporalis (Vallois, activity of the brain, as active neurons require more blood to sup-
1969; #63; see Fig. 3). The only endocranial character that could port their activity (Hecht and Stout, 2015). The identification of an
be considered as a synapomorphy for H. neanderthalensis is a bulky apomorphy indicating improved blood circulation in the braincase
spheno-parietal sinus (#2), but it is also present in two upper of upper Palaeolithic modern humans could be related to improved
Palaeolithic AMHs (Cro-Magnon 3 and Hofmeyr). The ‘classic’ cognitive abilities or at least to an increase in neuronal activity. If
Western Neandertals present specialisations in their endocast that confirmed, this result could support the hypothesis describing the
differentiate them from ‘early Neandertals’: the posterior branch of emergence of a ‘cultural modernity’, i.e., a behavior that demon-
the middle meningeal system is parallel to the bregmatic trunk strates modern human thought processes (Gargett, 1999), around
(#8), and the posterior (#6) and anterior (#5) middle meningeal 70 to 60 ka disconnected from the appearance of a modern skeletal
systems are well-developed (Grimaud-Herve , 2004a; Grimaud- morphology in humans 200 ka ago (Wadley, 2001; Conard, 2010;
Herve and Holloway, 2009). This endocranial morphology is, Texier et al., 2011). However, in our opinion, the concept of ‘cul-
however, homoplastic outside the Neandertal clade and constitutes tural modernity’ remains to be clarified as the debates over what
a reversion in the case of the ‘classic’ Western Neandertals. archeological evidence should be considered as demonstrating
In contrast, along with characters of the calvarium, the AMHs' modern human thought processes is far from being resolved
sister clade is supported by numerous endocranial features. How- (Gargett, 1999; McBrearty and Brooks, 2000). Moreover, Neander-
ever, most of those endocranial characters are variable within the tals have the largest brain size among hominins and share complex
clade. For instance, a joined base of the pars triangularis with the cognitive abilities with modern humans. Consequently, an alter-
temporal pole (#20) is common to the AMH specimens with the native explanation for the lack of a dense network of anastomoses
exception of Skhu l V, Hofmeyr and Nazlet Khater 2, which display in Neandertals could be that thermoregulation and blood circula-
the plesiomorphic condition (Table 3). The only endocranial true tion occur in different ways in the two species, minimising the
synapomorphy characterising the AMH sister group is a dense possibility of interpreting the dense network of anastomoses of
network of anastomoses in the middle meningeal system (#7). This modern humans as solely reflecting optimised brain functions.
character has been noted as being specific to current H. sapiens Finally, node 51 represents the possible common ancestor of
endocasts by one of us (Grimaud-Herve , 1997, 2004b) and accord- H. sapiens and H. neanderthalensis. The character state changes
ingly it segregates the upper Palaeolithic AMHs (Cro-Magnon 3, displayed at this node are only endocranial features. In particular,
Abri Pataud 1, Cro-Magnon 1, Nazlet Khater 2, Hofmeyr, Mladec 1 two true synapomorphies differentiate the Late Pleistocene sister
and Predmostí 3) from older specimens (Jebel Irhoud 1 and 2, groups: the supra-marginal gyrus is well-defined (#22) and the
occipital lobes are positioned under the parietal and temporal lobes comments and criticisms which contributed significantly to
(#30). These morphologies have been noted before as marking improve the quality of this manuscript.
important changes during the Middle Pleistocene (Grimaud-Herve ,
1997). Additionally, these anatomical features are directly related to
Appendix A. Supplementary Online Material
specificities of the modern human brain: the strong development
of the parietal lobes and the increase of the relief on its surface (e.g.,
Supplementary online material related to this article can be
Balzeau et al., 2012). The results of the present cladistic analysis
found at http://dx.doi.org/10.1016/j.jhevol.2015.12.006.
support this statement, furthermore they indicate that the hypo-
thetical last common ancestor of AMHs and Neandertals would
have developed a unique derived brain morphology before the References
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Journal of Human Evolution 92 (2016) 22e36

Contents lists available at ScienceDirect

Journal of Human Evolution

Brain, calvarium, cladistics: A new approach to an old question, who

Specimens Chronology Site Chronology references

Morphological features Character states Morphological features (endocast) Character states

Cranial capacity #1 0 <1200 Maximum length position between pars 19 0 Posterior

Morphological features Character states Morphological features (calvarium) Character states

Outline of the calvarium, norma 35 0 Triangular Occipital bun 53 0 Absent

A. Mounier et al. / Journal of Human Evolution 92 (2016) 22e36

KNM-ER 1470 0 2 1 2 2 0 1 0 0 0 0 0 0 2 0 0 1 1 0 0 0 0 1 0 e 1 1 1 0 1 e 0 2 0 0 1 2.9

Darlu, P., Tassy, P., 1993. La Reconstruction Phyloge ne

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