Journal of Human Evolution xxx (2014) 1e9

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Journal of Human Evolution

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Taxonomic differences in deciduous upper second molar crown

outlines of Homo sapiens, Homo neanderthalensis and Homo erectus
Shara E. Bailey a, b, *, Stefano Benazzi c, b, Caroline Souday a, Claudia Astorino d,
Kathleen Paul e, Jean-Jacques Hublin b
a
Center for the Study of Human Origins, Department of Anthropology, New York University, 25 Waverly Place, New York, NY 10003, USA
b
Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany
c
Department of Cultural Heritage, University of Bologna, Via degli Ariani 1, 48121 Ravenna, Italy
d
The Graduate Center, City University of New York, 365 Fifth Avenue, New York, NY 10016, USA
e
School of Human Evolution and Social Change, Arizona State University, P.O. Box 872402, Tempe, 85287-2402 AZ, USA

a r t i c l e i n f o a b s t r a c t

Article history: A signicant number of Middle to Late Pleistocene sites contain primarily (and sometimes only) de-
Received 17 June 2013 ciduous teeth (e.g., Grotta del Cavallo, Mezmaiskaya, Blombos). Not surprisingly, there has been a recent
Accepted 5 February 2014 renewed interest in deciduous dental variation, especially in the context of distinguishing Homo nean-
Available online xxx
derthalensis and Homo sapiens. Most studies of the deciduous dentition of fossil hominins have focused
on standard metrical variation but morphological (non-metric and morphometric) variation also
Keywords:
promises to shed light on long standing taxonomic questions. This study examines the taxonomic sig-
Dental variation
nicance of the crown outline of the deciduous upper second molar through principal components
Geometric morphometrics
Molar crown shape
analysis and linear discriminant analysis. We examine whether or not the crown shape of the upper
Pleistocene deciduous second molar separates H. neanderthalensis from H. sapiens and explore whether it can be used
Phylogeny to correctly assign individuals to taxa. It builds on previous studies by focusing on crown rather than
Tighenif cervical outline and by including a large sample of geographically diverse recent human populations. Our
Sangiran samples include 17 H. neanderthalensis, ve early H. sapiens, and 12 Upper Paleolithic H. sapiens. In
addition, we include two Homo erectus specimens in order to evaluate the polarity of crown shape
differences observed between H. neanderthalensis and H. sapiens. Our results show that crown outline
shape discriminates H. sapiens and H. neanderthalensis quite well, but does not do well at distinguishing
H. erectus from H. sapiens. We conclude that the crown outline shape observed in H. sapiens is a primitive
retention and that the skewed shape observed in H. neanderthalensis is a derived condition. Finally, we
explore the phylogenetic implications of the results for the H. erectus molars.
2014 Elsevier Ltd. All rights reserved.

Introduction
It is well established that dental morphological variation is a
useful tool in diagnosing hominin fossil taxa (Bermdez de Castro
et al., 1999; Harvati et al., 2003; Bailey et al., 2006; Bailey and
Hublin, 2006; Benazzi, 2012). Most studies of dental morphological
variation, especially in a fossil context, have focused on the perma-
nent teeth (Wood and Abbott, 1983; Wood et al., 1983; Wood and
Uytterschaut, 1987; Wood and Engleman, 1988; Kaifu et al., 2005;
Bailey, 2006; Martinn-Torres et al., 2008, 2012). The deciduous
dentition of early hominins has received some attention (Grine,1984,
* Corresponding author.
E-mail addresses: sbailey@nyu.edu (S.E. Bailey), stefano.benazzi@unibo.it
(S. Benazzi), claudia.m.astorino@gmail.com (C. Astorino), ksm.paul@gmail.com
(K. Paul), hublin@eva.mpg.de (J.-J. Hublin).
1985), but comparatively less has been paid to deciduous dental
morphological variation in the context of later Pleistocene human
evolution. Most studies focusing on Middle-Late Pleistocene humans
in the past have focused primarily on standard metrics (e.g., length,
breadth, crown indices) rather than morphology (Senyrek, 1959;
Thoma, 1963; Smith and Arensburg, 1977; Tillier, 1979, 1982, 1991;
Tillier et al., 1989). More recently, there has been a renewed inter-
est in deciduous dental variation especially in the context of dis-
tinguishing Homo neanderthalensis and Homo sapiens (Souday, 2008;
Bayle et al., 2010; Benazzi et al., 2011a, b).
In the context of human evolution, the deciduous teeth are
particularly important because they are generally accepted to be
morphologically conservative relative to their permanent successors
(Smith,1989; Smith and Tillier,1989). It is also believed that they may
provide a clearer picture of an individuals underlying genotype (i.e.,

http://dx.doi.org/10.1016/j.jhevol.2014.02.008
0047-2484/ 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
2 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9
one less muddied by environmental noise) than the permanent
morphology since they form more quickly and also earlier during
ontogeny; all are crown complete by the rst year (Liversidge and
Molleson, 1999). In addition, many fossil individuals are repre-
sented predominantly by the deciduous (versus permanent) denti-
tion (e.g., Mezmaiskaya, Kebara 1), and at some sites deciduous teeth
are the only human remains recovered (e.g., Grotta del Cavallo,
Blombos). The taxonomic afliation of such individuals is sometimes
scrutinized because of their immature status or because they are
represented only by (deciduous) teeth. Establishing differences
among hominin taxa, therefore, is of utmost importance.
A systematic and comparative study of non-metric dental traits
in the deciduous teeth of H. neanderthalensis and H. sapiens is
currently underway (Bailey, In preparation). Unfortunately some
important diagnostic traits like small accessory cusps and crests
can be obscured or obliterated with moderate wear. Analyses of
crown shape can, at least partially, circumvent this problem. For
example, in a follow up to Baileys (2004) study of permanent upper
rst molar shape differences between H. neanderthalensis and
H. sapiens based on cusp tip position, Gmez-Robles et al. (2007)
used geometric morphometric analysis of the crown outline in
conjunction with cusp tip landmarks to show similar shape dif-
ferences between the two species. A similar approach has been
somewhat successful in discriminating among the crown outlines
of hominin permanent second and third upper molars (Gmez-
Robles et al., 2012). In an application of these methods to the de-
ciduous teeth, Souday (2008) demonstrated important taxonomic
differences in the deciduous upper and lower second molars of
H. neanderthalensis and H. sapiens. Benazzi et al. (2012) also found
taxonomically important differences in the deciduous lower second
molar at the crown and cervical levels (as well as for other metric
traits such as lateral crown height and lateral dentine volume;
Benazzi et al., 2011a). In an application of these methods, Benazzi
et al. (2011b) used the crown outline of the deciduous upper rst
molar and cervical outline shape of the deciduous upper second
molar to determine that H. sapiens (rather than H. neanderthalensis)
were responsible for making the Uluzzian at Grotta del Cavallo.
These previous studies clearly demonstrate the potential of this
method for diagnosing certain fossil hominin taxa. However, they
are somewhat incomplete. Benazzi et al. (2011b) examined the
cervical outline, rather than the crown outline, of the deciduous
upper second molar from Grotta del Cavallo because the tooth was
quite worn. While we expect similar results to be obtained from the
crown outline based on Soudays earlier work (Souday, 2008), that
work has yet to be published. Moreover, neither of these studies
included a large comparative sample of recent H. sapiens in their
analysis. While this might not be imperative when the question at
hand is whether H. sapiens versus H. neanderthalensis were
responsible for a particular archaeological assemblage, it is
important for understanding human variability, trait polarity and
evolution within our own species. The present study rounds out,
rather than duplicates, these earlier studies, by including a large
geographically diverse sample of recent humans, as well as speci-
mens representing some of the early H. sapiens populations from
Africa and the Near East. In addition, we include two specimens
representing geographically distinct Homo erectus populations in
order to examine trait polarity of tooth shape.
First, we analyze the crown outlines of the upper second decid-
uous molar1 (hereafter upper dm2) to verify how well they separate
1
We are aware of the debate regarding whether to call human deciduous
postcanine teeth molars or premolars (e.g., deciduous m1 and m2 versus p3 and
p4). For consistency with the clinical and dental anthropological literature, we
prefer to refer to these teeth as deciduous m1 and m2.
Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
H. neanderthalensis from H. sapiens. We expect the distinction to be
as good or better than that found based on the cervical outline.
Second, we examine the strength of this distinction, and investigate
the aspects of shape that distinguish the two taxa. Third, we include
two H. erectus s.l. upper dm2s (one from Sangiran and one from
Tighenif) to examine their position vis--vis H. neanderthalensis and
H. sapiens. We predict that if the crown outline shape of
H. neanderthalensis is derived, as suggested by analyses of the per-
manent upper rst molar (Bailey, 2004; Gmez-Robles et al., 2007),
then the outlines of Tighenif and Sangiran should fall outside their
variation. They may fall within H. sapiens variation (if H. sapiens
retains the primitive condition) or they may cluster by themselves
(if H. sapiens is also derived but in a different way from
H. neanderthalensis). Finally, we undertake a linear discriminant
analysis (LDA) to determine how well the upper dm2 crown outline
predicts group membership. We also apply this LDA to the H. erectus
s.l. specimens to predict their likelihood of belonging to either the
H. neanderthalensis or H. sapiens groups based on the estimated
posterior probabilities of group membership.
Materials and methods
The fossil samples included in this study comprise 17
H. neanderthalensis, ve early H. sapiens, and 12 Upper Paleolithic
H. sapiens. About half of the H. neanderthalensis specimens come
from the site of Krapina (Croatia), while the remaining individuals
represent much of their geographic range including the Near East
(Kebara) and eastern Central Europe (Subalyuk). The early
H. sapiens sample includes specimens from both Africa and the Near
East. All of the Upper Paleolithic H. sapiens specimens date to the
Gravettian or later time periods. The recent H. sapiens sample in-
cludes 80 individuals representing Asia, the Americas, Africa, and
Europe (Table 1). In addition, we included in our analysis two
specimens from Sangiran and Tighenif, both attributed to H. erectus
s.l. (see below).
The crown preservation of teeth included in this analysis ranges
from unworn to moderately worn. In some cases, the mesial and/or
distal border had to be reconstructed. When necessary, care was
taken to follow the general contour of the tooth (Fig. 1). Broken or
badly chipped teeth were excluded from the analysis. The upper
dm2 from the left side was used when available but in its absence
the right tooth was used and then digitally mirror imaged to
represent the left.
Sangiran 7e13
The Sangiran upper dm2 is part of the G.H.R. von Koenigswald
collection curated at the Senckenberg Museum in Frankfurt am
Main, Germany. This collection of isolated teeth and jaw fragments
attributed to H. erectus was recovered from Pleistocene sediments
of the Sangiran Dome in central Java between 1937 and 1941. The
teeth are all surface nds. While the actual provenance is uncertain,
the hominin fossils collected by von Koenigswald and his team
most likely came from a section between the middle Pucangan and
the middle Kabuh, which dates to between 1.3 and 0.7 million years
(Matsuura, 1982; Grine and Franzen, 1994). This particular spec-
imen (7e13) has been associated with the Kabuh Formation (see
Table 1 in Grine and Franzen, 1994), which places it at the younger
end of this sequence (later Early Pleistocene).
Tighenif
The upper dm2 is one of nine isolated teeth (three of which are
deciduous) from the early Middle Pleistocene site of Tighenif
(formerly Ternine), Algeria. The material, which is curated at the
 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9 3

Table 1 been included into the H. erectus hypodigm (Howell, 1960; Tillier,
Deciduous upper second molars used in this analysis. 1980; Rightmire, 1990), more recently it has been suggested to
H. neanderthalensis (n 17) belong to Homo heidelbergensis s.l. (understood as a common
Arcy-sur-Cure GDRa 26 ancestor of H. neanderthalensis and H. sapiens) based on size and
Arcy-sur-Cure GDRa 45 morphology (Mounier et al., 2009; see also Antn, 2003). The site is
Arcy-sur-Cure GDBb B21
Cova Negra
currently dated to w700,000 years (Geraads et al., 1986).
La Ferrassie 8
Kebara 1
Krapina 45 Methods
Krapina 6 Maxilla B
Krapina 47 Images of recent humans (and most fossils) were taken with a
Krapina D185
Canon Digital Rebel XT camera (SEB, CS) and with a Nikon D80
Krapina D186
Krapina D188
digital camera with the built in macro setting (KSP). A previous
Krapina D189 study has shown that interobserver error in orienting tooth crowns
Krapina D190 is relatively low (0e5%) and not signicantly different from intra-
La Quina H18 observer error (Bailey et al., 2004). All teeth were oriented so that
Roc du Marsal
the cervical border was perpendicular to the optical axis of the
Subalyuk 2
camera. A scale was included in each image and both the scale and
Early H. sapiens (n 5) the camera were leveled using standard bubble devices. The
Die Kelders 6243 smallest aperture possible (dependant on lighting situation) was
Die Kelders 6244 used to maximize depth of eld. Images of some fossil material
Qafzeh 10
were taken from three-dimensional (3D) models based on mCT
Qafzeh 15
Skhul 1 scans obtained from the Max Planck Institute for Evolutionary
Anthropology and the Vienna micro-CT Lab (University of Vienna,
Upper Paleolithic H. sapiens (n 12) Austria). The scanning was conducted on both industrial and
Abri Pataud desktop microCT systems with resultant voxel resolutions ranging
Bruniquel II from 14 to 70 mm. The image stacks of each tooth were ltered
Cavallo-C
Combe-Capelle 3
(using a computer programmed macro that employs a three-
Kostenki 15 dimensional median and mean-of-least-variance lter) to
Lagar Velho improve tissue grayscale homogeneity and then manually
La Madeleine segmented into enamel and dentine components using Avizo
Le Figuier
(v6.0). The crown surface was extracted as a digital surface model
Le Veyrier 1
St. Germain B6 (.ply format), which could be manipulated in 3D for proper orien-
St. Germain B7 tation. The rst author loaded 3D models of the mCT scans into
Sunghir 3 Avizo, added a scale and oriented the tooth in both mesio-distal and
bucco-lingual directions. A screen shot of the occlusal surface was
Recent H. sapiens (80)
saved as a .jpg le.
Europe (Western) n 38
Asia (West Asia, SE Asia, India, Micronesia) n 6 Images were imported into Adobe Photoshop where they
Americas (North, Central and South) n 26 were oriented to approximate anatomical position. Where
Africa (South, West, East) n 10 necessary, backgrounds were removed and contrast was adjusted
a
Grotte du Renne. so that there was a clear distinction between crown and back-
b
Grotte de Bison. ground. Each image was scaled to approximately the same size
and resolution (300 dpi). Images of the occlusal surface of the
Department of Paleontology MNHN, Paris (France), also includes upper dm2s were then imported in Rhino 4.0 Beta CAD envi-
mandibular and cranial remains that were discovered between ronment (Robert McNeel & Associates, Seattle, WA) and aligned
1954 and 1956 by C. Arambourg (Arambourg, 1954; Arambourg and to the xy-plane of the Cartesian coordinate system. For each
Hoffstetter, 1954). While the Tighenif material has traditionally tooth, the crown outline was manually digitized using the spline

Figure 1. Range of wear in samples. Both images are from the recent human sample (left: Poundbury 21, right: East Africa 25106). Note some correction has been made to the mesial
aspect of the tooth on the right.

Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
4 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9

function, and then oriented with the lingual side parallel to the
x-axis.
All of the outlines were rst centered, superimposing the cen-
troids of their area. The outlines were represented by 24 pseudo-
landmarks obtained by equiangularly spaced radial vectors out of
the centroid. The rst radius is directed buccally and parallel to the
y-axis of the Cartesian coordinate system (Benazzi et al., 2011c).
Size information from the centered and oriented outlines was
removed with a uniform scaling of the pseudolandmark congu-
rations to unit centroid size (Benazzi et al., 2011a, b, 2012).
A principal components analysis (PCA) of the matrix of shape
coordinates was carried out for the upper dm2 crown outlines. The
two H. erectus s.l. specimens (Sangiran 7e13, Tighenif) were
considered to be taxonomically unknown, and their shape variables
were projected into the space built from the comparative sample to
assess their dental outline shapes with respect to the H. sapiens and
the H. neanderthalensis outline shape variation.
As variance was similar between the H. neanderthalensis and
H. sapiens [early H. sapiens (EHS), Upper Paleolithic (UPHS) and
recent H. sapiens (RHS) samples], we used leave-one-out cross-
validation linear discriminant analysis (LDA) of the rst seven
principal components that account for at least 90% of the total
variance to classify the specimens. The LDA was built up leaving
out the unknown specimens (Sangiran 7e13, Tighenif). Posterior
probabilities (Ppost) were calculated using equal prior probability
(Pprior) of 0.5 for H. neanderthalensis and H. sapiens groups (which
includes EHS, UPHS and RHS), and the unknown specimens were
tested through all of the iterations of leave-one-out cross-
validation LDAs. The data were processed and analyzed through
software routines written in R v. 2.15.1 (R Development Core
Team, 2012).
Results
Principal components analysis (PCA) is an exploratory tool to
visualize shape variation. Figs. 2 and 3 illustrate the results of the
shape-space PCA. In each case, a convex hull is used to circumscribe
the shape space occupied by the individuals in each sample
approximating the range of shape variation observed. The rst
three principal components account for 72.6% of the total variation
and provide the best separation when plotted against each other.
The rst principal component (PC1) accounts for 42.6% of the
variation. While there is overlap, H. neanderthalensis and H. sapiens
discriminate quite well along PC1 (Figs. 2 and 3). Specimens with
positive scores for PC1 include predominantly H. neanderthalensis.
They fall to the right of the graph and demonstrate a more exag-
gerated rhomboid outline with a protruding hypocone. Specimens
with negative scores for PC1 include predominantly H. sapiens.
They fall to the left of the graph and possess a more square
outline. Principal component 2 discriminates taxa less well,
although some differences are observed. A greater proportion of
H. neanderthalensis specimens have positive scores, while a greater
proportion of H. sapiens have negative scores. The shape difference
along PC2 is more difcult to interpret but appears to correspond to
reduction of the mesio-lingual portion of the crown outline (related

Figure 2. Results of the principal components analysis. PC1 plotted against PC2. Red triangle: H. neanderthalensis e N; pink cross: Early H. sapiens-EHS; blue square: Upper
Paleolithic H. sapiens-UPHS; black dot: recent H. sapiens-RHS; green X: H. erectus-HE. (For interpretation of the references to color in this gure legend, the reader is referred to the
web version of this article.)

Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9 5

Figure 3. Results of the principal components analysis. PC1 plotted against PC3. Symbols are as in Figure 2.

to the protocone cusp) and a less swollen distal side along the
negative axis.
Fig. 2 plots PC1 against PC2. In this two-dimensional space, a
number of H. sapiens specimens fall within the H. neanderthalensis
range of shape variability; most of these were sampled from recent
populations. Two exceptions include Bruniquel (UPHS) and Skhu l 1
(EHS). Likewise, two H. neanderthalensis specimens (La Quina H18
and Arcy GDR 45) fall within the H. sapiens distribution. The virtual
overlap of Arcy GDR 45 and Bruniquel specimens reects their
overall similarity in outline shape. The position of Skhu  l I within
H. neanderthalensis variation reects its exceptionally large hypo-
cone combined with retention of a large metacone. Both the San-
giran 7e13 and Tighenif molars t comfortably within the
H. sapiens shape space. Their position reects a more neutral shape,
being neither hyper skewed like many H. neanderthalensis nor
exceptionally reduced like many recent H. sapiens.
Principal components 2 and 3 account for nearly the same
amount of variation (15.9% and 14.1%, respectively), and a plot of PC1
against PC 3 shows clear separation between H. sapiens and
H. neanderthalensis (Fig. 3). With a single exception, the
H. neanderthalensis specimens fall on the negative axis for PC3. This
appears to correspond to disto-buccal reduction relating to their
relatively small metacone. Their negative scores for PC3 combined
with positive scores for PC1 place them in the lower right quadrant of
the gure. The H. sapiens specimens are more variable but only six
specimens fall in the lower right quadrant. One of these (Bruniquel)
falls within the H. neanderthalensis shape space. In this plot, the
H. neanderthalensis specimen Arcy GDB 21B falls within the H. sapiens
range of shape variability, while Arcy-sur-Cure 45 plots with other
H. neanderthalensis specimens. In addition, the positive score for PC3
(reecting its larger metacone) plots Skhu l 1 with other H. sapiens in
the upper right quadrant of the gure, fairly distant from the
H. neanderthalensis specimens. In this plot, the Tighenif and Sangiran
molars both fall within the H. sapiens shape space.
In order to investigate the patterning of geographic variation in
the recent H. sapiens sample, we have removed the fossil specimens
in Figs. 4 and 5 and present the PCA results of the recent H. sapiens
only. Fig. 4 plots PC1 against PC2 and shows a scattering of in-
dividuals with no discernible pattern. Fig. 5 plots PC1 against PC3
and does show some patterning to the geographic samples. In this
plot, the European sample is fairly well separated from the Native
American sample, while the African and Asian samples are
randomly scattered on all three principal components.
Since PCA is an exploratory tool, it is important to support our
observations with more advanced statistical analysis. Therefore, we
employed discriminant analysis (LDA) to conrm whether or not
our PCA plots accurately capture the differences between groups.
Results of the LDA are based on the rst seven PCs, which together
account for more than 90% of the total variance. Of the 114 in-
dividuals, 96.5% are correctly classied (94.1% of H. neanderthalensis
and 96.9% of H. sapiens). Of the correctly classied, 84% of the
H. sapiens individuals and 94% of the H. neanderthalensis individuals
are classied with posterior probabilities above 90%. Nearly all of
the remaining correctly classied specimens had posterior proba-
bilities above 75%. The exceptions are a recent H. sapiens individual
from the Poundbury collection (65.0%); Skhu  l 1, an early H. sapiens
individual (65.5%); and La Quina H18 a H. neanderthalensis
individual (58%). The Sangiran upper dm2 is classied as
H. neanderthalensis with a low posterior probability (54.0%), while
the Tighenif upper dm2 is classied as H. sapiens with a very high
probability (99.1%). We did not examine the correct classication of
H. sapiens individuals to their temporal group (early, Upper

Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
6 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9

Figure 4. Results of the principal components analysis showing distribution of recent humans only. PC1 is plotted against PC2. There is no geographic patterning of variation. (Black
dot: European e EU; red triangle: Native American e AM; green square: African e AF; blue cross: Asian e AS). Note: The scale of PC1 is different from that in Figures 2 and 3. (For
interpretation of the references to color in this gure legend, the reader is referred to the web version of this article.)

Paleolithic, or recent) because the complete overlap between Upper
Paleolithic and recent human samples in the PCA plots suggests
that their outlines are basically the same and we would predict very
little success in discriminating among H. sapiens groups.
Discussion
This analysis demonstrates that H. neanderthalensis and
H. sapiens can be distinguished quite well in shape space PCA based
on the crown outline of the upper dm2. This is not surprising given
the results of Benazzi et al. (2011b), which showed no overlap be-
tween the upper dm2 cervical outlines of Upper Paleolithic
H. sapiens and H. neanderthalensis. The present study of crown
outlines also demonstrates very strong separation between the
Upper Paleolithic H. sapiens and H. neanderthalensis specimens,
with only one Upper Paleolithic specimen (Bruniquel) falling
within the H. neanderthalensis range of shape variability. Moreover,
as already suggested by Benazzi et al. (2011b), the specimen
Cavallo-C (from the Uluzzian deposit of Grotta del Cavallo) falls
within the H. sapiens range of variation.
However, the current analysis also shows that when recent
H. sapiens specimens are included in the analysis, there is greater
overlap in shape space between the two groups. That being said, the
LDA provides excellent classication results (>95% correct assign-
ment) with overwhelmingly high posterior probabilities. We
conclude, therefore, that the crown outline shape of the upper dm2
can be used very successfully to identify the taxonomic assignment of
isolated teeth when the choice is H. neanderthalensis versus H. sapiens.
One of the aspects of this study that distinguishes it from previous
studies is the inclusion of a large geographically diverse recent hu-
man sample. While it is possible that the principal components re-
sults might reect the geographic patterning of the recent human
samples, the random scatter of recent humans along PC1 and PC2
suggest that neither reects aspects of geographic variation. Prin-
cipal component 3, however, does appear to reect some of this
recent human geographic variation. This principal component sep-
arates European and Native American samples (but not African and
Asian), which are two of the most divergent populations in aspects of
their permanent tooth crown morphology as well (Irish, 1998).
Before discussing the Tighenif and Sangiran teeth, we think it is
informative to examine more closely the individuals that were mis-
classied in the LDA (see Fig. 6 for images of misclassied teeth). One
of the 17 H. neanderthalensis specimens was misclassied. This tooth,
Arcy GDB B21, demonstrates unusual crown morphology with a very
large Carabellis cusp that blends into a large hypocone. There is no
separation of the two features on the lingual side of the tooth. This
unusual morphology gives the tooth a square (but not particularly
modern) appearance. Interestingly, the La Quina (H18) Neandertal
also shows this unusual morphology and it classies as
H. neanderthalensis with a relatively low posterior probability (58%).
The Upper Paleolithic specimen from Bruniquel classied as a
H. neanderthalensis with a 70% posterior probability. The tooth

Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9 7

Figure 5. Results of the principal components analysis showing distribution of recent humans only. PC1 is plotted against PC3. In this plot there is some separation of European (EU)
and Native American (AM) groups along PC3, but there is no pattern to the distribution of African (AF) or Asian (AS) groups. Symbols are as in Figure 4.

possesses a large hypocone, which contributes to its somewhat
skewed shape; however, an examination of the relative cusp areas
does not show the relatively small metacone/large hypocone
combination that is characteristic of H. neanderthalensis upper dm2
(Bailey, Unpublished data).
The remaining misclassied individuals were recent humans.
Two were from the Romano-British site of Poundbury and one was
from South Africa. Only one of these had a relatively high posterior
probability of belonging to the H. neanderthalensis group (81%). Like
the Bruniquel specimen, this individual (Poundbury #321) pos-
sesses a large hypocone resulting in a somewhat skewed outline,
but possesses relative cusp areas that align it with H. sapiens
(relatively smaller hypocone and larger metacone).
Sangiran
The Sangiran 7e13 crown exhibits a slightly skewed outline
reecting distal cusps that are equal in size but about 25% smaller
than the mesial cusps. It lacks the hypertrophied hypocone and
reduced metacone of H. neanderthalensis, resulting in a shape that
falls at the edge of the H. neanderthalensis range of variation (Fig. 2)
and comfortably within the H. sapiens range of variation (Figs. 2 and
3). The four main cusps show a derived (later Homo)
paracone > metacone relationship (Quam et al., 2009) but a
primitive metacone  hypocone relationship (Bailey, 2004). The
tooth lacks a cusp 5 as well as Carabellis trait. The lack of a cusp 5
on the upper dm2 is not unusual for H. neanderthalensis or
H. sapiens but the lack of a Carabellis trait on the upper dm2 is
(Bailey, Unpublished data). Given its rather neutral shape, it is not
surprising that its classication is somewhat ambiguous (54%
posterior probability of belonging to H. neanderthalensis).
Tighenif
Like Sangiran 7e13, the Tighenif upper dm2 possesses a distal
half that is smaller than the mesial half. Its crown shape is more
square than Sangiran 7e13 and its relatively neutral position in
Fig. 2 reects this: it ts comfortably within the H. sapiens shape
variation and just outside the shape space encompassed by
H. neanderthalensis specimens. In the plot of PC1 and PC3 (Fig. 3), its
position well within the H. sapiens shape space and far from
H. neanderthalensis specimens reects its relatively large metacone
and reduced hypocone, which is relatively smaller than that of
Sangiran 7e13. Like Sangiran 7e13, the tooth lacks a cusp 5, but
unlike the Sangiran tooth it shows weak Carabellis expression
(grade 3) and its paracone and metacone are approximately the
same size.
In sum, both H. erectus s.l. upper dm2 crown outlines are in-
termediate between the two extremes, occupying somewhat
neutral positions in shape space (i.e., they lack either the marked
hypocone reduction in many H. sapiens or the marked hypocone
hypertrophy in many H. neanderthalensis). This might be predicted
if the crown outline shape of H. erectus s.l. preserves the primitive
condition. Based on their positions in PC shape space, many of the
H. sapiens specimens also possess this primitive shape, whereas a
greater proportion of H. neanderthalensis specimens are more

Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
8 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9

Figure 6. Arcy-sur-Cure GDR B21 (a) was misclassied as H. sapiens and La Quina H18 (b) classied correctly as H. neanderthalensis but with a low posterior probability (see text).
Both demonstrate an exceptionally large Carabellis cusp that is incorporated into the hypocone. This results in a squarer outline. The Upper Paleolithic specimen from Bruniquel (c)
was misclassied as H. neanderthalensis and the recent specimen from Poundbury (d) classied correctly as H. sapiens but with relatively low posterior probability (see text).

extreme (and thus are likely derived). The nding that the Tighenif
tooth classied as H. sapiens with a very high posterior probability
(99.9%) was unexpected. However, a recent analysis of enamel
thickness of this same tooth also demonstrated a closer structural
similarity to H. sapiens than to H. neanderthalensis (Zanolli et al.,
2010). Unfortunately, there is no large body of comparative data
for H. erectus or H. heidelbergensis/rhodesiensis deciduous dental
morphology, external or internal, and so it is difcult to place these
specimens into a larger context.
Conclusions
We nd that analysis of the shape of the upper dm2 crown
outline is an excellent tool for discriminating between
H. neanderthalensis and H. sapiens. However, it would not be a
useful method for discriminating between H. erectus (and perhaps
H. heidelbergensis/rhodesiensis, if the Tighenif upper dm2 belongs to
this taxon; see considerations below) and H. sapiens. In the cases
when upper dm2 crown outlines fall in the area of overlap between
H. sapiens and H. neanderthalensis, occlusal crown morphology (in
particular relative cusp areas and occlusal polygon area, but also
minor morphological variants like cusp 5 and Carabellis trait) can
provide important taxonomic information.
We believe that the analysis of the H. erectus upper dm2 pro-
vides support for the conclusion that the skewed upper dm2 crown
shape is derived for H. neanderthalensis and members of their
lineage. A similar conclusion has been suggested for the upper M1,
(Bailey, 2004; Gmez-Robles et al., 2007). A recent study
comparing these two teeth conrms that the upper dm2 and M1
have the same basic shape, even though the upper M1 is even more
extreme in its skew than the dm2 (Bailey et al., in press). Previous
studies of recent humans also suggest morphological similarity
between the dm2 and M1 based on non-metric and morphometric
traits (Edgar and Lease, 2007; Paul and Bailey, 2013).
As for the H. erectus specimens, the African and Asian H. erectus
specimens in this study show differences in the upper dm2 crown
outline that may be attributable to geographic and/or temporal
variation. However, these differences may have phylogenetic
meaning as well. The strong similarity of the Tighenif tooth to
H. sapiens might be interpreted to support the suggestion that the
Tighenif material belongs in the taxon H. heidelbergensis s.l.
(Mounier et al., 2009), but only if H. heidelbergensis is viewed as the
common ancestor to both H. neanderthalensis and H. sapiens (sensu
Rightmire, 2008; see also Hublin, 2009). So far as we know, the
oldest specimens attributed to H. heidelbergensis or Homo rhode-
siensis date to approximately 600,000 years ago (Bischoff et al.,
2007). If the Tighenif material also belongs to this taxon, it would
push this date back even further into the past. Alternatively, the
Tighenif material may, indeed, belong in the taxon H. erectus s.l., but
if future analyses show similar differences between African and
Asian morphs in crown morphology, this would support hypothe-
ses that the Asian morph represents an evolutionary dead end,
leaving the African morph to contribute exclusively (or at least
predominantly) to later human evolution.

Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
 S.E. Bailey et al. / Journal of Human Evolution xxx (2014) 1e9
Acknowledgments
We would like to thank Ottmar Kullmer for making the cast of
the Sangiran 7e13 tooth and Tim Bromage for transporting it to
New York University. We also thank Heiko Temming and Matt
Skinner for making and processing the 3D scans used in this
analysis, and Laura Buti for helping in digitizing the crown outlines.
This research was funded by the L.S.B. Leakey Foundation (SEB) and
also by the Max Planck Society while the rst author was in
Germany.
References
Antn, S.C., 2003. Natural history of Homo erectus. Yearb. Phys. Anthropol. 46,
126e170.
Arambourg, C., 1954. LHominien fossile de Ternine (Algrie). C. R. Acad. Sci. 239,
893e894.
Arambourg, C., Hoffstetter, R., 1954. Dcouverte en Afrique du Nord de restes
humains du Palolithique infreur. C. R. Acad. Sci. 239, 71e74.
Bailey, S.E., 2004. A morphometric analysis of maxillary molar crowns of Middle-
Late Pleistocene hominins. J. Hum. Evol. 47, 183e198.
Bailey, S.E., 2006. Beyond shovel shaped incisors: Neandertal dental morphology in
a comparative context. Period. Biol. 108 (3), 253e267.
Bailey, S.E., Hublin, J.-J., 2006. Dental remains from Grotte du Renne at Arcy-sur-
Cure (Yonne). J. Hum. Evol. 50, 485e508.
Bailey, S.E., Pilbrow, V.C., Wood, B.A., 2004. Interobserver error involved in inde-
pendent attempts to measure cusp base areas of Pan M1s. J. Anat. 205, 323e331.
Bailey, S.E., Glantz, M.M., Weaver, T.D., Viola, B., Krivoshapkin, A., Wrinn, P.J., 2006.
The taxonomic afnity of the Obi-Rakhmat dentition. In: von Koenigswald, W.,
Litt, T. (Eds.), 150 Years of Neanderthal Discoveries: Early Europeans e Conti-
nuity and Discontinuity. GeoUnion Alfred-Wegener-Stiftung, Bonn.
Bailey, S.E., Benazzi, S., Hublin, J.-J., 2014. Allometry, merism and tooth shape of the
upper deciduous M2 and permanent M1. Am. J. Phys. Anthropol.. http://
dx.doi.org/10.1002/ajpa.22477 (in press).
Bayle, P., Macchiarelli, R., Trinkaus, E., Duarte, C., Mazurier, A., Zilho, J., 2010. Dental
maturational sequence and dental tissue proportions in the early Upper
Paleolithic child from Abrigo do Lagar Velho, Portugal. Proc. Natl. Acad. Sci. 107
(4), 1338e1342.
Benazzi, S., 2012. The rst modern Europeans. J. Anthropol. Sci. Rivista di
antropologia : JASS/Istituto italiano di antropologia 90, 3e6.
Benazzi, S., Fornai, C., Bayle, P., Coquerelle, M., Kullmer, O., Mallegni, F., Weber, G.W.,
2011a. Comparison of dental measurement systems for taxonomic assignment
of Neanderthal and modern human lower second deciduous molars. J Hum
Evol. 61, 320e326.
Benazzi, S., Douka, K., Fornai, C., Bauer, C.C., Kullmer, O., Svoboda, J., Pap, I.,
Mallegni, F., Bayle, P., Coquerelle, M., Condemi, S., Ronchitelli, A., Harvati, K.,
Weber, G.W., 2011b. Early dispersal of modern humans in Europe and impli-
cations for Neanderthal behaviour. Nature 479, 525e528.
Benazzi, S., Coquerelle, M., Fiorenza, L., Bookstein, F., Katina, S., Kullmer, O., 2011c.
Comparison of dental measurement systems for taxonomic assignment of rst
molars. Am. J. Phys. Anthropol. 144 (3), 342e354.
Benazzi, S, Fornai, C., Buti, L., Toussaint, M., Mallegni, F., Ricci, S., Gruppioni, G.,
Weber, G., Condemi, S., Ronchitelli, A., 2012. Cervical and crown outline analysis
of worn Neanderthal and modern human lower second deciduous molars. Am J
Phys. Anthropol. 149, 537e546.
Bermdez de Castro, J.M., Rosas, A., Nicols, M.E., 1999. Dental remains from Ata-
puerca e TD6 (Gran Dolina, site Burgos, Spain). J. Hum. Evol. 37 (3/4), 523e566.
Bischoff, J., Williams, R.W., Rosenbauer, R.J., Aramburu, A., Arsuaga, J.L., Garcia, N.,
Cuenca-Bescos, G., 2007. High-resolution U-series dates from the Sima de los
Huesos hominids yields 600 N/e66 kyrs: implications for the evolution of the
early Neanderthal lineage. J. Archaeol. Sci. 34 (5), 763e770.
Edgar, H., Lease, L., 2007. Correlations between deciduous and permanent tooth
morphology in a European sample. Am. J. Phys. Anthropol. 133, 726e734.
Geraads, D., Hublin, J.-J., Jaeger, J.J., Tong, J., Sen, S., Toubeau, P., 1986. The Pleistocene
hominid site of Ternine, Algeria: New results on the environment, age and
human industries. Quatern. Res. 25, 380e386.
Gmez-Robles, A., Martinn-Torres, M., Bermdez de Castro, J.M.,
Margvelashvili, A., Bastir, M., Arsuaga, J.L., Prez-Prez, A., Estebaranz, F.,
Martnez, L.M., 2007. A geometric morphometric analysis of hominin upper rst
molar shape. J. Hum. Evol. 55 (4), 627e638.
Gmez-Robles, A., Bermdez de Castro, J.M., Martinn-Torres, M., Prado-Simon, L.,
Arsuaga, J.L., 2012. A geometric morphometric analysis of hominin upper sec-
ond and third molars, with particular emphasis on European Pleistocene pop-
ulations. J. Hum. Evol. 63 (3), 512e526.
Grine, F.E., 1984. Comparisons of the deciduous dentitions of African and Asian
hominids. Cour. Forsch.-Inst. Senckenberg 69, 69e82.
Please cite this article in press as: Bailey, S.E., et al., Taxonomic differences in deciduous upper second molar crown outlines of Homo sapiens,
Homo neanderthalensis and Homo erectus, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.02.008
9
Grine, F.E., 1985. Australopithecine evolution: The deciduous dental evidence. In:
Delson, E. (Ed.), Ancestors: The Hard Evidence. Alan R. Liss, Inc., New York,
pp. 153e167.
Grine, F.E., Franzen, J.L., 1994. Fossil hominid teeth from the Sangiran Dome (Java,
Indonesia). Cour. Forsch.-Inst. Senckenberg 171, 75e103.
Harvati, K., Panagopoulou, E., Karkanas, P., 2003. First Neanderthal remains from
Greece: the evidence from Lakonis. J. Hum. Evol. 45 (6), 465e473.
Howell, F.C., 1960. European and Northwest African Middle Pleistocene Hominids.
Curr. Anthropol. 1 (3), 195e232.
Hublin, J.-J., 2009. The origin of Neandertals. Proc. Natl. Acad. Sci. 106 (38),
16022e16027.
Irish, J., 1998. Ancestral dental traits in recent sub-Saharan Africans and the origins
of modern humans. J. Hum. Evol. 34, 81e98.
Kaifu, Y., Aziz, F., Baba, H., 2005. Hominid mandibular remains from Sangiran:
1952e1986 collection. Am. J. Phys. Anthropol. 128 (3), 497e519.
Liversidge, H.M., Molleson, T., 1999. Deciduous tooth size and morphogenetic elds
in children from Christ Church, Spitalelds. Arch. Oral Biol. 44, 7e13.
Martinn-Torres, M., Bermdez de Castro, J., Gmez-Robles, A., Margvelashvili, A.,
Prado, L., Lordkipanidze, D., Vekua, A., 2008. Dental remains from Dmanisi
(Republic of Georgia): Morphological analysis and comparative study. J. Hum.
Evol. 55, 249e273.
Martinn-Torres, M., Bermdez de Castro, J.M., Gmez-Robles, A., Prado-Simn, L.,
Arsuaga, J.L., 2012. Morphological description and comparison of the dental re-
mains from Atapuerca-Sima de los Huesos site (Spain). J. Hum. Evol. 62 (1), 7e58.
Matsuura, S., 1982. A chronological framing for the Sangiran hominids: fundamental
study by the uorine dating method. Bull. Natl. Sci. Mus. Tokyo D 8, 1e53.
Mounier, A., Marchal, F., Condemi, S., 2009. Is Homo heidelbergensis a distinct spe-
cies? New insight on the Mauer mandible. J. Hum. Evol. 56, 219e256.
Paul, K., Bailey, S.E., 2013. Comparative analysis of intercusp dimensions and crown
morphology between the deciduous second molar and permanent rst molar
within the same maxillary arcade. Am. J. Phys. Anthropol. 147 (S54), 217.
Quam, R.M., Bailey, S.E., Wood, B.A., 2009. Evolution of M1 crown size and cusp
proportions in the genus Homo. J. Anat. 214, 655e670.
Rightmire, G., 1990. The Evolution of Homo erectus: Comparative Anatomical
Studies of an Extinct Human Species. Cambridge University Press, Cambridge.
Rightmire, G.P., 2008. Homo in the Middle Pleistocene: hypodigms, variation and
species recognition. Evol. Anthropol. 17, 8e21.
Senyrek, M.S., 1959. A study of the deciduous teeth of the fossil Shanidar infant: a
comparative study of the milk teeth of fossil men. Publications of the Faculty of
Languages, History and Geography of the University of Ankara, 174 p.
Smith, P., 1989. Dental evidence for phylogenetic relationships of Middle Paleolithic
hominids. In: Otte, M. (Ed.), LHomme de Nandertal. Universit de Lige, Lige,
pp. 111e120.
Smith, P., Arensburg, B., 1977. A Mousterian Skeleton from Kebara Cave. Eretz, Israel,
pp. 164e176.
Smith, P., Tillier, A.M., 1989. Additional infant remains from the Mousterian Strata,
Kebara Cave (Israel). In: Bar-Yosef, O., Vandermeersch, B. (Eds.), Investigation in
South Levantine Prehistory, British Archaeological Reports International Series.
Archaeopress, Oxford.
Souday, C., 2008. Analyse morphomtrique des molaires dciduales et dnitives
dans le genre Homo: prespectives phylogntiques et biogographiques [Doc-
teur]. Musum National dHistoire Naturelle, Paris.
Team R, 2012. R: a language and environment for statistical computing. R Foun-
dation for Statistical Computing, Vienna.
Thoma, A., 1963. The dentition of the Subalyuk Neandertal child. Z. Morph.
Anthropol. 54, 127e150.
Tillier, A.M., 1979. Le dentition de lenfant moustrien Chteauneuf 2 dcouverte a
lAbi de Hauteroche (Charente). LAnthropologie 83, 417e438.
Tillier, A.M., 1980. Les dents denfant de Ternine (Plistocne Moyen dAlgrie).
LAnthroplogie 84 (3), 413e421.
Tillier, A.M., 1982. Les enfants nandertaliens de Devils Tower (Gibraltar). Z. Morph.
Anthropol. 73 (2), 125e148.
Tillier, A.M., 1991. Le mandible et les dents. Le Squelette Mousterian de Kebara, vol.
2. CNRS, Paris.
Tillier, A.-M., Arensburg, B., Duday, H., 1989. La mandibule et les dents du nean-
dertalien de Kebara (Homo 2) Mont Carmel, Israel. Paleorient 15, 39e58.
Wood, B.A., Abbott, S.A., 1983. Analysis of the dental morphology of Plio-Pleistocene
hominids. I. Mandibular molars: crown area measurements and morphological
traits. J. Anat. 136, 197e219.
Wood, B.A., Engleman, C.A., 1988. Analysis of the dental morphology of Plio-Pleistocene
hominids. V. Maxillary postcanine tooth morphology. J. Anat. 161, 1e35.
Wood, B.A., Uytterschaut, H., 1987. Analysis of the dental morphology of Plio-
Pleistocene hominids. III. Mandibular premolar crowns. J. Anat. 154, 121e156.
Wood, B.A., Abbott, S.A., Graham, S.H., 1983. Analysis of the dental morphology
of Plio-Pleistocene hominids. II. Mandibular molars e study of cusp
areas, ssure pattern and cross sectional shape of the crown. J. Anat. 137,
287e314.
Zanolli, C., Bayle, P., Macchiarelli, R., 2010. Tissue proportions and enamel thickness
distribution in the early Middle Pleistocene human deciduous molars from
Tighenif, Algeria. C. R. Palevol 9 (6e7), 341e348.