-
ol
hilipaMax Planck Institute for Evolutionary Anthropology,
DbAnthropology Ph.D. Program, City University of New YcNew York
Consortium in Evolutionary Primatology, USd Paleoanthropology,
Department of Early Prehistory andRmelinstr. 23, 72070 Tbingen,
Germany
a r t i c l e i n f o
Article history:Received 24 December 2011Accepted 8 August
2012Available online 11 September 2012
features, variously aligning them with Homo erectus sensu lato,
H.neanderthalensis and H. sapiens. The most complete faces
include
breadth, and details of the nasal margin and palate (Stringer,
1974;Arsuaga et al., 1997; Rightmire, 1998, 2008; Trinkaus, 2003,
2006;Athreya, 2009). They also share several facial features with
Nean-derthals, such as facial prognathism, broad nasal apertures,
anda lack of concavity in the infraorbital region (Rak, 1986;
Trinkaus,1987, 2003, 2006; Arsuaga et al., 1997; Harvati et al.,
2010).
Striking differences between MPhs, Neanderthals and recentmodern
humans occur in their facial size and robusticity. Inparticular,
Bodo, Petralona and Kabwe are characterized by their
* Corresponding author.E-mail addresses:
[email protected], [email protected]
(S.E. Freidline), [email protected] (P. Gunz),
[email protected](K. Harvati),
[email protected] (J.-J. Hublin).1 Present address: Max Planck
Institute for Evolutionary Anthropology, Depart-
Contents lists available at
Journal of Hum
journal homepage: www.el
Journal of Human Evolution 63 (2012) 723e740ment of Human
Evolution, Deutscher Platz 6, Leipzig 04103, Germany.differences
between Neanderthals and Middle Pleistocene humans are due to
scaling along a sharedallometric trajectory. These features include
aspects of the frontal bone, browridge morphology, nasalaperture
size and facial prognathism. Infraorbital surface topography and
orientation of the midface inthe European Middle Pleistocene
hominins is intermediate between the African Middle Pleistocene
andNeanderthal condition. This could suggest that the European
Middle Pleistocene hominins displayincipient Neanderthal
features.
2012 Elsevier Ltd. All rights reserved.
Introduction
The Eurasian and African Middle Pleistocene hominins (MPh)are
characterized by a combination of craniofacial morphological
Bodo and Kabwe (i.e., Broken Hill) from Africa, and Arago 21,
Pet-ralona, and Sima de los Huesos 5 from Europe. MPh specimens
arecharacterized bymassive facial bones, broad upper faces,
projectingbrowridges, especially in the lateral region, large
interorbitalKeywords:AllometryFaceOntogenyHomo
heidelbergensisNeanderthalsSemilandmark geometric
morphometrics0047-2484/$ e see front matter 2012 Elsevier
Ltd.http://dx.doi.org/10.1016/j.jhevol.2012.08.002epartment of
Human Evolution, Deutscher Platz 6, Leipzig 04103, Germanyork
Graduate School, 365 Fifth Avenue, NY 10016, USAAQuaternary
Ecology, Eberhard Karls Universitt Tbingen and Senckenberg Center
for Human Evolution and Paleoecology,
a b s t r a c t
Neanderthals and modern humans exhibit distinct facial
architectures. The patterning of facialmorphology of their
predecessors, the Middle Pleistocene humans, is more mosaic showing
a mix ofarchaic and modern morphologies. Signicant changes in
facial size and robusticity occurred throughoutPleistocene human
evolution, resulting in temporal trends in both facial reduction
and enlargement.However, the allometric patterning in facial
morphology in archaic humans is not well understood. Thisstudy
explores temporal trends in facial morphology in order to gain a
clearer understanding of thepolarity of features, and describes the
allometric patterning of facial shape.The modern human sample
comprises cross-sectional growth series of four morphologically
distinct
human populations. The fossil sample covers specimens from the
Middle Pleistocene to the UpperPaleolithic. We digitized landmarks
and semilandmarks on surface and computed tomography scans
andanalyzed the Procrustes shape coordinates. Principal component
analyses were performed, andProcrustes distances were used to
identify phenetic similarities between fossil hominins. In order
toexplore the inuence of size on facial features, allometric
trajectories were calculated for fossil andmodern human groups, and
developmental simulations were performed.We show that facial
features can be used to separate Pleistocene humans into temporal
clusters. The
distinctly modern human pattern of facial morphology is already
present around 170 ka. Species- andpopulation-specic facial
features develop before two years of age, and several of the
large-scale facialSarah E. Freidline a,b,c,d,*,1, P p Gunz a,
Katerina Harvati b,c,d, Jean-Jacques Hublin aMiddle Pleistocene
human facial morphand developmental contextAll rights reserved.ogy
in an evolutionary
SciVerse ScienceDirect
an Evolution
sevier .com/locate/ jhevol
-
umamassive facial bones compared with Neanderthals and
recentmodern humans (Rightmire, 1998), and both the MPhs and
Nean-derthals have longer and more prognathic faces than
recentmodern humans (Trinkaus, 2003). To what extent the
facialdifferences among recent modern humans, MPhs, and
Neander-thals are related to facial size is uncertain.
Allometry, as dened by Gould (1966), is the study of size and
itsconsequences. Conventionally, it is used to investigate the
rela-tionship between the total body size of the organism and its
shape,anatomy, and physiology among other characteristics
(Gould,1966). Julian Huxley (1932) introduced the concept of
allometryinto studies of growth, evolution and function, and later
S.J. Gouldsseminal work in both allometry (e.g., Gould, 1966, 1975)
and het-erochrony (e.g., Gould, 1968, 1977), the dissociation of
size, shapeand age (Gould, 1977; Alberch et al., 1979), set the
framework forcomparative allometric ontogenetic investigations
among livingand extinct organisms. Since Gould, a substantial body
of workinvestigating heterochrony and growth allometry in human
andnon-human primates has accumulated (e.g., Shea, 1981, 1983;
Leighand Cheverud, 1991; Ravosa, 1991, 1998; Collard and
OHiggins,2001; Penin et al., 2002; Leigh et al., 2003; Berge and
Penin,2004; Strand Viarsdttir and Cobb, 2004; Mitteroecker et
al.,2004, 2005; Leigh, 2006; Lieberman et al., 2007; Bruner
andRipani, 2008; Gonzalez et al., 2011), however studies on
fossilhominins are less common.
Rosas (1997, 2000) and Rosas and Bastir (2004) identiedseveral
features on the Middle Pleistocene Sima de los Huesos (SH)mandibles
associated with an increase in size, including the pres-ence of a
retromolar space, the curvature and orientation of thesymphysis,
and the position of the mental foramen with respect tothe
dentition. Similarly, in their geometric morphometric study
onmodern human and Neanderthal mandibular shape, Nicholson
andHarvati (2006) found that the retromolar gap was related to
anincrease in mandibular size. Size-correlated shape changes in
laterhominins and recent modern humans have also been observed
inthe relative breadth of the nasal aperture (Rosas and Bastir,
2002;Holton and Franciscus, 2008), nasoglabellar prole (Rosas
andBastir, 2002), alveolar prognathism (Rosas and Bastir, 2002),
andinfraorbital surface topography (Maddux and Franciscus, 2009).
Inthe latter study, Maddux and Franciscus (2009) identied an
allo-metric relationship between infraorbital size and surface
topog-raphy within Middle to Late Pleistocene Homo and
modernhumans. They found that individuals with large infraorbital
regionstend to exhibit at, or inated, surface topographies
(characteristicof Neanderthals), while individuals with small
infraorbital areaspossess depressed surface topographies (like
modern humans).They argued that depressed versus inated
infraorbital shapes arenot dichotomous congurations, but fall along
a continuous sizegradient. Together, these studies demonstrate that
some Neander-thal apomorphies (e.g., retromolar space and
infraorbital ination)are size-correlated.
However, a major limitation to several of the studies
mentionedabove is the lack of ontogenetic data. Without a
developmentalgrowth series, these studies can only demonstrate that
there areallometric shape changes among adults (i.e., static
allometry). Anunderstanding of the developmental basis of
morphologicalfeatures is crucial to interpreting the taxonomic
importance ofcharacters because features that develop earlier in
ontogeny arethought to be less susceptible to epigenetic factors,
or less likely torespond to exposure to environmental effects
(Lieberman et al.,1996, 2002; Wood and Lieberman, 2001; but see;
Roseman et al.,2010).
Due to a growing body of ontogenetic studies, it is
becomingincreasingly clear that taxon-specic craniofacial
morphology
S.E. Freidline et al. / Journal of H724among hominin species
developed prenatally or very earlypostnatally (e.g., Ponce de Len
and Zollikofer, 2001; Ackermannand Krovitz, 2002; Lieberman et al.,
2002; Strand Viarsdttiret al., 2002; Williams et al., 2002;
Krovitz, 2003; Bastir and Rosas,2004; Mitteroecker et al., 2004;
McNulty et al., 2006; Gunz et al.,2010, 2012; Gunz, 2012). These
morphometric studies largelysupport descriptive research
identifying unique Neanderthalmorphology at an early age (e.g.,
Tillier, 1989, 2011; Rak et al., 1994;Akazawa et al., 1995). For
example, at birth the ear labyrinth ofNeanderthals are different in
size and shape when compared withmodern humans (Hublin et al.,
1996; Ponce de Len and Zollikofer,1999), and by at least two years
of age Neanderthal features on theoccipital, such as the suprainiac
fossa and a bilaterally protrudingoccipital torus, have already
developed (Hublin,1980). Additionally,studies have shown that at
the time of birth, the face of a Nean-derthal is already larger
than that of a modern human (Ponce deLen and Zollikofer, 2001;
Ponce de Len et al., 2008; Zollikoferand Ponce de Len, 2010; Gunz
et al., 2010, 2011, 2012). On theother hand, several Neanderthal
facial features, such as midfacialprojection, maxillary ination,
and double-arched browridges, arenot fully developed until later in
childhood (Tillier, 1996).
Ponce de Len and Zollikofer (2001) showed that Neanderthalsand
modern humans share a common pattern of cranial andmandibular shape
change from an early age and onward. Thegeneral pattern of shape
change comprised a projection anddownward elongation of the face
and mandible combined witha contraction of the cranial vault. They
concluded that the cranio-facial and mandibular differences between
these two groupsprobably results from differential activity of
growth elds early inontogeny (Ponce de Len and Zollikofer, 2001).
Similarly, in theirgeometric morphometric study on facial
development in great apesand Australopithecus africanus, Ackermann
and Krovitz (2002)found that facial features arose very early in
development fol-lowed by parallel postnatal developmental patterns
(with thepossible exception of the gorillas). Additionally, they
found thataspects of facial growthweremore similar between A.
africanus andmodern humans, relative to the great apes. Therefore,
their studysuggests that our early human ancestors were already
demon-strating some human-like aspects of facial growth. The
implicationsof these ndings are that one can interchange hominid
postnatalgrowth trajectories without producing signicant
differences in theend results. This has been further demonstrated
by the study ofMcNulty et als. (2006) on the taxonomic afnities of
the subadultTaung fossil specimen. To evaluate the adult morphology
of theTaung child, McNulty et al. (2006) performed a series of
develop-mental simulations. They grew Taung along various
homininedevelopmental trajectories and compared its adult
morphologywith adults of both Australopithecus and Paranthropus.
WhileMcNulty et al. (2006) found the developmental patterns of
extanthominine species to be statistically different, the results
from theirdevelopmental simulations indicate that the postnatal
develop-mental differences between hominines have little impact on
theestimation of the adult morphology. McNulty et al.
(2006)demonstrated that the adult morphology of Taung can be
reliablyestimated even through the application of an incorrect
develop-mental trajectory.
However, several geometric morphometric analyses on humansand
primates have found that both early postnatal cranialmorphology and
later postnatal growth contribute to furtherdifferentiate
populations and species (Richtsmeier et al., 1993;OHiggins and
Jones, 1998; OHiggins et al., 2001; StrandViarsdttir et al., 2002;
Bastir and Rosas, 2004; Cobb andOHiggins, 2004; Strand Viarsdttir
and Cobb, 2004; Bastir et al.,2007). For example, Bastir et al.
(2007) argued that both pre- andpostnatal ontogenetic growth are
important in establishing
n Evolution 63 (2012) 723e740morphological differences in
mandibular shape between
-
umaNeanderthals and modern humans. Their results showed
divergentontogenetic shape changes between Neanderthals and
modernhumans and signicantly different allometric scaling
patterns.
The aim of this study is to place the MPhs in both a
geographi-cally and chronologically broad evolutionary and
developmentalcontext to gain a clearer understanding of how archaic
(i.e., MPhsand Neanderthals) and modern human facial features are
affectedby facial size and how they change through time. More
specically,the goals of this study are to: 1) explore temporal
trends in facialmorphology in order to gain a clearer understanding
of the polarityof facial features, 2) describe the shape changes
associated withallometric scaling in archaic and modern human
faces, and 3) testwhether differences in facial shape between
archaic and modernhumans are attributable to the differential
extension or truncationof common growth allometries (i.e.,
ontogenetic scaling), orwhether shape variation is due to divergent
growth patterns.
Temporal trends in facial morphology are explored through
themeans of a principal component analysis (PCA) of Procrustes
shapevariables and Procrustes distance comparisons. The second
andthird objectives are addressed by comparing the angle and
orien-tation of Neanderthal and modern human ontogenetic
allometrictrajectories in both shape and Procrustes form space, and
byapplying developmental simulations (McNulty et al., 2006;Neubauer
et al., 2010; Gunz et al., 2010, 2012; Gunz, 2012) to growmodern
human andNeanderthal faces to the size of selectedMiddlePleistocene
fossils. The predicted facial shapes are then visualizedand
compared between archaic and modern human groups.
In this study, we recognize three categories of
allometry:ontogenetic, static and evolutionary (Cock, 1966;
Cheverud, 1982;Klingenberg, 1998). We use cross-sectional data on
recent modernand Pleistocene humans to explore patterns in
ontogenetic allom-etry, dened as the covariation of traits with
size across differentage groups (i.e., ontogenetic stages) of a
given species (Klingenberg,1998). Static allometry reects trait
covariationwith size within thesame ontogenetic stage of a single
species (Klingenberg, 1998). Thistype of allometry is observed
among the adults in our sample.Lastly, evolutionary allometry
arises from covariation of traits withsize and their phylogenetic
changes and can be analyzed eitherwithin one ontogenetic stage or
across stages (Klingenberg, 1998).In his inuential paper evaluating
the relationship between thesethree types of allometry, Cheverud
(1982), following work by Cock(1966), Gould (1966) and Shea (1981),
demonstrated that patternsof static adult allometry cannot be
assumed to reect ontogeneticprocesses (although see Klingenberg and
Zimmermann, 1992;Klingenberg, 1998). This is mainly because adult
data usuallyrepresent a very restricted (in both size and time)
subset of theontogenetic range (Inouye and Shea, 1997).
Following Gould (1975), an allometric regression line can act
asan ontogenetic criterion of subtraction such that the points
alongthe line can be explained in terms of size-required changes.
Devi-ations from the line are non-allometric shape changes and
themorphological differences may indicate specic functional
adap-tations (Gould, 1975). In this study, we used ontogenetic
scaling asa criterion of subtraction because it is a powerful means
for iden-tifying shared effects of size change between groups or
species, aswell as derived dissociations of ancestral allometries
(Gould, 1975;Shea, 1981, 1983; Inouye and Shea, 1997). Here we use
a multivar-iate approach to allometric scaling that differs in
certain method-ological aspects from the classical allometric
studies. Departingfrom the conventional denition and applications
of allometry, e.g.,we substitute facial size for body size because
we are specicallyinterested in how differences in facial size
inuence the expressionof facial features and overall facial shape.
Surface semilandmarkgeometric morphometric techniques are used to
quantify facial
S.E. Freidline et al. / Journal of Hfeatures that are otherwise
difcult to capture, such as theinfraorbital surface topography, and
developmental simulations areapplied to visualize the effects of
allometry on the face.
Evolutionary models of Middle Pleistocene hominins
The two main competing phylogenetic interpretations of theMiddle
Pleistocene human fossil record are: 1) most of the MPhscomprise a
single, cross-continental taxon, spanning Africa, Europeand
possibly Asia, or 2) the European and African MPhs, at leastthose
fromMarine Isotope Stage 11 and onward, belong to separateclades.
In the rst model, the MPhs are assigned to the taxon
H.heidelbergensis and are considered to be the last common
ancestorto both Neanderthals and modern humans. This view is
supportedby the strong morphological and metric similarities
between theEuropean and African specimens (e.g., Stringer, 1974,
1983; Arsuagaet al., 1997; Rightmire, 1998, 2007, 2008; Mounier et
al., 2009;Harvati, 2009a).
In the second model, the European MPhs are seen as ancestralto
Neanderthals and are classied as either H.
neanderthalensis(Hublin,1998, 2009) or as the
exclusivemembersofH.heidelbergensis,a chronospecies of the
Neanderthal lineage (e.g., Arsuaga et al., 1997;Manzi, 2004; but
seeWolpoff et al.,1994; Rosas et al., 2006; Tattersalland Schwartz,
2006; Bruer, 2008 for alternative interpretations ofthe fossil
record). In this scenario, the AfricanMPhs are interpreted asbeing
ancestral to H. sapiens and often classied as H.
rhodesiensis(Hublin, 2009). As evidence for the Neanderthalization
process,proponents of this model refer to a series of features on
the skeletonthat foreshadow the Neanderthal condition and that
occur uniquelyin the European MPhs (Dean et al., 1998; Hublin,
1998, 2009). Thesefeatures are found on the face, occiput, temporal
bone and dentition.They include, but are not limited to, a convex
and receding horizontalinfraorbital prole, anteriorly advanced and
sagittally oriented face,wide occipital torus, incipient suprainiac
fossa, bilaterally protrudingoccipital torus, strong juxtamastoid
eminence (Dean et al., 1998;Hublin, 1998), and derived conditions
expressed in different non-metrical traits of the dentition
(Martinn-Torres et al., 2012).However, quantitative support for
this model is limited. This may inpart be due to the difculty in
quantifying these complex featuresespecially on the face (Harvati
et al., 2010).
Materials and methods
Sample
This study includes a comprehensive sample of subadult
andadultMiddle to Late Pleistocene fossil hominins (Table 1) and
recentmodernhumans (Table 2). The fossil samplewas designed to
includeall available Middle to Late Pleistocene fossils that
preserve rela-tively complete faces (see section on Missing data
reconstructionbelow). Table 1 lists the 26 fossils, their broad
geographical loca-tion, chronology and repository.
The modern human sample (Table 2) comprises a cross-sectional
growth series from four geographically diverse humanpopulations
spanning three continents: Africa, North America andEurope. The
individuals within each growth series range in agefrom two years to
adulthood. The African sample consists of anarchaeological Khoisan
population from South Africa. The NorthAmerican sample is divided
into two groups: a combined NativeAmerican archaeological sample
from Canyon del Muerto, Arizona,and Grand Gulch, Utah, and an
archaeological population fromPoint Hope, Alaska. Lastly, the
European sample consists ofa temporally more recent combined sample
from Strasbourg(France) and Greifenberg (Austria). The modern human
cranial datawere obtained from specimens housed in the American
Museum of
n Evolution 63 (2012) 723e740 725Natural History (AMNH, New
York), Iziko South African Museum
-
Table 1Fossil specimens used in the analysis, their abbreviation
(Ab.), repository and chronology.a
Specimen Ab.b Repositoryc Chronology
Middle Pleistocene: AfricaBodo Bd NME ca. 600 ka (Clark et al.,
1994)Kabwe Kb NHM 700e400 ka (Klein, 1994); late
Middle Pleistocene (Stringer, 2011)Middle Pleistocene:
Europe
Arago 21d Ar UM 600e350 ka (Cook et al., 1982;Falgures et al.,
2004)
Petralona Pt AUT 670eca. 250 ka (Harvati et al., 2009)Sima de
los Huesos 5e Sm5 UCM ca. 530 ka (Bischoff et al., 2007)
Late MiddleeLate Pleistocene: AfricaA
MNPEHHH
PP
S.E. Freidline et al. / Journal of Human Evolution 63 (2012)
723e740726Jebel Irhoud 1 I1 MLate MiddleeLate Pleistocene:
Europe
Gibraltar 1 Gb1 NHGuattari Gt MLa Chapelle-aux-Saints LCh MLa
Ferrassie 1 LF1 MPech-de-lAz I Pech M
Late MiddleeLate Pleistocene: AsiaLiujiange Ljg IVQafzeh 6 Q6
UTQafzeh 9 Q9 UTShanidar 1e Sh1 IMShanidar 5e Sh5 IMSkhul 5 Sk5
PM(Cape Town), the University of Cape Town, and the Medical
Facultyof Strasbourg.
Individual specimens in the human subadult skull collectionfrom
the Medical Faculty of Strasbourg have known ages witha precision
ranging from one month to one day (Rampont, 1994).Age estimates for
all other subadult individuals were assessedaccording to dental
eruption patterns following Ubelaker (1989).Each specimen in the
modern human sample was classied bydevelopmental stage according to
dental eruption sequence. Agegroup one is composed of subadults
with a deciduous dentition,lacking the eruption (as dened by the
exposure of cusps) of any
Table 2Recent modern human adult and subadult specimens used in
the analysis.
Population/Geographic region AGa 1
Khoisan, South Africac,d,e 8Arizona (Canyon del Muerto), Utah
(Grand Gulch), USAe 7Alaska (Point Hope), USAe 6Strasbourg, Francef
and Greifenberg, Austriae 7
a The abbreviation AG represents Age Group. See text (Material
and Methods e Sampb The specimen sex is denoted as M for males and
F for females.c Iziko South African Museumd University of Cape
Towne American Museum of Natural Historyf Medicine Faculty of
Strasbourg
Teshik Tashe T-T MSU
Upper Paleolithic: EuropeCro-Magnon 1 e MHGrotte des Enfants 6e
e MAPMladec 1 e NMPredmost 3e e DVM (
materOberkassel 1 e RLOberkassel 2 e RL
Upper Paleolithic: AsiaZhoukoudian 101d e Origin
Zhoukoudian 102d e Origin
a Subadult individuals are italicized.b Individual European and
Asian Upper Paleolithic fossil material were not labeled inc The
complete names of the repositories are available as a table in the
SOM.d Casts from the Department of Human Evolution, Max Planck
Institute for Evolutionae Casts from the Division of Anthropology,
American Museum of Natural History (Newca. 160 ka (Smith et al.,
2007)
71e50 to 35 ka (Klein, 1999)ca. 50 ka (Schwarcz et al.,
1991)56e47 ka (Grn and Stringer, 1991)71e50 to 35 ka (Klein,
1999)51e41 ka (Soressi et al., 2007)
139e111 ka (Shen et al., 2002)135e100 ka (Grn et al.,
2005)135e100 ka (Grn et al., 2005)ca. 50 ka (Trinkaus, 1983)ca. 50
ka (Trinkaus, 1983)135e100 ka (Grn et al., 2005)permanent teeth.
Age group two is dened by the eruption of therst molar. Age group
three is dened by the eruption of the secondmolar. Age group four
is dened by the eruption of the third molar(i.e., complete set of
permanent dentition). Table 2 lists the numberof subadults
distributed among each age groupwithin eachmodernhuman population,
and Table 3 lists the age estimates and group-ings for the subadult
fossil specimens. Because of the difculty anduncertainty in
identifying the sex of subadult individuals (Scheuerand Black,
2000), we made no attempt to do so, although studieshave shown that
size and shape differences occur between malesand females
throughout ontogeny and aremost pronounced during
AG 2 AG 3 AG 4 (adult) Total
8 4 38 (Mb: 14; F: 24) 586 4 52 (M: 25; F: 27) 6910 4 48 (M: 26;
F: 22) 684 4 49 (M: 27; F: 22) 64
le) for denition of each age group.
ca. 70 ka (Movius, 1953); 57e24 ka(Vishnyatsky, 1999)
28e27 ka (Holt and Formicola, 2008)Gravettian (Henry-Gambier,
2001)ca. 31 ka (Holt and Formicola, 2008)
originalial missing)
Early Upper Paleolithic (Smith, 1982)
ca. 12 ka (Street, 2002)ca. 12 ka (Street, 2002)
al material missing ca. 13e33 (Chen et al., 1989;Brown, 1992;
Hedges et al., 1992)
al material missing ca. 13e33 (Chen et al., 1989;Brown, 1992;
Hedges et al., 1992)
the gures and therefore no abbreviation is provided for these
specimens.
ry Anthropology (Leipzig, Germany).York).
-
each specimen and the Procrustes consensus conguration.
Aftersliding, landmarks and semilandmarks were treated the same
insubsequent statistical analyses. To convert the landmark
andsemilandmark coordinates to shape variables, a
generalizedProcrustes analysis (GPA) was performed. GPA removes the
effectsof translation and rotation in the raw coordinate data and
stan-dardizes each specimen to unit centroid size, the square root
of thesum of squared distances from each landmark to the
specimenscentroid (Dryden and Mardia, 1998). All data processing
andstatistical analyses were performed in Mathematica
(WolframResearch) and R (R Development Core Team, 2010).Missing
data reconstruction As geometric morphometric methodsrequire all
specimens to have the same number of homologouspoints,
someminordata reconstructionwasnecessary for some fossilspecimens.
First, bilateral symmetry was exploited by mirroring the
following Harvati (2001)Staphylion staZygomatic process root
inferiorb zri The malar root origin
projected onto buccalalveolar surface
Zygomatic process root superiorb zrs The point where malarroot
arises from themaxilla (often a pointof concavity betweenalveolare
region andzygomaxillare) followingMcNulty (2003)
Zygomaxillareb zm
a All landmarks are dened following White et al. (2012).
Denitions and refer-ences (if available) are provided for the less
common landmarks
b Paired right and left landmarks
umaLandmark Editor software (Wiley et al., 2005). This
templatemesh of surface semilandmarks was warped into the vicinity
ofthe surface of every specimen using a thin-plate spline
(TPS)interpolation according to the landmark and curve data.
Thewarped points were then projected onto the surfaces by
pickingand after adolescence (e.g., Strand Viarsdttir et al.,
2002;Bulygina et al., 2006). Adult individuals were sexed according
toHowells (1973) criteria, and when possible an equal number
ofmales and females were included.
Measurement protocol
Computed tomography (CT) and surface scans CT or surface scansof
the fossil and modern human crania were acquired. The CT scanswere
made with either an industrial (BIR ACTIS 225/300) ormedical
(Toshiba Aquilion) CT scanner, and the remaining speci-mens were
surface scanned with either a Minolta Vivid 910 ora Breuckmann
optoTOP-HE. The pixel size of the CT scans rangedfrom 0.24 to 0.49
mm and the slice thickness was between 0.25and 1.00 mm. The
resolution of the surface scanners ranged fromw30 microns to w6
microns in the z plane. The differences inresolution among these
scanners are much smaller than thedigitizing error and differences
among the specimens. Forexample, although the adults and juveniles
in the Europeansample were scanned using two different methods
(adults:Minolta surface scanner, juveniles: medical CT scanner),
theycluster together in a principal component analysis (PCA).
Three-dimensional surface models were extracted from eitherthe
surface or CT scans and saved as .ply polygon model le
format.Surface scans were processed using either Geomagic Studio
orOptoCat (Breuckmann) software, depending on the scanner
modelused. For the CT data, three-dimensional surfaces were
extractedusing Avizo (Visualization Sciences Group Inc.). The
landmarks andsemilandmarks were digitized on the surface models
using Land-mark Editor (Wiley et al., 2005). If CT or surface scan
data of theoriginal fossil material were not available, surface
scans of highquality casts (see Table 1) from the Division of
Anthropology of theAMNH (New York) or the Max Planck Institute for
EvolutionaryAnthropology (Leipzig) were made.Landmark data
Landmarks and semilandmarks, dening curvesand surfaces, were
digitized by one observer (S.F.). 3D coordinatesof landmarks (Table
4) and semilandmarks along curves weredigitized on all specimens
and a mesh of surface semilandmarkswas digitized on one template
individual (see Fig. 1) using
Table 3Ontogenetic age and age group classication of the
subadult fossil specimens used inthe analysis.a
Specimen Ontogenetic age (ca. yr.) Age group
Pech-de-lAz I 2 (Tillier, 1996) 1Teshik-Tash 9e11 (Tillier,
1989; Williams et al., 2002) 2Grotte des Enfants 6 13e15
(Henry-Gambier, 2001) 4
a See text (Material and Methods e Sample) for denition of age
groupclassications.
S.E. Freidline et al. / Journal of Hthe closest vertices from
the specimens .ply le following otherstudies (e.g., Gunz, 2005;
Gunz and Harvati, 2007; Neubaueret al., 2009, 2010; Gunz et al.,
2009a,b; Harvati et al., 2010;Stanseld and Gunz, 2011; Freidline et
al., 2012). This protocolguarantees that every specimen has the
same number of curvesemilandmarks and surface semilandmarks in
approximatelycorresponding locations. A detailed description can be
found inGunz et al. (2005, 2009b) and Mitteroecker and Gunz
(2009).
The initially equidistant semilandmarks were slid alongtangents
to the curves and tangent planes to the surfaces so as tominimize
the bending energy of the TPS interpolation betweenTable
4Homologous landmarks used in the analysis.a
Landmark Abbreviation Denition
Alveolare idsAnterior nasal spine ans Thin projection of
bone
on the midline at theinferior margin of thenasal aperture
Auriculareb auFrontomalare orbitaleb fmoFrontomalare temporaleb
fmtFrontotemporaleb ftGlabella gJugaleb juMedial orbital marginb mm
The point of maximal
concavity on the medialinferior corner of theorbital margin,
wherethe orbital margin andthe frontal process ofthe maxilla
meet
Nasion nNasospinale nsPorionb poRhinion rhiSphenopalatine
sutureb ss Suture between palatine
and sphenoid bonesposterior and inferior tomaxillary
tuberosity
n Evolution 63 (2012) 723e740 727surface of the better-preserved
side along themidsagittalplaneusingGeomagic Studio and Avizo. The
following specimens werecompleted by mirror-imaging: Bodo,
Cro-Magnon 1, Gibraltar 1,Guattari, Kabwe, La Ferrassie 1,
Oberkassel 1, and Shanidar 1.
Second, if missing data occurred bilaterally on a specimen
oralong its midline, landmarks were estimated using
geometricreconstruction via TPS interpolation (Gunz et al., 2009a).
Thismethod has been applied in several other studies (e.g., Gunz,
2005,2012; Gunz andHarvati, 2007; Gunz et al., 2009a,b, 2010, 2011,
2012;Harvati et al., 2010; Bastir et al., 2011; Benazzi et al.,
2011; Stanseldand Gunz, 2011; Freidline et al., 2012; Neubauer et
al., 2012) to
-
umareconstruct fragmentary fossil material. Arago 21 required
the mostextensive reconstruction. A detailed account of this
reconstructionand the protocol can be found in Gunz et al.
(2009b).
Statistical analyses
To explore the temporal variability in facial morphology
amongPleistocene humans, a PCA was performed in shape space. A
PCA
Figure 1. The landmark and semilandmark dataset. 671 landmarks
and semiland-marks digitized on all specimens, red: homologous
landmarks; blue: curve-semilandmarks; yellow:
surface-semilandmarks. Homologous landmarks are abbre-viated. The
full names are listed in Table 4. (For interpretation of the
references tocolour in this gure legend, the reader is referred to
the web version of this article.)
S.E. Freidline et al. / Journal of H728reduces the
dimensionality of high dimensional shape space andprovides
summaries of large-scale trends within the data(Bookstein, 1991;
Rohlf, 1993). We used TPS warping of theProcrustes mean shape along
the rst two principal components(PCs) to visualize the shape
changes (see Gunz and Harvati, 2007;Mitteroecker and Gunz, 2009).
Additionally, to identify whichindividuals are most phenetically
similar to one another, nearestneighbors were calculated using
inter-individual Procrustesdistances. To visualize the
morphological similarities sharedbetween nearest neighbors, each of
the Middle Pleistocene homi-nins was superimposed on its nearest
neighbor.
In morphometrics, a distinction is made between shape andform.
Shape refers to the geometric properties of an object that
areindependent of its overall size, position and orientation,
whereasthe form of an object includes both its shape and size
(Mitteroeckerand Gunz, 2009). Because this study focuses on
allometry, theinclusion of size in our statistical analyses is
essential. To quantifyfacial size, we used the variable centroid
size, which is computedduring the Procrustes superimposition.
Following Mitteroeckeret al. (2004, 2005), we performed a PCA in
Procrustes form space(also called size-shape space) on the
Procrustes landmark andsemilandmark coordinates. Form space
includes the geometric size(as the natural logarithm of centroid
size) of each specimen(Mitteroecker et al., 2004) and is valuable
because the relationshipbetween shape and size can be readily
explored.
In this study, we compute the ontogenetic allometric
trajectoriesas multivariate regressions of the Procrustes shape
variables on thenatural logarithm of centroid size. As outlined
byMitteroecker et al.(2004, 2005), properties of these trajectories
(e.g., length, shape,divergence) can be compared between
populations and species.Coincidental ontogenetic trajectories
indicate a common pattern ofshared development between the groups
under investigation. Weinterpret coincidental growth trajectories
for the extant (recentmodern humans) and extinct groups
(Neanderthals) as a sharedpattern of relative growth that also may
be truncated or extended.Parallel trajectories reveal that the
morphological divergencebetween groups has already occurred prior
to the age of the youn-gest specimen, and that there is a common
pattern of subsequentgrowth shared between groups. By contrast,
divergent trajectoriesindicate that development further accentuates
group differences.
Ontogenetic trajectories were plotted in shape and
Procrustesform space for Neanderthals, each of the four modern
humanpopulations, and the modern human mean. The modern humanmean
trajectory was calculated by regressing Procrustes shapecoordinates
on the natural logarithm of centroid size on the entiremodern human
sample. Because only adult MPhs faces are includedin this study,
static, rather than ontogenetic, allometric trajectorieswere
calculated and plotted in Procrustes shape and form space forthese
hominins.
To see if modern humans and Neanderthals share a
commonontogenetic allometric trajectory during postnatal ontogeny,
wecomputed the angle between the Neanderthal and the meanmodern
human ontogenetic allometric vectors. We then testedwhether the
angle was statistically different from zero usinga permutation test
(McNulty et al., 2006; Gunz, 2012). We rstmean-centered the
respective groups and then compared theactual angle with angles
obtained from regressions computed for5000 permutations that
randomly reassigned group membership,permuting the entire sample
for each iteration. Likewise, the anglesbetween the ontogenetic
allometric trajectories of the four modernhuman populations were
calculated and tested to see if they weresignicantly different from
zero. To assess the effects of the smallNeanderthal sample size on
the computation of the ontogeneticallometric trajectory, we
bootstrapped subsamples from the recentmodern human sample,
simulating the composition of the Nean-derthal sample (i.e., one
specimen from age group 1, one from agegroup 2 and six adults).
Developmental simulations and visualization techniques
The aim of the series of developmental simulations was
toidentify the allometric shape changes that occur when scaling
anadult modern human and Neanderthal to the size of a MPh. To doso,
we calculated the mean adult modern shape and grew itfollowing the
modern human mean ontogenetic allometric trajec-tory to the size of
a) Kabwe, an African MPh that has a particularlyinated infraorbital
surface topography for a MPh, and b) Bodo, anAfrican MPh that has
the largest face in our sample. Shape changeswere visualized by TPS
warping of the adult modern human meanshape to the modern human
mean grown to the size of Bodo andKabwe. The same approach was
applied to Neanderthals. We war-ped the surface of La Ferrassie 1
to the mean adult Neanderthalshape, and then grew it following the
Neanderthal ontogeneticallometric trajectory to the size of Kabwe
and Bodo.
Results
Principal component analyses and permutation tests
To explore temporal trends in facial morphology, a PCA
wasperformed in Procrustes shape space of only the adult
individuals(Fig. 2). The rst two principal components (PCs)
represent 46.9% ofthe total shape variation, and neither of the PCs
correlate with size.
n Evolution 63 (2012) 723e740There is a clear separation between
the modern humans, including
-
umaS.E. Freidline et al. / Journal of Hthe early modern and
Upper Paleolithic humans, and the archaichumans. Additionally,
members of each temporal group clustertogether. However, there is
some overlap between Middle Pleisto-cene humans and Neanderthals.
Themain shape changes that occuralong PC 1 are in the curvature of
the anterior portion of the frontalbone, browridge projection,
width of the nasal aperture and facialprognathism. Middle
Pleistocene specimens, such as Bodo andSima de los Huesos 5, and
Neanderthals, such as La Chapelle-aux-Saints, cluster at the
extreme positive end of PC 1. These fossilsshare a more receding
anterior frontal bone, anteriorly projectingbrowridge, wide nasal
aperture, and prognathic mid and lower facewhen compared with
recent modern humans, which generally plotat the negative end of PC
1. While several shape changes are sharedbetween PC 1 and PC 2,
such as frontal bone curvature, facialprognathism and infraorbital
surface topography, PC 2 primarilydemonstrates changes in facial
length and orientation of themaxillary body (i.e., maxillary body
facies). Shanidar 5, Petralonaand Kabwe share a
superiorlyeinferiorly long face and theirmaxillary body is oriented
near vertically. On the opposite end of PC2, the modern humans
express a shorter face and a maxillary bodythat is oriented down
and slightly posteriorly.
Figure 2. PCA in shape space of adult fossil and modern humans.
A convex hull is drawnnearest neighbor according to
inter-individual Procrustes distances. The black arrows specifyfull
names and abbreviations for the fossil specimens are listed in
Table 1. The surface visun Evolution 63 (2012) 723e740 729Based on
pairwise Procrustes distances (PD), Bodo is mostsimilar to Sima de
los Huesos 5 (PD 0.068), Sima de los Huesos 5 ismost similar to
Arago 21 (PD 0.06), Arago 21 is most similar to LaChapelle (PD
0.05), Petralona and Kabwe are most similar to oneanother (PD
0.056), and Shanidar 5 is most similar to Petralona(PD 0.056). To
illustrate the resemblances between these speci-mens, we
superimposed each MPh onto its nearest neighbor(Fig. 3aeo). Bodo
and Sima de los Huesos 5 share similarly projec-ting lateral
browridges, wide nasal apertures and interorbitalbreadths. However,
Bodos glabellar region is more anteriorly pro-jecting and itsmid
and lower facemorphology is especially differentfrom Sima de los
Huesos 5 (Fig. 3aec). For example, Sima de losHuesos 5 has a more
prognathic mid and lower face, a slightly moreinated infraorbital
surface topography and a more parasagittallyoriented midface when
compared with Bodo (Fig. 3c: Sima de losHuesos 5 is green and Bodo
is bone color). Sima de los Huesos 5 andArago 21 (Fig. 3def) share
a similar mid and lower face morphologyand diverging upper faces
(i.e., browridges). Thus they sharea similar infraorbital surface
topography, and they exhibit a similardegree of facial prognathism
and parasagittal rotation. However,Arago 21 has a more projecting
browridge, especially the middle
for the Upper Paleolithic modern humans. The arrows indicate
each fossil specimensif an individual is most similar to another
individual outside of its temporal group. Thealizations represent
the mean shapes at the positive and negative ends of PC 1 and
2.
-
umaS.E. Freidline et al. / Journal of H730portion (Fig. 3f: Sima
de los Huesos 5 is green). The similaritiesbetween Arago 21 and La
Chapelle (Fig. 3gei) are in midfacialprognathism and infraorbital
surface topography. La Chapelle hasamore anteriorly projecting
browridge thanArago 21, except for thelateral portions, its midface
is more parasagitally oriented, and itsnasal aperture is more
anteriorly projecting (Fig. 3i: La Chapelle isred). Kabwe and
Petralona (Fig. 3jel) primarily share similarities inthe
lateralmidface,mainly in zygomatic bone projection. Kabwehasa more
anteriorly projecting browridge, and a superiorlyeinferiorlylonger
and more prognathic subnasal region. However, the
Figure 3. Procrustes superimposition of each of the Middle
Pleistocene hominins on its necontained in the landmark and
semilandmarks and everything in between these landmarkspecimens
surface color (dark yellow is associated with the bone colored
surfaces; dark greecolored landmarks are exposed this indicates
overlapping (i.e., similar) morphology. Differesurface is visible.
Nearest neighbors are indicated by the arrows in Fig. 2. The full
names anreferences to colour in this gure legend, the reader is
referred to the web version of thisn Evolution 63 (2012)
723e740infraorbital topography of Petralona is more inated than
Kabwe(Fig. 3l: Kabwe is green). Lastly, Shanidar 5 and Petralona
(Fig. 3meo) share a similar degree of mid and lower facial
prognathism,infraorbital ination, and nasal aperturewidth. Themain
differencebetween these two specimens is in the morphology of their
brow-ridge. Petralona expresses a more anteriorly projecting
browridgeand upper face (Fig. 3o: Shanidar 5 is red).
The results of the PCA in Procrustes shape space of the
completesample (i.e., subadult modern humans and Neanderthals)
areshown in Fig. 4. The rst three PCs were plotted and
represent
arest neighbor in shape space. The Procrustes shape information
for each specimen iss is interpolated. The landmarks and
semilandmarks are color-coded according to thenwith the green
surfaces; and dark red with the red surfaces). Thus, when two
differentnt surface morphologies are present when only one landmark
color and correspondingd abbreviations for the fossil specimens are
listed in Table 1. (For interpretation of thearticle.)
-
Figure 4. PCA in shape space including subadult and adult fossil
and modern humans. The rst three PCs are plotted. PC 1 represents
32.5% of total shape variance, PC 2 represents17.8%, and PC 3
represents 8.8%. The lines indicate the ontogenetic allometric
trajectories for Neanderthals (in red), the mean modern human
trajectory (in dark gray), and the
for td retraps to
S.E. Freidline et al. / Journal of Human Evolution 63 (2012)
723e740 73160.0% of total shape variance. PC 1 is correlated with
size(r y 0.79). The solid lines represent the ontogenetic
allometrictrajectories for each of the four modern human
populations, theNeanderthal and mean modern human ontogenetic
allometrictrajectories, and the MPh static allometric trajectory.
The shadedregion represents the 95% single prediction interval of
the modernhuman regressions of shape on the natural logarithm of
centroidsize. It is evident that all Neanderthal and MPh adults
fall outsidethis condence interval for allometric scaling. The thin
lines
trajectory for each modern human population (in black). The
static allometric trajectorylogarithm of centroid size. The
specimen color-coding is the same as in Fig. 2. The shadeshape on
the natural logarithm of centroid size. The thin gray lines
represent the bootsthat simulate the Neanderthal sample
composition. (For interpretation of the referencerepresent the
bootstrapped estimates of the modern human allo-metric trajectory
computed from subsamples that simulate theNeanderthal sample
composition.
None of the Neanderthal or recent modern human
ontogeneticallometric trajectories coincide. Because each
ontogenetic
Figure 5. PCA in form space of subadults and adult fossil and
modern humans. Form spacerepresents 79.0% of total form variance,
PC 2 represents 5.0%, and PC 3 represents 3.3%. The lmodern human
trajectory (in dark gray), and the trajectory for each modern human
populatwere calculated by regressing form on the natural logarithm
of centroid size. The specimeprediction interval of the modern
human regressions of shape on the natural logarithm ofhuman
allometric trajectory computed from subsamples that simulate the
Neanderthal samhuman overgrown along the mean modern human
ontogenetic allometric trajectory to thpretation of the references
to colour in this gure legend, the reader is referred to the
webtrajectory has a unique starting point, this plot shows that
pop-ulation and species-specic facial morphology is present
beforepermanent teeth erupt. As in Fig. 2, clusters of temporal
groups arealso apparent when including the entire sample (i.e., all
subadultsincluded) although the MPh and Neanderthals overlap. Apart
fromQafzeh 9, the early and Upper Paleolithic modern humans
fallwithin the range of recent human variation.
The variance explained by ontogenetic allometry is 26.0%
forrecent modern humans and 59.7% for Neanderthals. The angle
he MPhs is in green. The trajectories were calculated by
regressing shape on the naturalgion represents the 95% single
prediction interval of the modern human regressions ofped estimates
of the modern human allometric trajectory computed from
subsamplescolour in this gure legend, the reader is referred to the
web version of this article.)between the modern human average
ontogenetic trajectory andthe Neanderthal ontogenetic trajectory in
the subspace of the rstthree PCs is 28.0. A permutation test using
all dimensions of shapespace, however, reveals that the slopes of
the Neanderthal andmean modern human (MH) ontogenetic trajectories
are not
includes the log centroid size for each individual. The rst
three PCs are plotted. PC 1ines indicate the ontogenetic allometric
trajectories for Neanderthals (in red), the meanion (in black). The
static allometric trajectory for the MPhs is in green. The
trajectoriesn color-coding is the same as in Fig. 2. The shaded
region represents the 95% singlecentroid size. The thin gray lines
represent the bootstrapped estimates of the modernple composition.
The two circles demonstrate where the predicted shapes of a moderne
size of Kabwe and Bodo plot in the PCA (see text for more
information). (For inter-version of this article.)
-
signicantly different from zero (p < 0.31). Therefore, we
cannotreject the null hypothesis that the mean modern human
andNeanderthal ontogenetic allometric trajectories are
parallel.
To further explore the effects of size on facial morphology,
weperformed a PCA in Procrustes form space (Fig. 5). The rst
threePCs represent 85.0% of total variance. The Neanderthal and
modernhuman mean ontogenetic trajectories do not coincide. The
anglebetween the two trajectories in the subspace of the rst three
PCs is8.8. However, a permutation test cannot reject the null
hypothesisthat these trajectories are parallel (p< 0.35). As
expected in a form-
facial shape and its ontogenetic allometric trajectory.
Thesedevelopmental simulations are depicted in Fig. 7def. Table 6
liststhe facial features affected by allometry in both recent
modernhumans and Neanderthals. Among the recent modern humans inour
sample, the Point Hope group has the largest faces
accordingcentroid size. Therefore, to verify that this population
was notdriving our results, we removed them and recalculated the
meanmodern human developmental allometric trajectory. The
sameallometric shape changes occurred in modern humans when
thePoint Hope sample was not included. The following facial
shape
ma
mer
< 0
0.00.0
r) an
S.E. Freidline et al. / Journal of Human Evolution 63 (2012)
723e740732space analysis, PC 1 is highly correlated with centroid
size(r 0.99). The variance explained by ontogenetic allometry
inrecent modern humans is 80.1% and in Neanderthals it is 92.4%.
Asin shape space, the shaded region in Fig. 5 represents the 95%
singleprediction interval of themodern human regressions of form on
thenatural logarithm of centroid size, and, as in shape space,
allNeanderthal and MPh adults fall outside this modern
humancondence interval for allometric scaling. The thin lines
representthe bootstrapped estimates of the modern human
allometrictrajectory computed from subsamples that simulate the
Neander-thal sample composition.
The Neanderthal infant Pech de LAz and the youngest recentMH
subadult individuals cluster at the left end of the plot
(indi-cating smaller size) and the individuals with larger faces,
e.g., Bodo,Petralona, and Kabwe fall at the opposite end. The MPhs
fall at theend of the Neanderthal ontogenetic allometric trajectory
and theorientation of the Neanderthal ontogenetic and MPh static
trajec-tories appear similar. The position of the larger MPhs,
Kabwe,Petralona and Bodo suggests that allometric scaling alonga
common trajectory explains some differences in facialmorphology
between them and Neanderthals. The early MH andUpper Paleolithic
humans cluster with the adult recent MH.
Table 5 lists the angles between the ontogenetic
allometrictrajectories for each of the four modern human
populations. Theangles were computed in the subspace of the rst
three PCs tomake them easier to interpret. The permutation tests
werecomputed using all dimensions of shape space and Procrustes
formspace, respectively. The results of the permutation test
indicate thatin both shape and form space, the trajectories of each
of themodernhuman populations is signicantly different from zero
(i.e., notparallel). The only exceptions are the angles between the
PointHope and Khoisan populations (shape space: angle 4.3, p<
0.23;form space: angle 18.5, p < 0.07).
Developmental simulations
To visualize the allometric shape changes that occur in the
faceof recent modern humans, the modern human mean shape
wascalculated and grown to the size of Bodo, the largest specimen
inour sample, following the modern human mean ontogenetic
allo-metric trajectory. Fig. 6def illustrates the allometric shape
changesthat occur in recent modern humans. Developmental
simulationswere also performed on Neanderthals using the
Neanderthal mean
Table 5Angles between the ontogenetic allometric trajectories of
the four recent modern hu
Africa North A
Africa 0 23.7 (pNorth Americab 6.3 (p < 0.006) 0Europe 8.4 (p
< 0.0005) 5.3 (p