Evol Biol (2012) 39:499–520
DOI 10.1007/s11692-011-9153-4
RESEARCH ARTICLE
Postnatal Cranial Development in Papionin Primates:
An Alternative Model for Hominin Evolutionary Development
Michelle Singleton
Received: 4 November 2011 / Accepted: 30 November 2011 / Published online: 7 January 2012
Springer Science+Business Media, LLC 2011
Abstract The evolution of hominin growth and life history has long been a subject of intensive research, but it is
only recently that paleoanthropologists have considered the
ontogenetic basis of human morphological evolution. To
date, most human EvoDevo studies have focused on
developmental patterns in extant African apes and humans.
However, the Old World monkey tribe Papionini, a diverse
clade whose members resemble hominins in their ecology
and population structure, has been proposed as an alternative model for human craniofacial evolution. This paper
reviews prior studies of papionin development and socioecology and presents new analyses of juvenile shape
variation and ontogeny to address fundamental questions
concerning primate cranial development, including:
(1) When are cranial shape differences between species
established? (2) How do epigenetic influences modulate
early-arising pattern differences? (3) How much do postnatal developmental trajectories vary? (4) What is the
impact of developmental variation on adult cranial shape?
and, (5) What role do environmental factors play in
establishing adult cranial form? Results of this inquiry
suggest that species differences in cranial morphology arise
during prenatal or earliest postnatal development. This is
true even for late-arising features that develop under the
influence of epigenetic factors such as mechanical loading.
Papionins largely retain a shared, ancestral pattern of
ontogenetic shape change, but large size and sexual
dimorphism are associated with divergent developmental
trajectories, suggesting differences in cranial integration.
Developmental simulation studies indicate that postnatal
M. Singleton (&)
Department of Anatomy, Midwestern University,
555 31st Street, Downers Grove, IL 60515, USA
e-mail: [email protected]
ontogenetic variation has a limited influence on adult cranial morphology, leaving early morphogenesis as the primary determinant of cranial shape. The ability of social
factors to influence craniofacial development in Mandrillus
suggests a possible role for phentotypic plasticity in the
diversification of primate cranial form. The implications of
these findings for taxonomic attribution of juvenile fossils,
the developmental basis of early hominin characters, and
hominin cranial diversity are discussed.
Keywords Rungwecebus Mandrillus Paranthropus Human EvoDevo Phenotypic plasticity Developmental
simulation
Organismal form, shape, morphological structure, and the generative
mechanisms underlying their evolution represent the essential questions
within EvoDevo.
-Gerd Müller (2005: 91)
Introduction
Biological anthropologists’ fundamental interest in the
patterning of phenotypic and ontogenetic variation predates
the origins of evolutionary developmental biology (EvoDevo) by at least a half-century. The evolution of hominin
growth and life history, in particular, has been a subject of
intensive research (see reviews in Thompson et al. 2003;
Coqueugniot et al. 2004; Ponce de León et al. 2007), but it
is only recently that paleoanthropologists have begun to
focus more narrowly on the ‘‘actual ontogenetic mechanisms that underlie the crucial phenotypic transformations
in hominid evolution’’ (Müller 2005: 102). With only a
small number of reasonably complete juvenile fossils to
directly inform our understanding of fossil hominin growth
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and development (Dart 1925; Rak and Howell 1978;
Brown et al. 1985; Walker and Ruff 1993; Rak et al. 1994;
Akazawa et al. 1995, 1999; Duarte et al. 1999; Golovanova
et al. 1999; Coqueugniot et al. 2004; Alemseged et al.
2006; Berger et al. 2010), human EvoDevo necessarily
relies upon extant models to investigate the developmental
basis of hominin morphological evolution. Nonprimate
experimental models are yielding fascinating insights into
the molecular and cellular processes responsible for early
pattern formation as well as epigenetic influences on cranial form (Herring and Lakars 1982; Hallgrı́msson et al.
2004; Nie 2005; Vecchione et al. 2007; Lieberman et al.
2008; Prabhakar et al. 2008, 2010). But the classical
comparative approach, augmented by recent advances in
multivariate shape analysis, remains the principal means of
investigating hominin developmental and phenotypic variation (Müller 2005).
To the extent that they embody developmental, functional, and phylogenetic constraints on the evolution of
primate cranial form generally, extant primates (including
humans) furnish the comparative basis for interpretation of
ontogenetic and phenotypic diversity in the hominin fossil
record (Jolly 2001). To date, most human EvoDevo studies
have focused on developmental patterns in extant African
apes, who together with humans and their closest fossil
relatives (hominins) comprise the hominines (subfamily
Homininae, sensu Groves 2001). The phylogenetic propinquity of gorillas, chimpanzees, and bonobos makes
them obvious models for fossil hominin developmental
patterns (e.g., Lieberman et al. 2000; Ackermann and
Krovitz 2002; Strand Viðarsdóttir et al. 2002; Williams
et al. 2002; Berge and Penin 2004; Cobb and O’Higgins
2004; Mitteroecker et al. 2004, 2005; McNulty et al. 2006).
However, comparisons limited to this small group of ecologically and morphologically specialized taxa may not
encompass the entire spectrum of developmental phenomena that have contributed to hominin craniofacial
diversity. But even if extant apes were fully representative
of hominine developmental variation, Jolly’s contention
that ‘‘patterns and processes imputed to human evolution
are made more plausible if they can be shown to be widely
applicable outside the human lineage’’ (Jolly 2009: 187)
offers a strong argument for extending comparisons beyond
the hominine clade.
Clifford Jolly, among others, has advocated the Old
World monkey tribe Papionini—a monophyletic group
(Fig. 1) that includes macaques (genus Macaca), mangabeys (Cercocebus, Lophocebus, Rungwecebus), and
‘‘baboons’’ (Mandrillus, Papio, Theropithecus)—as an
appropriate model for craniofacial variation in early hominins (Jolly 1972, 2001, 2009; Leigh et al. 2003; Harvati
et al. 2004). In contrast with the extant apes, papionins are
both taxonomically diverse and similar to hominins in their
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Evol Biol (2012) 39:499–520
Fig. 1 Papionin phylogenetic relationships (adapted from Singleton
et al. 2010). Following Harris (2000), the Lophocebus/Papio/
Theropithecus clade is shown as a trichotomy with alternate
placements of Rungwecebus indicated (Davenport et al. 2006; Olson
et al. 2008; Burrell et al. 2009; Zinner et al. 2009; Roberts et al. 2010)
ecology and population structure (Jolly 2001, 2003; Harvati et al. 2004). They are also, Jolly argues, ‘‘phylogenetically close enough to share many basic attributes by
homology, yet far enough that homoplastic modifications
of these features are easily recognized’’ (2001: 177) as the
result of parallel and/or convergent evolution between papionins and hominins. The African papionin clade (subtribe
Papionina), in particular, exhibits a complex phylogenetic
distribution of morphological and ecological traits.
Molecular phylogenetic studies have consistently shown
the two African ecomorphs—small-bodied, short-faced,
largely arboreal mangabeys versus large-bodied, longfaced, terrestrial baboons—to be paraphyletic (Disotell
1994; Harris 2000), making this group useful for elucidating developmental, functional, and historical sources of
primate facial homoplasy (Lockwood and Fleagle 1999;
Jolly 2001). Genus Macaca (subtribe Macacina), on the
other hand, has the broadest geographic distribution and
greatest morphological diversity of any nonhominin primate and thus offers valuable insights into intrageneric
variation in geographically dispersed primate lineages
(Miller et al. 1999). Additionally, macaques have been
widely used in studies of primate craniofacial growth and
development (e.g., Sirianni and Swindler 1985; Dechow
and Carlson 1990; Schneiderman 1992; Zumpano and
Richtsmeier 2003; Hallgrı́msson et al. 2004), analyses of
in vivo bone strain (e.g., Hylander and Bays 1979;
Hylander 1986; Hylander and Johnson 1997; Ross 2001),
and computer modelling of facial biomechanics (e.g.,
Curtis et al. 2008; Kupczik et al. 2009; Nakashige et al.
2011; Ross et al. 2011).
Leigh et al. (2003: 287) specifically recommend papionins as a developmental model, citing ‘‘The availability of
a known phylogeny, coupled with abundant life history,
ecological, and ontogenetic data [that] promise improvements in our understanding of the relations between
development and evolution.’’ And the recent discovery of a
new papionin, Rungwecebus kipunji (Jones et al. 2005;
Evol Biol (2012) 39:499–520
Davenport et al. 2006; Ehardt and Butynski 2006; Olson
et al. 2008), has catalyzed research in this direction.
Molecular analyses have yielded contradictory findings
concerning the kipunji’s phylogenetic affinities and
potential hybrid origin, making it the object of considerable
interest (Davenport et al. 2006; Olson et al. 2008; Burrell
et al. 2009; Zinner et al. 2009; Roberts et al. 2010).
Unfortunately, its skeletal morphology is presently known
solely from juvenile voucher specimens, the best studied of
which is an M1-stage juvenile (FMNH 187122) (Davenport
et al. 2006; Singleton 2009; Singleton et al. 2010; Gilbert
et al. 2011). In several respects, this first kipunji juvenile
resembled the Taung child at the time of its discovery (Dart
1925). As a lone, immature representative of a new and
controversial primate taxon, this specimen renewed interest
in the nature of juvenile cranial morphology and the processes by which adult cranial form is attained.
A central debate within human EvoDevo concerns the
contribution of postnatal ontogeny to hominine cranial
diversity. While there is general agreement that major
differences in human and ape cranial morphology appear
early in ontogeny and are largely stable by the eruption of
the first permanent molar, there is little consensus on the
extent to which postnatal developmental patterns differ
among hominines (Shea 1983a, 1985; Richtsmeier and
Walker 1993; Ackermann and Krovitz 2002; Strand
Viðarsdóttir et al. 2002; Williams et al. 2002; Krovitz
2003; Bastir and Rosas 2004; Cobb and O’Higgins 2004;
Mitteroecker et al. 2004; McNulty et al. 2006; Bastir et al.
2007; Ponce de León et al. 2007; Gonzalez et al. 2010).
Additionally, authors who have found significant differences among hominine ontogenetic patterns disagree concerning the influence of this variation on adult cranial form
(Cobb and O’Higgins 2004, 2007; McNulty et al. 2006).
These questions are not restricted to the hominine clade
(e.g., Richtsmeier et al. 1993); there is a substantial literature, some of it equally contradictory, addressing postnatal
ontogenetic variation within and among papionin species
(see Leigh 2007). As in hominines, the relative contributions of prenatal pattern establishment and postnatal ontogenetic variation are a principal research focus (Richtsmeier
et al. 1993; Collard and O’Higgins 2001; O’Higgins et al.
2001; Leigh 2007; Singleton 2009; Singleton et al. 2010).
Here, I review prior studies of papionin development
and socioecology and present new craniometric analyses
to address several fundamental questions concerning
cranial development, including: (1) When are cranial shape
differences between species established? (2) How do epigenetic influences modulate early-arising pattern differences? (3) How much do postnatal developmental
trajectories vary? (4) What is the impact of developmental
variation on adult cranial shape? and, (5) What role do
environmental factors play in establishing adult cranial
501
form? The results of this inquiry are discussed with respect
to primate developmental variation and its implications for
fossil hominin cranial diversity and human EvoDevo.
Papionin Cranial Development
Early Pattern Formation
Prenatal development is frequently invoked to explain
observed differences in juvenile cranial form (e.g., Richtsmeier et al. 1993; O’Higgins et al. 2001; Strand Viðarsdóttir et al. 2002; Krovitz 2003; Leigh 2007), but there is
relatively little comparative data concerning infant, much
less prenatal, growth patterns in nonhuman primates (Shea
1983a; Ravosa 1992; Richtsmeier et al. 1993; Jeffery 2003,
2007; Zumpano and Richtsmeier 2003). Rather, the actions
of prenatal processes are inferred mainly from the phenotypes of more accessible infant and juvenile stages.
Papionins exhibit species-typical cranial morphologies
from a very early age (Fig. 2). Suborbital fossae are present
in mangabey infants prior to eruption of the deciduous
incisors (pers. obs.), and differences in fossa shape and
composition that distinguish mangabey genera are well
established prior to M1 eruption (Singleton 2009). Many
phylogenetic characters that differentiate the two African
Fig. 2 Expression of species-typical morphology in juvenile papionins. Left dp4 stage Macaca nigra (top) and M1-stage Lophocebus
albigena (bottom). Right M1-stage Mandrillus leucophaeus (top) and
Cercocebus agilis (bottom). Crania scaled to approximately equal
size; all scale bars 1 cm
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Fig. 3 Expression of phylogenetic characters in M1-stage papionins.
In comparison with Cercocebus agilis (top), Lophocebus aterrimus
exhibits more projecting nasal bones, more anteriorly positioned
zygomatic roots, and deeper facial fossae, all characteristics of the
Lophocebus/Papio/Theropithecus clade (Gilbert 2007)
papionin clades—e.g., differences in nasal-bone projection
and maxillary fossa depth (Groves 1978, 2001; Gilbert
2007; Gilbert et al. 2011)—are also fully expressed in M1stage juveniles (Fig. 3). Other traits, such as relative facial
prognathism, muzzle shape, and paranasal ridge orientation, foreshadow their species’ adult morphologies from
the early juvenile period onward (Fig. 2).
These qualitative observations are supported by quantitative shape analyses. Collard and O’Higgins (2001)
found genus-level differences in facial shape to be present
in juvenile papionins, and Singleton (2009) demonstrated
that cranial shape differences among species are already
present by M1 eruption. In the latter study, principal
components analyses showed clear separation of genera
and species according to well-known taxonomic characters
such as zygomatic shape and position, nasal projection, and
neurocranial shape (Singleton 2009).
Epigenetic Modification
In comparison with characters discussed above, the juvenile precursors of some adult traits are much less readily
apparent. For example, the African papionin clades are
distinguished by their cranial superstructures (McGraw and
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Evol Biol (2012) 39:499–520
Fleagle 2006; Gilbert 2007). In Cercocebus and Mandrillus,
the superior nuchal lines turn upward, the external occipital
protuberance (inion) points superiorly, and the temporal
lines are widely set anteriorly, giving the frontal bone a
shield-like appearance; in Lophocebus and Papio, the
nuchal lines turn downward, inion points inferiorly, and the
temporal lines are closely approximated anteriorly. These
features, which develop in response to mechanical loading
by the nuchal and masticatory muscles, respectively, are
undeveloped in subadults and typically achieve their full
expression only in mature adulthood, especially in males
(Gilbert 2007). However, Singleton (2009) identified differences between Lophocebus/Papio and Cercocebus in
juvenile frontal bone shape, suggesting that the foundations
of these late-arising morphological differences are also laid
early in ontogeny.
To test this hypothesis, I conducted separate geometric
morphometric analyses of juvenile frontal and occipital
bone shape, the results of which are newly presented here.
The sample comprised 32 M1-stage juveniles representing
all African papionin genera omitting Theropithecus
(Table 1); all specimens were wild shot and of known
provenience. From a larger 3D landmark set (Singleton
2009), subsets of 21 and 17 landmarks and semi-landmarks
were selected to capture the shapes of the frontal and
occipital bones, respectively (Table 2, Fig. 4a). Generalized Procrustes analysis performed in Morpheus (Slice
1998) was used to remove the nuisance parameters of
translation, rotation, and scale, thus aligning specimens in a
common shape space (Gower 1975; Rohlf and Slice 1990;
Dryden and Mardia 1998). Semi-landmarks were treated as
regular landmarks during analysis. Aligned coordinates for
each species were averaged to yield mean landmark configurations, and principal components analysis (PCA) was
performed to ordinate species mean shapes in a lowerdimension morphospace (Dryden and Mardia 1998). Species means were used rather than individual specimens to
prevent larger samples from unduly influencing the PCA
ordination (Mitteroecker and Gunz 2009).
Table 1 Sample of M1-stage African papionins
N
Mandrillus sphinx
2
Cercocebus agilis
6
Cercocebus atys
5
Cercocebus torquatus
Lophocebus albigena
2
4
Lophocebus aterrimus
5
Rungwecebus kipunji
1
Papio hamadryas kindae
4
Papio hamadryas anubis
3
Evol Biol (2012) 39:499–520
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Table 2 Craniometric landmarks used in geometric morphometric
analyses
Frontal
shape
Occipital
shape
Macaque
ontogeny
Table 2 continued
Frontal
shape
Mandrillus
simulation
Sphenobasion
Dorsal landmarks
Hormion
Midsagittal
Posterior Nasal Spine
Inion
Lambda
X
X
X
X
X
X
Palatomaxillary
suture
Occipital
shape
Macaque
ontogeny
X
Mandrillus
simulation
X
X
X
Staphylion
X
X
X
Bregma
X
Supraorbital torus
X
X
Incisivion
Glabella
X
X
X
Orale
Nasion
X
X
X
Bilateral
X
X
Asterion
X
X
X
X
X
Rhinion
Subnasal clivus
Nasospinale
X
X
Lateral foramen
magnum
Prosthion
X
X
Occipital condyle
X
X
Prosthion2
Alare
X
Premax-nasal
X
Premax-max superior
Malar root
Zygomaxillare
inferior
X
X
X
X
X
X
X
Orbitale
X
Dacryon
X
X
Midtorus inferior
X
X
X
Midtorus superior
X
X
X
Frontomalare
orbitale
X
X
X
Frontomalare
temporale
X
X
X
Maxillary ridge
X
Suborbital bar
X
Suborbital fossa
X
Porion
X
Auriculare
X
X
Zygotemporale
superior
X
Jugale
X
X
X
Pterion posterior
Pterion anterior
X
Ventral landmarks
X
X
Temporospheno-petrous
X
Inferior petrous
process
X
Petrous apex
X
Sphenobasion
laterale
X
X
X
Medial pterygoid
X
Mastoidale
Postglenoid process
X
X
X
Articular tubercle
X
Central glenoid
X
Entoglenoid process
X
Zygotemporale
inferior
X
X
Petrotympanic
fissure
Postorbital septum
X
X
X
Maxillary tubercle
X
P4-M1 contact
X
P3-P4 contact
X
Mesial P3
X
X
Premax-max inferior
X
X
X
X
Midsagittal
X
Inion-Glabella (11)
X
Bregma-Glabella (3)
X
Opisthion-Inion (5)
Opisthion-Inion (3)
Basion
X
X
Cranial Base Flexion
X
X
X
X
X
X
Glabella-Rhinion (7)
X
X
Infratemporal crest
Contours
Midsagittal
Opisthion
X
Lateral pterygoid
Zygomaxillare
superior
X
X
Jugular process
Bilateral
Temporal point
X
X
X
X
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Evol Biol (2012) 39:499–520
Table 2 continued
Frontal
shape
Occipital
shape
Macaque
ontogeny
Mandrillus
simulation
Left side
Temporal fossa (13)
X
Suborbital fossa (9)
X
Inferior zygomatic
(7)
X
3D landmarks and contours were registered using a Microscribe
3DX contact digitizer. Midsagittal landmarks and contours were
registered in the midsagittal plane. Bilateral landmarks were collected
on both sides of the skull; contours, on the left side only. Contours
were resampled to equidistant semi-landmarks using Resample (Raaum 2006); numbers of resampled semi-landmarks are indicated in
parentheses. For details of data collection and landmark definitions,
see Singleton (2002), Frost et al. (2003), and Singleton (2009, Supplementary Material)
As seen in Fig. 4, PCAs of frontal and occipital bone
shape segregate M1-stage juveniles of the two African papionin clades (Fig. 4b, c). In both analyses, the first principal
shape component (not shown) summarizes allometric variation, while subsequent axes reflect phylogenetic shape
differences. In the frontal analysis (Fig. 4b), the second
principal shape component (PSC2) completely separates the
two sister groups. Visualization of shape variation summarized by this axis indicates that in Cercocebus and
Mandrillus (black wireframe) the coronal suture intersects
the temporal line farther antero-inferiorly, the frontosphenoid suture is shorter, and glabella is less prominent than in
Lophocebus, Papio, and Rungwecebus (grey).
Occipital shape (Fig. 4c) separates the two groups
less completely; Lophocebus aterrimus falls closer to
Cercocebus and Mandrillus than to more closely related
taxa. In Cercocebus, Mandrillus, and L. aterrimus (Fig. 4c),
inion is more inferiorly positioned, resulting in a relatively
long occipital plane. By contrast, the higher inion of Lophocebus albigena, Papio, and Rungwecebus creates a relatively
short occipital plane and slightly longer nuchal plane, providing a larger attachment area for the nuchal musculature,
possibly reflecting greater emphasis on anterior dental loading
(Daegling and McGraw 2000; Singleton 2004, 2005). Irrespective of their potential adaptive significance, it appears that
adult neurocranial superstructures are the product of early
pattern formation as well as epigenetic modification in the
form of mechanical loading.
Patterns of Postnatal Developmental Variation
Developmental Variation in Macaca
Genus Macaca (subtribe Macacina) comprises at least four
species groups encompassing a minimum of 20 species
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Fig. 4 Geometric morphometric analysis of frontal and occipital
bone shape in African papionins. a 21 Frontal and 17 occipital 3D
landmarks and semi-landmarks were used in separate Procrustes
analyses (basi-occipital landmarks not shown); see Singleton (2009)
for landmark definitions. b In the frontal analysis, the second
principal shape component (PSC2) separates Cercocebus and Mandrillus (black) from Lophocebus, Papio, and Rungwecebus (grey);
symbols represent species M1-stage means. c Occipital PSC3
separates Lophocebus albigena, Papio, and Rungwecebus from
Cercocebus, Mandrillus, and L. aterrimus; symbols as in b. Wireframes represent phylogenetic shape differences summarized by PSC
axes; colors correspond to plot symbols
Evol Biol (2012) 39:499–520
505
(Fooden 1976; Delson 1980; Groves 2001, 2005). There
have been relatively few comparative studies of macaque
cranial ontogeny and even fewer (e.g., O’Higgins and
Collard 2002; Rook and O’Higgins 2002) including more
than two species groups. Fooden (1975) found ontogenetic
scaling of cranial proportions between M. silenus and
M. nemestrina. Within the sinica group, vertical displacements of ontogenetic trajectories have been shown to result
in geometric similarity between larger and smaller species
(Fooden 1988), a pattern commonly observed in response
to selection for increased body size (Gould 1971; Shea
1983a, b, 1985; Ravosa 1992; Vinyard and Ravosa 1998).
Profant’s comparison of M. fascicularis and M. nemestrina
found ontogenetic scaling of individual cranial dimensions
but significant displacements of multivariate growth vectors
(Profant 1995; Ravosa and Profant 2000). Mouri’s (1996)
comparison of multivariate ontogenetic allometries within
the fascicularis group found acceleration of positive facial
allometries and negative displacement of size-shape allometries resulting in increased relative facial prognathism at
absolutely smaller cranial sizes (Mouri 1996). Collard and
O’Higgins (2002) reported an absence of significant differences between ontogenetic vectors for M. mulatta and either
M. sylvanus or M. fascicularis; however, Rook and O’Higgins (2002) noted allometric displacements leading to
greater facial prognathism in M. fascicularis. Although
similar in their findings of parallel allometric trajectories,
with or without displacement, differences among these
studies in taxonomic sampling and methodology make it
difficult to draw more general conclusions.
To unify these prior findings, I present here a new comparative ontogenetic analysis encompassing the four major
species groups. Three-dimensional coordinates for 42 standard craniometric landmarks (Table 2) were collected on
cross-sectional ontogenetic series of five macaque species
(Table 3). Most specimens were wild shot and of known
provenience; however, zoo-reared specimens judged to
present normal (i.e., nonpathological) morphology were
included for M. sylvanus, which is poorly represented in
museum collections. Following generalized Procrustes
analysis in Morpheus (Slice 1998), cranial growth
allometries were explored using a principal components
analysis in form space, a morphospace constructed by augmenting the matrix of Procrustes-aligned coordinates by a
size vector, specifically log centroid size (Bookstein 1991;
Slice et al. 1996; Mitteroecker et al. 2004). In a form-space
PCA, the first principal component (FPC1) summarizes both
geometric size and the common allometric shape trend
(Mitteroecker et al. 2004), while subsequent PCs summarize
shape variation that is statistically independent of size
(Jolicoeur and Mosimann 1960; Jolicoeur 1963; Klingenberg
1996; Mitteroecker et al. 2004). Differences in allometric
scaling between species were tested by random permutation
of the angular difference between FPC1 eigenvectors calculated separately for individual species (Jolicoeur 1963;
Klingenberg 1996). Following McNulty et al. (2006), equal
random samples were drawn from every dental stage of each
species to yield equal samples with controlled dental-stage
distributions. The resulting mixed-sex samples each comprised a maximum of 7 juveniles and 10 adults. For each
comparison, individuals were randomly reassigned to species, and the angular difference between the randomized
samples was calculated. The observed angle, equaling the
arcosine of the vector correlation (Zelditch et al. 2004), was
significant if the proportion of 1,000 permuted values
exceeding it was less than a Bonferroni-corrected critical
value of 0.005 (Good 2000; Zelditch et al. 2004).
Angular differences between macaque ontogenetic trajectories (Table 4) are uniformly small (\10) and none are
statistically significant. Macaca sylvanus, which is distant
from other species both geographically and genetically
(Morales and Melnick 1998; Tosi et al. 2000), exhibits the
largest interspecies angles. A plot of the first two FPCs
(Fig. 5) shows parallel ontogenetic trajectories, with individuals sorted by dental stage on FPC1 and species on FPC2.
The interspecific differences in relative facial prognathism
and neurocranial shape summarized by FPC2 scores are
significant (one-way ANOVA; Bonferroni P \ 0.01) for all
species comparisons except M. assamensis–M. nemestrina,
which are not statistically distinguishable. These morphological differences are already present by the dp4 stage and
appear stable from M1 eruption through maturity.
Table 3 Macaque cross-sectional ontogenetic samples by dental stage
dp4
M1
M2
Ad$
Ad#
Total
M. assamensis
2
2
0
8
7
M. fascicularis
7
7
7
10
10
19
41
M. mulatta
4
4
5
5
5
23
M. nemestrina
2
5
4
4
10
25
M. sylvanus
3
2
3
11
13
32
Dental stage defined by eruption of the nominal tooth to full occlusion
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Evol Biol (2012) 39:499–520
Table 4 Angular differences between macaque ontogenetic trajectories
Ma
Mf
Mm
Mn
Ms
M. assamensis
–
0.387
0.036
0.078
0.080
M. fascicularis
6.55
–
0.373
0.237
0.131
M. mulatta
8.17
7.26
–
0.012
0.008
M. nemestrina
6.88
6.07
7.51
–
0.027
M. sylvanus
8.06
8.57
9.29
8.37
–
Below diagonal: angular differences (in degrees) between species ontogenetic trajectories are calculated as the arcosine of the vector correlation.
Above diagonal: P values based on 1,000 random permutations (see text); no angle is significant at the Bonferroni-corrected level of P = 0.005
While postnatal growth patterns have been investigated in a
number of papionins, there have been relatively few comprehensive, multi-genus studies of cranial ontogeny. Leigh
et al. (2003) and Leigh (2007) found Macaca, Lophocebus,
Cercocebus, and Mandrillus to largely follow associated
ontogenetic trajectories. By contrast, Papio exhibited a
complex allometry characterized by early displacement,
reflecting differences in neurocranial proportions that diminished during ontogeny due to convergence of ontogenetic
trajectories. O’Higgins and Collard (2002) also reported
shared ontogenetic shape trajectories in small-bodied papionins (Macaca, Lophocebus, and Cercocebus) but significantly
divergent trajectories in Mandrillus as well as Papio; in this
study, angular differences among trajectories were uniform,
falling in a narrow range of 21–36. Singleton et al.’s (2010)
comparison of papionin male developmental trajectories used
dental stage, rather than size, as a surrogate for ontogeny in
order to compare developmental patterns independent of
cranial size, which varies widely within this group. Pairwise
angular differences between species developmental vectors
were statistically insignificant and mostly small. Angles
between the trajectories of small-bodied papionins (macaques
Fig. 5 Form-space principal components analysis of macaque crosssectional ontogenetic series. The first principal component (FPC1,
x-axis) summarizes both cranial centroid size and the common pattern
of ontogenetic shape change; species’ allometric trajectories are
parallel (Table 2). FPC2 (y-axis) summarizes interspecific differences
in cranial shape, which are present by dp4 eruption and remain stable
from M1 eruption through adulthood. All pairwise differences in
FPC2 scores are significant (Bonferroni P \ 0.01) except that
between M. assamensis and M. nemestrina, which are not significantly different
These results indicate that although macaques have
undergone a rapid genetic and morphological diversification
(Fabre et al. 2009), they appear to have retained a common
postnatal growth pattern. Consistent with prior results
(Profant 1995; Mouri 1996; Ravosa and Profant 2000; Rook
and O’Higgins 2002), differences in adult cranial form result
either from simple allometric size shifts, as in M. fascicularis, or from differences in early, probably prenatal, morphogenesis that alter juvenile craniofacial proportions.
Developmental Variation in Papionini
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and mangabeys) ranged from 14 to 29; those for Papio,
Mandrillus, and Theropithecus, large-bodied taxa with pronounced sexual dimorphism, were considerably greater
(24–47). These results suggest that the conservation of
ontogenetic trajectories within Macaca reflects a papioninwide phenomenon; however, increases in size and/or size
dimorphism are associated with ontogenetic dissociation.
Effects of Postnatal Developmental Variation
While empirical studies of postnatal ontogeny can identify
differences in developmental patterning, they are less
successful at quantifying the impact of these differences on
adult cranial morphology. Developmental simulation
studies, in which different ontogenetic trajectories are
applied to a juvenile form to estimate its adult morphology
(Richtsmeier et al. 1993; Richtsmeier and Walker 1993;
Fig. 6 Estimated adult-male cranial morphology of Rungwecebus
kipunji. Estimates were created by applying the developmental vector
of different model species (indicated by taxon name) to the original
kipunji voucher specimen, FMNH 187122 (see Singleton et al. 2010
for details of estimation and visualization procedures). Wireframes
507
Ackermann and Krovitz 2002; Cobb and O’Higgins 2004;
McNulty et al. 2006), offer an alternative means of
exploring this question. In recent studies focusing on extant
hominines, estimated adults generated from the juvenile of
one species and the trajectory of another most closely
resembled adults of the juvenile species, even when species
trajectories were significantly different (Ackermann and
Krovitz 2002, Table S2; Cobb and O’Higgins 2004, Fig. 6;
McNulty et al. 2006, Table 4). However, the cranial morphologies of extant hominines are so different that they
may not provide a fair test of postnatal development’s
potential to alter the course of cranial morphogenesis.
Singleton et al. (2010) conducted a similar study of
Rungwecebus kipunji, using male developmental vectors
for a range of papionin species to ‘‘grow up’’ the cranium
of the M1-stage kipunji juvenile, FMNH 187122. Different
papionin vectors yielded extremely similar estimated adult
compare individual estimates (grey) to the average estimated adult
(black). Estimates are extremely similar to their average and to each
other; however, the simulated adult based on a mandrill developmental pattern reveals altered patterns of cranial integration (see text)
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508
morphologies (Fig. 6) with a level of shape variation (as
measured by Procrustes distances) comparable to that found
within papionin species (Singleton et al. 2010). This study
did not control for differences in vector length; however,
when developmental vectors were assumed to be infinite, all
but one passed closest to Lophocebus aterrimus in shape
space, irrespective of the vector’s source taxon (Singleton
et al. 2010). This test showed that differences in vector
length, while certainly important, would not be sufficient to
alter the kipunji’s fundamentally mangabey-like morphology. Although individual estimates did show minor speciesvector effects, e.g., adults based on Lophocebus vectors had
slightly more pronounced suborbital fossae (Fig. 6, center),
the influence of postnatal developmental variation was
minimal. This finding is perhaps best illustrated by an estimate based on the developmental vector of M. sphinx
(Fig. 6, far right), whose extreme level of developmental
shape change excluded it a priori as an appropriate model for
the kipunji (Singleton et al. 2010). Although based on a
patently unreasonable model, this estimate is not as dissimilar from the others as one might expect. Shape differences are restricted mostly to the face, which is both longer
and somewhat ‘‘boxier,’’ while the neurocranium and base
are virtually identical to those of the average estimate
(Fig. 6, far right wireframe). A mid-facial ‘‘break’’ in the
corresponding adult model reflects the morphing algorithm’s
inability to reconcile disparate patterns of developmental
shape change in these two regions. This obvious incompatibility between the mandrill developmental vector and the
kipunji’s juvenile cranial shape indicates that Mandrillus has
a different pattern of developmental integration between the
face and neurobasicranial complex (Enlow 1990; Lieberman
et al. 2000) than the other papionins studied. That the
mandrill vector neverthless yielded a mangabey-like adult
demonstrates that even major differences in regional
developmental patterns have only limited ability to divert a
juvenile morphology from its fated adult form.
Environmental Influences on Development
Postnatal cranial development in mammals is influenced by
a range of external environmental factors, including
nutrition, dietary consistency, mechanical loading, and
even temperature (Herring and Lakars 1982; Herring 1993;
Biewener and Bertram 1994; Ciochon et al. 1997; Cesani
et al. 2003; Lieberman et al. 2004; Ramı́rez Rozzi et al.
2005). Less frequently considered are the potential influences of social environment on cranial growth and development; however, there is growing evidence that social
factors can influence adult cranial phenotype.
Genus Mandrillus is characterized by extreme sexual size
dimorphism and bimaturism (Leigh 1992; Setchell et al.
2001). Male mandrills and drills experience an extended
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ontogeny during which body mass and facial dimensions
increase and sexual ornaments such as facial coloration and
bony paranasal ridges develop under the influence of androgenic hormones (Wickings and Dixson 1992b; Setchell et al.
2001; O’Higgins and Collard 2002; Setchell and Dixson 2002;
Elton and Morgan 2006). Social environment plays a pivotal
role in this process. Socially dominant males accelerate maturation, exhibiting faster growth, larger testes, higher testosterone levels, and more pronounced secondary sexual
characteristics (Wickings and Dixson 1992b; Setchell and
Dixson 2002). Sons of high-ranking mothers and males with
fewer peers garner similar developmental benefits (Setchell
et al. 2006), but only males who achieve alpha status fully
express the dominant ‘‘fatted’’ phenotype (Wickings and
Dixson 1992b).
Circulating androgenic hormones play a central role in
craniofacial development, particularly during adolescence,
via their direct effects on bone growth and remodeling as
well as indirectly through their impact on skeletal muscle
mass (Barrett and Harris 1993; Noda et al. 1994; Abu et al.
1997; Verdonck et al. 1999; Byron et al. 2004; Fujita et al.
2004; Lin et al. 2004; Cray 2009). In experimental studies,
androgens have been shown to increase cranial length and
facial dimensions, especially height and breadth (Barrett
and Harris 1993; Verdonck et al. 1999; Fujita et al. 2004).
Interestingly, these same facial dimensions are only weakly
correlated with measures of body size in male Mandrillus
(Wickings and Dixson 1992a; Elton and Morgan 2006),
suggesting that socially mediated differences in testosterone levels contribute to craniofacial variation in mandrills
and drills.
Leigh et al. (2003) hypothesized that late-growing structures such as the face are more strongly affected by growth
rate differences, which are greatest in late ontogeny (Leigh
1996). It follows that late-growing structures should also be
more susceptible to environmental perturbations affecting
growth. If so, the abnormal social environment of captivity
may account for a distinctive morphotype seen in captive
male mandrills and drills, whose crania typically appear less
klinorhynch (Ross and Ravosa 1991) than those of wild-type
males and exhibit increased facial dimensions and hypertrophy of the paranasal ridges and cranial superstructures
(Fig. 7, top right), making them seem ‘‘ultra-male.’’ It is
plausible that captive males, who typically lack male peers
(Bassett 2000), and thus experience unchallenged dominance, extend the normal developmental trajectory by
growing faster and/or longer under the influence of prolonged, elevated testosterone levels.
To explore this hypothesis, the methods of Singleton et al.
(2010) were adapted to model the effects of extended
ontogeny on male Mandrillus cranial morphology; the
results of this new developmental simulation are presented
here. The analysis employed a cross-sectional ontogenetic
Evol Biol (2012) 39:499–520
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Fig. 7 Wild- and captive-type adult male morphology in Mandrillus.
Top left young adult male Mandrillus leucophaeus cranium showing
normal, wild-type morphology. Top right cranium of zoo-housed
male M. leucophaeus, exhibiting captive-type morphology characterized by increased robustness, pronounced cranial superstructures,
lengthening of the anterior cranial base and face, increased facial
height, dorsal expansion of the paranasal ridges, and facial retroflexion. Bottom left digital surface model of a young-adult male
M. sphinx with wild-type morphology (courtesy of E. Delson and
W. Harcourt-Smith). Bottom right M. sphinx cranium simulated by
extending the male developmental trajectory two stages beyond the
normal adult terminus. In lateral view, the simulated ‘‘peramorph’’
exhibits multiple features of the captive-male morphotype (top right),
including robust cranial superstructures and zygomatic arches,
increased facial height and length, dorsal rotation of the palate, and
flattening of the cranial base. See Fig. 8 for additional views
series comprising crania of 7 juveniles (M1-stage = 2, M2stage = 5) of unknown sex and 7 adult males of Mandrillus
sphinx; all specimens were wild shot and of known provenience. The use of a (presumably) mixed-sex juvenile sample
is supported by prior findings that male and female
ontogenetic trajectories do not typically diverge until late
in ontogeny (O’Higgins and Jones 1998; O’Higgins and
Collard 2002; Leigh 2006). The data set comprised Procrustes-aligned 3D coordinates for 112 landmarks and 41
semi-landmarks (Table 2). Semi-landmarks were treated as
standard landmarks during superimposition (Gower 1975;
Rohlf and Slice 1990; Dryden and Mardia 1998).
The developmental vector for Mandrillus sphinx was
approximated by linear regression of Procrustes-aligned
coordinates on dental stage (McNulty et al. 2006); the
resulting regression coefficient vector summarizes shape
change between stages. To extend cranial development
beyond the normal adult terminus, the coefficient vector
was augmented by two stages and applied to the average
adult-male landmark configuration. This transformed
configuration was reflected and averaged to yield a symmetrical configuration with semi-landmarks on both sides.
Using Landmark 3.0.0.6, a 3D surface model of a wild
adult-male Mandrillus sphinx (Fig. 7, bottom left) was
warped to the transformed landmark configuration using
corresponding landmarks to direct the shape transformation
and thin-plate splines (TPS) to interpolate surfaces between
landmarks (Bookstein 1991; Wiley et al. 2005).
The resulting ‘‘peramorph’’ (Fig. 7, bottom right; Fig. 8,
right) exhibits many characteristics of captive males. In
comparison with the wild type, its palate and anterior cranial
base are relatively longer, and its muzzle is taller, particularly posteriorly, with dorsally expanded paranasal ridges
and larger, deeper maxillary fossae. Facial and bizygomatic
breadths and overall facial robustness are greater, and the
neurocranium exhibits frontal flattening and hypertrophy of
the sagittal, temporal, and nuchal crests. The appearance of
increased airorhynchy in the peramorph is due in part to
differences in muzzle shape but may also involve retroflexion (extension) of the cranial base. Certain aspects of the
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Evol Biol (2012) 39:499–520
Fig. 8 Wild-type and simulated captive morphology in male
Mandrillus. Left frontal and basal views of a young-adult male
M. sphinx cranium with wild-type morphology (surface model
courtesy of E. Delson and W. Harcourt-Smith). Right corresponding
views of the simulated M. sphinx ‘‘peramorph.’’ In frontal view (top
right), the peramorph exhibits increased midfacial and bizygomatic
breadths, increased facial prognathism, and dorsal expansion of the
paranasal ridges. In basal view (bottom right), the peramorph exhibits
lengthening of the anterior cranial base and palate and increased
bizygomatic breadth
simulated ‘‘peramorph’’ (e.g., its elongated molars and relatively small neurocranium) reflect limitations of the TPS
interpolation used to transform the surface model as well as
the inability of a global, linear model based on relatively
sparse data to account for differences in growth offset among
tissues (tooth versus bone) and regions (face versus neurocranium) (Mitteroecker et al. 2005). That said, the developmental model of mandrill peramorphosis successfully
reproduces multiple features of the captive mandrill
morphotype and therefore supports the hypothesis that captive male morphology is produced by extension of the normal developmental trajectory.
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Discussion
In the context of EvoDevo, the comparative method
‘‘yields phylogenetic morphospaces against which to test
Evol Biol (2012) 39:499–520
the developmental capacities of extant taxa’’ (Müller 2005:
98) as well as the plausibility of inferred ancestral patterns.
The goal of this study was to explore developmental patterns and processes hypothesized to have contributed to the
evolution of hominin cranial diversity. By extending the
taxonomic scope of comparison beyond the hominine
clade, it was hoped to establish the generality and/or particularity of hominin developmental patterns and increase
understanding of their contributions to fossil hominin cranial diversity. This ‘‘papionin perspective’’ on human
EvoDevo offers insights into postnatal development’s
potential role in the evolution of primate, thus hominin,
cranial form and suggests directions for future research.
Early Pattern Formation
Studies of hominine cranial development have consistently
found species-typical morphologies to be already present in
early juveniles stages, suggesting that species differences
in cranial form are the product of variation in prenatal
morphogenesis (Richtsmeier and Walker 1993; Ackermann
and Krovitz 2002; Strand Viðarsdóttir et al. 2002; Krovitz
2003; Bastir and Rosas 2004; Cobb and O’Higgins 2004;
Mitteroecker et al. 2004; McNulty et al. 2006; Bastir et al.
2007; Ponce de León et al. 2007; Gonzalez et al. 2010).
The present survey of juvenile papionin morphology suggests that early pattern formation is a more general phenomenon. Diagnostic cranial traits such as suborbital
fossae and paranasal ridges, as well as differences in the
relative proportions of cranial modules, are present from
earliest infancy (Leigh et al. 2003; Leigh 2007). Both
the present analysis of macaque ontogeny and prior studies
of juvenile morphology demonstrate that papionin
neurocranial and facial shape differences are present prior
to completion of the deciduous dentition and remain
stable through M3 eruption (O’Higgins and Jones 1998;
O’Higgins and Collard 2002; Singleton 2007, 2009).
The ontogeny of papionin cranial superstructures presents an interesting variation on the theme of early pattern
formation. In this case, it appears that subtle but consistent differences in juvenile neurocranial shape (Fig. 4) are
modulated by the epigenetic effects of mechanical loading
to yield phylogenetically diagnostic adult morphologies
(Moss and Young 1960; Cobb and O’Higgins 2004). By
extension, differences among hominines in the configuration of neurocranial crests and tori should not be written
down to relative size and/or muscle mass without first
looking for underlying neurocranial shape differences. It
is certainly worth exploring whether similar patterns
can be identified in juveniles of hominine taxa such as
Gorilla, Paranthropus, and Homo erectus, where cranial
superstructures are a prominent feature of the adult
phenotype.
511
Taken together, these findings indicate that in papionins,
as in hominines, species differences in cranial morphology
arise in the prenatal or very earliest postnatal phases of
development. This finding is consistent with a growing
body of direct evidence that fetal, and perhaps even
embryonic, developmental variation is a major contributor
to craniofacial differences among primate taxa (Richtsmeier et al. 1993; Jeffery 2003, 2007; Zumpano and
Richtsmeier 2003). Our growing appreciation of the influence of early development should inform hypotheses concerning early hominin cranial variation. It is unlikely, for
example, that differences in infra-orbital morphology
between modern humans and Neanderthals are due to
simple allometric variation (contra Maddux and Franciscus
2009).
Although beneficial to field workers, who can have
greater confidence in taxonomic attributions of juvenile
fossil specimens, the pivotal role of fetal morphogenesis
places a primary source of cranial diversity beyond the
reach of the fossil record and direct paleoanthropological
inquiry. The difficulties of investigating primate (including
human) fetal development are manifest, but advances in
imaging modalities such as magnetic resonance microscopy (lMRI) may ultimately furnish more and better data
on primate morphogenesis (Maronpot et al. 2004). In the
interim, hypotheses derived from the human fossil record
will continue to be tested against experimental and comparative research—and vice versa.
Postnatal Developmental Variation
The roots of the modern papionin radiation lie in the
latest Miocene (ca. 6–10 Mya), somewhat earlier than
the divergence of the hominin lineage around 6–7 Mya
(Raaum et al. 2005; Steiper and Young 2006). Despite a
long evolutionary history and considerable morphological
and geographic diversification, most extant papionin species exhibit similar patterns of postnatal cranial shape
change (O’Higgins and Collard 2002; Leigh et al. 2003;
Leigh 2007; Singleton et al. 2010; present study). Angular
differences between ontogenetic vectors of small-bodied
papionins are generally uniform and insignificant; however, large-bodied taxa show larger, and in some studies
significant, divergence of ontogenetic trajectories (O’Higgins and Collard 2002; Singleton 2009), as well as altered
size-shape relationships (Leigh et al. 2003; Leigh 2007).
The uniformity of developmental trajectories and absence
of phylogenetic patterning in trajectory variation imply that
small-bodied papionins conserve an ancestral pattern of
ontogenetic shape change from which the largest, most
sexually dimorphic taxa have diverged to varying degrees.
The general developmental conservatism of papionins
contrasts with extant hominines, where most studies find
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significant differences within and between extant genera in
patterns of postnatal ontogenetic shape change (Strand
Viðarsdóttir et al. 2002; Bastir and Rosas 2004; Berge and
Penin 2004; Cobb and O’Higgins 2004; Mitteroecker et al.
2004; Strand Viðarsdóttir and Cobb 2004; McNulty et al.
2006; Cobb and O’Higgins 2007; but see Ackermann and
Krovitz 2002). Interestingly, Homo, rather than the larger
and more dimorphic Gorilla, typically exhibits the most
divergent ontogenetic trajectories (Cobb and O’Higgins
2004). Divergence of multivariate ontogenetic trajectories
reflects differing patterns of ontogenetic shape change
(global or local), differences in morphological integration,
or combinations thereof (Cobb and O’Higgins 2004; Mitteroecker et al. 2004; McNulty et al. 2006). The strong
ontogenetic divergence described for the cranium of Homo
reflects its radically altered spatial relationships due to
dental reduction, accelerated brain growth, etc. (Cobb and
O’Higgins 2004; Leigh 2007). Among papionins, only
Theropithecus, which also possesses a dramatically reorganized and uniquely derived cranial morphology, exhibits
interspecific angles comparable to those for Homo (Cobb
and O’Higgins 2004; McNulty et al. 2006). But large
angles in Mandrillus and Papio are also indicative of
modularity, as evidenced by dissociations of neurocranial
and facial development (Leigh 2007; present study).
The function of size as a line of least evolutionary
resistance (Schluter 1996; Marroig and Cheverud 2005,
2009) is apparent in Macaca, where many interspecific
differences in cranial shape are linked to differences in
size. However, the apparent correlation in papionins
between very large body size and altered patterns of cranial
integration suggests this phenomenon may be self-limiting.
Increased body size exposes animals to a range of new
selective pressures—developmental, functional, ecological,
and social—any of which, alone or in combination, might
lead to differences in cranial integration (Marroig and
Cheverud 2005; Goswami 2006; Leigh 2007). But it is also
possible that large size itself, either directly or through its
attendant allometric shape changes, affects patterns of
cranial integration. It is likely that any given integration
pattern can be optimal only within a limited size range
beyond which it will become developmentally or functionally maladaptive, causing selection to favor new patterns of modular organization. Given the large range of
early hominin body sizes, the potential impacts of absolute
size and sexual dimorphism on cranial integration merit
further investigation.
Developmental simulation is proving to be a powerful tool
for identifying and exploring the effects of postnatal ontogenetic variation (Richtsmeier et al. 1993; Ackermann and
Krovitz 2002; Williams et al. 2002; McNulty et al. 2006;
Singleton et al. 2010). Applying different ontogenetic trajectories to a common starting shape highlights differences
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in morphological integration among species (e.g., in
Mandrillus, Fig. 6) and maps phenotypic ‘‘norms of reaction’’ for a given morphology under different ontogenetic
programs. In simulation studies of both papionins and
hominines, divergent ontogenetic trajectories have been
shown to produce only minor differences in adult shape,
mostly within observed ranges of intraspecific variation
(McNulty et al. 2006; Singleton et al. 2010). Even the trajectory of Mandrillus, which differs from other papionins in
its magnitude of ontogenetic shape change and patterns of
cranial integration (Singleton et al. 2010), yielded an estimated kipunji adult that is far more mangabey-like than
mandrill-like. Although postnatal development contributes
to cranial shape differences (Fig. 6), juvenile morphology
appears to be a far stronger determinant of adult cranial form.
Environmental Influences on Development
Cranial, and especially facial, development is characterized
by phenotypic plasticity, the ability of a genotype to produce alternative phenotypes in response to environmental
variation (Lieberman 1995, 1997, 2000; Schlichting and
Pigliucci 1998; West-Eberhard 2003; Lieberman et al.
2004). Plastic phenotypes may be continuously distributed
as norms of reaction, often under the influence of growth
factors and/or hormones (Schlichting and Pigliucci 1995,
1998), or exist as discrete alternative morphologies, i.e.,
polyphenism (West-Eberhard 1989). While the effects on
craniofacial development of environmental influences such
as nutrition and dietary consistency have been studied in a
variety of mammals, including primates (Herring and
Lakars 1982; Herring 1993; Biewener and Bertram 1994;
Ciochon et al. 1997; Cesani et al. 2003; Lieberman et al.
2004; Ramı́rez Rozzi et al. 2005), the impact of social
environment has yet to be fully explored (Setchell et al.
2006).
Adolescent male development in Mandrillus is mediated
by multiple social factors (e.g., maternal and individual
rank, peer cohort size), principally through their influence
on serum testosterone levels (Setchell et al. 2006). As seen
in this and prior studies, male cranial development is
characterized by divergence of adolescent ontogenetic
trajectories, decreased integration of the face and neurobasicranial complex, and increased variation in adult facial
dimensions (Wickings and Dixson 1992a; O’Higgins and
Collard 2002; Elton and Morgan 2006; Singleton et al.
2010). While the bimodal distribution of adult paranasal
ridge form is consistent with the polyphenic dichotomization
of males as ‘‘fatted’’ and ‘‘nonfatted,’’ most facial measurements are continuously distributed, suggesting hormonal mediation of cranial variation (West-Eberhard 1989;
Wickings and Dixson 1992a; Elton and Morgan 2006).
These trait distributions parallel those of androgen-sensitive,
Evol Biol (2012) 39:499–520
soft-tissue characters linked to dominance, indicating a
strong sociohormonal effect on craniofacial development
(West-Eberhard 1989; Wickings and Dixson 1992a, b;
O’Higgins and Collard 2002; Setchell and Dixson 2002;
Elton and Morgan 2006).
The present study employed developmental simulation
to test the hypothesis that captive-type cranial morphology
is the product of a socially induced extension of the normal
male ontogenetic trajectory. This ‘‘virtual experiment’’
indicates that many features of the captive phenotype are
peramorphic relative to the wild type (Figs. 7, 8). The
absence of a comparable captive-female morphotype and
restriction of the phenomenon to sexually dimorphic,
androgen-sensitive regions of cranium both point to a
hormonal rather than nutritional basis for this ontogenetic
shift. Given the close relationship between dominance and
male-hormone levels (Setchell and Dixson 2002), perturbation of the social environment is the likeliest cause.
Although further study of this phenomenon is needed, it is
probable that captive males are peramorphic due to a
socially induced, hormone-mediated extension of normal
male cranial development.
Paleoanthropologists have viewed phenotypic plasticity
primarily as a potential source of homoplasy and an
obstacle to phylogeny reconstruction (reviewed in Collard
and Wood 2007). By contrast, West-Eberhard emphasizes
‘‘the importance of plasticity as a diversifying factor in
evolution…contributing to the origin of novel traits and to
altered directions of change’’ (West-Eberhard 1989: 250).
The example of Mandrillus highlights several ways in
which phenotypic plasticity may have factored into early
hominin evolution.
Environmental parameters compatible with successful
development typically exceed those encountered in the
normal environment; the phenotypic potential of a developmental system may be fully expressed only under
extreme conditions, thus exposing new variation to natural
selection (West-Eberhard 1989; Schlichting and Pigliucci
1998). The captive mandrill morphotype demonstrates a
latent phenotypic potential only hinted at in wild individuals. The source of this untapped variation probably lies in
the dissociation of somatic and sexual development that
distinguishes mandrills from baboons (Leigh and Bernstein
2006).
Regardless of its source, the ability of social cues to
release new, and possibly extreme, variation to the action
of natural selection has the potential to accelerate (e.g.,
through runaway sexual selection) or alter the trajectory of
evolutionary change (West-Eberhard 1989; Schlichting and
Pigliucci 1998). This is particularly true when adult phenotypic variation has profound fitness consequences, as it
does for Mandrillus males. Not all males achieve social
dominance; for those who do, the reproductive window is
513
extremely limited and reproductive variance is consequently high (Wickings et al. 1993; Dixson et al. 2006;
Leigh et al. 2008). Thus, even subtle variations, particularly in secondary sexual characters, may confer disproportionate reproductive advantages.
The potential relationship between plasticity and male
reproductive variance may have implications for early
hominin evolution. Lockwood et al. (2007) identified patterns of male facial variation in Paranthropus robustus that
they interpreted as evidence for a mandrill-like pattern of
extended cranial development and a single-male mating
system. Whether Paranthropus males also exhibited polyphenic soft-tissue characters, as in Mandrillus and Pongo
(Utami et al. 2002), is (sadly) unlikely ever to be known.
But Lockwood et al.’s (2007) interpretation of Paranthropus cranial variation complements new findings concerning early hominin craniofacial and dietary adaptations.
The distinctive craniofacial morphology of robust australopiths was long thought to be an evolutionary adaptation to a specialized diet of hard and/or abrasive foods such
as nuts and tubers (Jolly 1970; Teaford and Ungar 2000;
Ungar and Sponheimer 2011); however, current evidence
suggests that australopiths were not hard-object specialists
(Ungar et al. 2011; Ungar and Sponheimer 2011). Microwear texture and stable isotope analyses indicate that
Paranthropus robustus was, at most, a hard-object fallback
feeder, while P. boisei ate predominantly C4 plants, most
likely sedges (Scott et al. 2005; Sponheimer et al. 2006;
Ungar et al. 2008; Ungar et al. 2011; Ungar and Sponheimer 2011). Not only did robust australopiths consume
very different diets from each other (Scott et al. 2005;
Ungar et al. 2008; Cerling et al. 2011), studies of extant,
durophagous primates fail to support the association of
robust-type facial morphology with habitual hard-object
feeding (Daegling et al. 2011).
With the classical dietary-adapatation model thus in
question, alternative hypotheses for the origin of robust
facial morphology should now be considered. Ackermann
and Cheverud (2004) found that to derive a robust australopith from a gracile ancestor requires positive selection on
the zygomatic region alone. Given that zygomatic breadth
is consistently dimorphic in catarrhine primates (O’Higgins
and Dryden 1993; O’Higgins et al. 2001; O’Higgins and
Collard 2002; Weston et al. 2004), this suggests a possible
role for sexual selection in australopith diversification.
Early hominin mating systems are a matter of fierce
debate, but the magnitude of australopith dimorphism
strongly favors some form of polygyny and intense male/
male competition (Plavcan 2001). Both male/male competition and high reproductive variance, as in Mandrillus,
favor the development of alternative male mating strategies
(West-Eberhard 1989; Leigh 1995; Plavcan 2001; Utami
et al. 2002). When alternative strategies are associated with
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adult-male polyphenism, disruptive selection (e.g., through
female choice) can lead to sympatric speciation (WestEberhard 1989). As noted by West-Eberhard, ‘‘Same-stage
alternative phenotypes are of special interest for the evolution of diversity because they are independent of each
other in the sense of being readily dissociable into separate
lineages’’ (1989: 260). Furthermore, species derived via
fixation of alternate phenotypes would be ‘‘expected to
achieve sympatry more readily than do those derived via
allopatric speciation from monophenic populations’’ (1989:
262). This mode of speciation produced the well-known
cichlid ‘‘species swarms’’ (Liem and Kaufmann 1984;
Meyer 1987), which demonstrate that in lineages possessing the requisite phenotypic plasticity, speciation via fixation of alternate phenotypes may occur repeatedly.
This phenomenon has yet to be documented in primates;
however, Singleton et al. (2010) noted similarities in
the developmental trajectories of Mandrillus sphinx and
Cercocebus torquatus, so it is possible that sympatric phenotypic divergence accounts for the apparent paraphyly
within the Cercocebus/Mandrillus clade (McGraw and
Fleagle 2006; Gilbert 2007). This conjecture requires testing,
but if speciation via male phenotypic divergence can be
shown to operate in nonhuman primates, then the answer to a
perennial question—how hominin species with broadly
overlapping diets survived in the same landscape—may lie
in sexual rather than adaptive selection.
Conclusions
This survey of papionin cranial ontogeny was undertaken to
examine aspects of primate cranial development potentially
relevant to human EvoDevo as well as to highlight the
importance of nonhominine models to our understanding of
the evolutionary development of hominin cranial diversity.
New findings concerning papionin development presented
here add to a substantial body of evidence that differences in
cranial proportions among primate species as well as specific
diagnostic characters (e.g., suborbital fossae) arise prior to or
shortly after birth and remain largely stable throughout
postnatal ontogeny. The development of papionin cranial
superstructures exemplifies the contribution of epigenetic
factors, such as mechanical loading, to the development of
adult morphology but also reiterates the importance of early
pattern formation in directing the expression of later-acting
factors. In addition, developmental simulation studies demonstrate that postnatal ontogenetic variation has only limited
influence on adult cranial morphology, with even extreme
developmental models producing reasonable results. It
seems increasingly clear that early morphogenesis is the
primary determinant of cranial shape, making juvenile
morphology reliably predictive of adult form.
123
Evol Biol (2012) 39:499–520
Although a principal source of cranial diversity is
effectively invisible to the fossil record, the implications of
these findings for both classical paleoanthropology and
human EvoDevo are generally positive. The primacy of
early development allows paleoanthropologists to have
confidence both in the taxonomic attribution of juvenile
hominin specimens and in the ability of developmental
simulation to provide robust estimates of ontogenetic
stages not represented in the fossil record. As embryonic
and fetal morphogenetic processes underpinning mammalian craniofacial variation are better understood, it should
be increasingly possible to link fossil hominin morphologies to the rate and timing of specific early developmental
events.
That said, the study of postnatal ontogenetic variation
remains an important and productive area of inquiry. The
overall conservatism of papionin postnatal developmental
patterns illustrates that differences in early pattern formation in combination with simple allometric shifts are sufficient to account for considerable morphological variation,
even in geographically and morphologically diverse lineages. Departures from this evolutionary path of least
resistance (Schluter 1996; Arthur 2004; Marroig and
Cheverud 2005, 2009), which signal strong natural selection on postnatal development leading to novel patterns of
developmental integration, are potentially informative
concerning adaptation and frequently suggest new directions for research.
The divergent ontogenetic trajectories of the largebodied ‘‘baboons’’ indicate links between cranial integration, sexual dimorphism, and body size that merit closer
scrutiny. It is unclear from prior studies whether interspecific differences in development are present throughout
postnatal ontogeny or are restricted to the more labile,
terminal period, as seen in intraspecific comparisons of
male and female trajectories (O’Higgins et al. 1990;
O’Higgins and Collard 2002). Interspecific comparisons of
female and pre-adolescent trajectories are required to
determine if postnatal ontogenetic divergences, and the
altered patterns of integration they imply, are species-wide
attributes, or restricted to a particular sex and/or life stage.
Much about papionin postnatal development points to the
latter, suggesting that a barbell—which is narrow for most
of its length but broad at its extremes—might be a more apt
metaphor for post-phylotypic primate ontogeny than Raff’s
hourglass (Raff 1996).
Primates are among the most intensely social of mammals, and the influence of socially mediated hormonal
differences on male development in Mandrillus clearly
implicates social environment in somatic as well as
behavioral variation. The capacity of social factors to
expose latent variation to natural and, especially, sexual
selection implies that under the right circumstances,
Evol Biol (2012) 39:499–520
primate social systems may actively create particular
variants, as opposed to merely favoring them. Thus, the
example of Mandrillus underscores the importance of
developmental plasticity as a source of phenotypic novelty
and a potential engine of diversification and speciation.
Extant hominids exhibit markedly divergent cranial
morphologies and occupy extremes of the postnatal
developmental spectrum, from delayed maturation and
minimal sexual dimorphism in humans to more rapid
development, pronounced sexual dimorphism, bimaturism,
and even polyphenism in the great apes (Plavcan 2001). By
exploring the more continuous developmental landscape of
papionins, it was hoped to achieve a better appreciation of
primate developmental variation and its effects on cranial
diversity. This admittedly selective review demonstrates
that the papionin perspective helps clarify the contributions
of embryogenesis, epigenesis, and environment to primate
cranial form, while new questions arising from these
inquiries show the value to human EvoDevo of casting the
comparative net a bit lower in the primate family tree.
Acknowledgments I am extremely grateful to Philip Mitteroecker
and Philip Gunz for inviting me to participate in the 21st Altenberg
Workshop in Theoretical Biology; to Gerd Müller and the staff of the
Konrad Lorenz Institute for their outstanding hospitality; and to my
fellow participants for their stimulating presentations and exceptional
collegiality. Analyses presented in this paper build on over a decade
of work by members of the NYCEP Morphometrics Group. In addition to my collaborators—Kieran McNulty, Steve Frost, John
Soderberg, and Emily Guthrie—I wish to thank the following institutions and individuals: Lawrence Heaney and William Stanley (Field
Museum of Natural History), Emmanuel Gilissen and Wim Wendelen
(Royal Museum for Central Africa), Georges Lenglet (Royal Belgian
Institute of Natural Sciences), Malcom Harmon (Powell-Cotton
Museum), Darren Lunde and Eileen Westwig (American Museum of
Natural History), Richard Thorington and Linda Gordon (National
Museum of Natural History), and Craig Hood and Nelson Rios
(Tulane University Museum of Natural History) for access to specimens and curatorial assistance. For data collection and other research
assistance, I thank Laura Mitchell, Leila Wagner, Matt Hunstiger,
Hayley Jirasek, Claire Kirchhoff, Caitlin Schrein, and Tony Tosi. For
use of the Mandrillus surface scan and generous, ongoing contributions to this research, I thank Eric Delson, Will Harcourt-Smith, the
late Leslie Marcus, and members of the NYCEP Morphometrics
Group. This research was supported by Midwestern University, the
University of Minnesota, the University of Oregon, the Field Museum
of Natural History, the University of Illinois–Urbana-Champaign,
NYCEP, and NSF #IIS-0513660 (S. Frost). This paper is NYCEP
Morphometrics Contribution 45.
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