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Journal of Human Evolution 118 (2018) 43e55

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Journal of Human Evolution

journal homepage: www.elsevier .com/locate/ jhevol

Basicranium and face: Assessing the impact of morphologicalintegration on primate evolution

Dimitri Neaux a, *, 1, Gabriele Sansalone a, b, c, 1, Justin A. Ledogar a, Sarah Heins Ledogar d,Theodora H.Y. Luk a, Stephen Wroe a

a Function, Evolution & Anatomy Research Lab, Zoology Division, School of Environmental and Rural Science, University of New England, NSW, 2351,Armidale, Australiab Department of Sciences, Roma Tre University, Largo San Leonardo Murialdo 1, I-00146, Rome, Italyc Center for Evolutionary Ecology, Largo San Leonardo Murialdo 1, I-00146, Rome, Italyd Department of Archaeology & Palaeoanthropology, School of Humanities, University of New England, NSW 2351, Armidale, Australia

a r t i c l e i n f o

Article history:Received 8 September 2017Accepted 12 February 2018

Keywords:DisparityModularityEvolutionary ratesGeometric morphometricsCranial base

* Corresponding author.E-mail address: dimitrineaux@gmail.com (D. Neau

1 Dimitri Neaux and Gabriele Sansalone should be

https://doi.org/10.1016/j.jhevol.2018.02.0070047-2484/© 2018 Elsevier Ltd. All rights reserved.

a b s t r a c t

The basicranium and facial skeleton are two integrated structures displaying great morphological di-versity across primates. Previous studies focusing on limited taxonomic samples have demonstrated thatmorphological integration has a significant impact on the evolution of these structures. However, thisinfluence is still poorly understood. A more complete understanding of craniofacial integration acrossprimates has important implications for functional hypotheses of primate evolution. In the present study,we analyzed a large sample of primate species to assess how integration affects the relationship betweenbasicranial and facial evolutionary pathways across the order. First, we quantified integration andmodularity between basicranium and face using phylogenetically-informed partial least squares ana-lyses. Then, we defined the influence of morphological integration between these structures on rates ofevolution, using a time-calibrated phylogenetic tree, and on disparity through time, comparing themorphological disparity across the tree with that expected under a pure Brownian process. Finally, weassessed the correlation between the basicranium and face, and three factors purported to have animportant role in shaping these structures during evolution: endocranial volume, positional behavior(i.e., locomotion and posture), and diet. Our findings show that the face and basicranium, despite beinghighly integrated, display significantly different evolutionary rates. However, our results demonstratethat morphological integration impacted shape disparity through time. We also found that endocranialvolume and positional behavior are important drivers of cranial shape evolution, partly affected bymorphological integration.

© 2018 Elsevier Ltd. All rights reserved.

1. Introduction

1.1. Morphological integration and cranial shape evolution

There is a considerable cranial morphological diversity acrossthe nearly 500 species, andmore than 70 genera, of extant primates(Mittermeier et al., 2013; Rylands and Mittermeier, 2014). Much ofthis variation is located in the basicranium and in the facial skeleton(Fleagle et al., 2010, 2016; Bennett and Goswami, 2012). Previousstudies suggest that these two structures evolved in a coordinated

x).considered co-first authors.

fashion in Homo (Bastir and Rosas, 2006, 2016; Gkantidis andHalazonetis, 2011), in the Hominoidea (Singh et al., 2012; Neauxet al., 2013; Neaux, 2017), and in the Platyrrhini (Marroig andCheverud, 2001; Marroig et al., 2004; Makedonska, 2014), indi-cating they may be morphologically integrated. This coinheritanceof character complexes (Cheverud, 1995) has been described as theconsequence of shared genetic processes, developmental path-ways, functional selective pressures, and/or phylogenetic con-straints (Lieberman, 2011; Marcucio et al., 2011; Parsons et al., 2011,2015; Bastir and Rosas, 2016; Martínez-Abadías et al., 2016).

Morphological integration between biological structures ispurported to have a significant impact on the evolution of newmorphologies (Wagner and Altenberg,1996; Schlosser andWagner,2004; Klingenberg, 2005). When the covariation level is high, the

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e5544

integration between traits is strong. In this case, morphologicalvariation is constrained and channeled into specific directions ofphenotypic space, corresponding to paths of least resistance(Marroig et al., 2004; Wagner et al., 2007; Klingenberg, 2010;Goswami et al., 2014; Evans et al., 2017). Conversely, whencovariation is lower between traits than within traits (i.e., traitsconstitute different modules), constraints on morphological varia-tion are reduced. In this case, specialization of traits is facilitated, asthe different structures can respond independently to selectiveforces.

In addition to phenotypic diversity, integration may also affectthe rate at which morphologies evolve, i.e., evolutionary rates. Astrong integration among structures, limiting the ability of aparticular structure to respond to selective pressures, or themagnitude of that response, may lead to a reduction in rates ofevolution for this specific structure (Goswami et al., 2014).

Previous studies underline the key role of morphological inte-gration in shaping the phenotypic diversity of the primate basi-cranium and face, notably in hominoids (Strait, 2001; Bastir andRosas, 2006, 2016; Gkantidis and Halazonetis, 2011; Singh et al.,2012; Neaux et al., 2013; Neaux, 2017). However, a comprehen-sive understanding of the impact of covariation on the evolution ofthese structures across primates is lacking. The present study isdesigned to assess how morphological integration affects therelationship between primate basicranial and facial evolutionarypathways. First (objective #1), we will quantify integration andmodularity between these structures across the primate clade.Then (objective #2), we will assess the extent of correlation be-tween primate basicranial and facial shapes, and three of the mainfactors purported to have played an important role in shaping thesestructures during primate evolution (i.e., endocranial volume [ECV],positional behavior, and diet). Finally (objective #3), we will definethe influence of morphological integration on shape disparitythrough time and rates of evolution for the basicranium and face.

1.2. Objectives of this study

Objective #1 The basicranium and face have been previouslydescribed as integrated structures in different primate clades(Marroig and Cheverud, 2001; Marroig et al., 2004; Bastir andRosas, 2006, 2016; Gkantidis and Halazonetis, 2011; Singh et al.,2012; Neaux et al., 2013; Makedonska, 2014; Neaux, 2017). Yet,studies of modularity in primates (Esteve-Altava et al., 2013,2015; Esteve-Altava, 2017), and at higher taxonomic levels(Goswami, 2006, 2007; Goswami and Polly, 2010), have revealedthat the basicranium and face can also be considered as twopartially decoupled modules. In the present study, we will, for thefirst time, test for both integration and modularity between thebasicranium and face across primates, including all the majorclades.Objective #2 Alongside morphological integration, multiple fac-tors influence the development and evolution of the basicraniumand face. The ECV and positional behavior (i.e., locomotion andposture) are among the main features influencing basicranialshape. Previous studies suggest that variation in morphology andflexion of the basicranium are mainly structural responses togenerate enough space in the braincase for an enlarged brain(Biegert, 1957; Ross and Ravosa, 1993; Spoor, 1997; Lieberman et al.,2000b; Bastir et al., 2010). Additionally, it has been hypothesizedthat primate species with more upright, or orthograde, positionalbehaviors exhibit an anteriorly positioned foramen magnum andcorresponding modifications to the morphology of thebasicranium (Dean and Wood, 1981; Russo and Kirk, 2013, 2017).Orthograde posture might also influence aspects of facialprognathism and orientation (Sirianni and Swindler, 1979; Ross,

1995; Zollikofer et al., 2005; Lieberman, 2011). Further, diet isconsidered to be a major factor affecting facial shape evolution inprimates (Anapol and Lee, 1994; Spencer, 1999). In particular, biteforce efficiency is considered to be adaptively significant (Rossand Iriarte-Diaz, 2014; Smith et al., 2015).

If morphological integration impacts the way ECV, positionalbehavior, and diet influence basicranial and facial shapes, changesin one of these features (ECV, positional behavior, and/or diet) arelikely to influence both structures (face and basicranium). Specif-ically, ECV and positional behavior, linked to basicranial shape,should also influence facial shape. Conversely, diet, related to themorphology of the face, should also impact the basicranium. Inorder to assess the impact of morphological integration, we definethe relationship between ECV, positional behavior, and diet on onehand, and between the ‘basicranium-face complex’ (BFC; i.e., theassociation of basicranial and facial structures), basicranium, andface on the other hand. We test the hypothesis that ECV, positionalbehavior, and diet significantly influence the shape of both thebasicranium and the face.

Objective #3 As previously suggested, morphological integrationcan affect both shape disparity and rates of phenotypic evolution(Goswami et al., 2014). In the present study, we test the influence ofintegration on the evolution of the basicranium and face byassessing shape disparity through time and rates of evolution inthe BFC, the basicranium, and the face. These analyses aim todetermine how morphological integration impacts the evolutionof the basicranium and face. If integration impacts shapedisparity and evolutionary rates, the two studied structuresshould behave as an almost uniform system (Klingenberg, 2008,2014). We will, thus, test the hypothesis that shape disparity andrates of evolution are similar in the BFC, the basicranium, and theface.

2. Material and methods

2.1. Sample

The sample consists of 141 crania of extant primates belongingto 54 different species (Table 1), constituting a representativesample of the diversity of the order, i.e., ~75% of the recognizedextant genera (Groves, 2001). One to three individuals, dependingon the availability of the specimens, represent each species. Thesample includes males and females for each species whereverpossible. We chose to include a great number of species ratherthan a great number of specimens for each species, as our studyfocuses on integration at the interspecific level. The list of speci-mens, including museum catalog number and location, can befound in the Supplementary Online Material (SOM) Table S1.Computed tomography (CT) scans were obtained from the Mor-phosource [dataset] (Aguilar et al., 2017a, 2017b; Allen andSchaeffer, 2017; Copes et al., 2017) and the National Museum ofNatural History (http://humanorigins.si.edu/evidence/3d-collection/primate) digital repositories. They belong to the col-lections of the Museum of Comparative Zoology at Harvard Uni-versity (Cambridge, USA), the National Museum of Natural History(Washington, USA), the Natural History Museum (London, UK),and the Duke Lemur Center (Durham, USA). All specimens weredetermined to be adults based on the full eruption of the thirdmolars. We created three-dimensional (3D) virtual representa-tions in PLY file format from CT scans with pixel size and slicethickness adjusted according to the cranial size of each specimenranging from 0.3 mm to 1 mm. We subsequently edited the sur-faces with Geomagic v.2014 software (3D Systems, 2014) to haveaccess to internal basicranial structures.

Table 1Species included in the study and number of specimens (n), males(m), females (f) and not determined individuals (nd).

Species n (m,f,nd)

Allenopithecus nigroviridis 2 (0,1,1)Alouatta caraya 3 (1,1,1)Aotus trivirgatus 3 (1,1,1)Arctocebus aureus 3 (2,1,0)Ateles geoffroyi 3 (1,1,1)Avahi laniger 1 (1,0,0)Bunopithecus hoolock 2 (0,2,0)Cacajao calvus 3 (1,1,1)Callicebus moloch 3 (3,0,0)Callithrix argentata 3 (2,1,0)Cebus capucinus 3 (0,3,0)Cercocebus torquatus 3 (2,1,0)Cercopithecus mitis 3 (1,2,0)Chiropotes satanas 3 (2,1,0)Chlorocebus sabaeus 2 (1,1,0)Erythrocebus patas 3 (1,1,1)Eulemur fulvus 2 (0,2,0)Euoticus elegantulus 3 (2,1,0)Galago senegalensis 3 (2,1,0)Gorilla beringei 3 (1,2,0)Hapalemur griseus 2 (2,0,0)Homo sapiens 3 (2,1,0)Hylobates lar 3 (1,2,0)Lagothrix lagotricha 3 (1,1,1)Lemur catta 3 (2,0,1)Leontopithecus rosalia 3 (0,3,0)Lepilemur mustelinus 1 (0,0,1)Lophocebus albigena 3 (1,2,0)Loris lydekkerianus 2 (1,1,0)Macaca fascicularis 3 (0,2,1)Mandrillus leucophaeus 3 (3,0,0)Microcebus murinus 2 (1,0,1)Miopithecus talapoin 2 (1,1,0)Mirza coquereli 1 (0,0,1)Nasalis larvatus 3 (2,1,0)Nomascus leucogenys 3 (0,3,0)Nycticebus coucang 3 (1,0,2)Otolemur crassicaudatus 1 (0,0,1)Pan troglodytes 3 (1,2,0)Papio anubis 3 (2,1,0)Perodicticus potto 3 (1,1,1)Piliocolobus badius 3 (1,2,0)Pithecia monachus 2 (1,0,1)Pongo abelii 3 (1,2,0)Presbytis rubicunda 3 (1,1,1)Propithecus verreauxi 3 (1,0,2)Pygathrix nemaeus 2 (1,1,0)Rhinopithecus roxellana 2 (2,0,0)Saimiri sciureus 3 (2,1,0)Semnopithecus priam 3 (1,2,0)Symphalangus syndactylus 3 (2,1,0)Theropithecus gelada 2 (1,1,0)Trachypithecus cristatus 3 (1,2,0)Varecia variegata 2 (0,0,2)

Figure 1. Cranium of Hylobates lar showing the basicranial (red) and facial (green)landmarks used in the study in superior (a), frontal (b) and, inferior views (c). (Forinterpretation of the references to color in this figure legend, the reader is referred tothe Web version of this article.)

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e55 45

2.2. Data acquisition

We used 3D landmark coordinates to describe basicranial andfacial shapes (Fig. 1, Table 2). The first dataset, describing the innerpart of the basicranium, included 26 landmarks. The second data-set, located on the face, consisted of 25 landmarks. We placed themon the 3D polygonal surfaces with IDAV Landmark v3.0 software(Wiley et al., 2005). To test for repeatability, we computed amultivariate analysis of variance (MANOVA) on the landmark co-ordinates of three Hylobates lar and three Nomascus leucogenysspecimens resampled three times, on three different days. Wecomputed the symmetric configurations from original landmarkcoordinates using MorphoJ v1.06 software (Klingenberg, 2011) to

reduce dimensionality in datasets where variables exceed samplesize (Singh et al., 2012).

2.3. Phylogenetic tree and covariates

The phylogenetic tree used in the following analyses is a time-calibrated consensus tree based on a Bayesian estimate (SOMFig. S1) obtained from the 10kTrees Project v3 for the 54 spe-cies in our dataset (Arnold et al., 2010). We also classified thespecies using similar taxonomic groups to those defined byFleagle et al. (2010, 2016) in their analysis of primate cranialshape diversity (SOM Table S2): Hominoidea, Cercopithecinae,Colobinae, Platyrrhini, Lemuriformes, and Lorisiformes. To allowfor a better assessment of intergroup variation, we divided theCercopithecidae into the Cercopithecinae and the Colobinae. Wemeasured the ECV of each specimen from virtual endocastsgenerated from the CT data (see SOM 1 and SOM Fig. S2 for de-tails). We also classified the species following their principal po-sitional behavior and their main dietary habits (see SOM Table S2for details and references).

2.4. Shape variation analyses

We performed all analyses in the R statistical environment (RCore Team, 2017). We used a generalized Procrustes analysis(Rohlf and Slice, 1990), implemented in the procSym() functionfrom the package ‘Morpho’ (Schlager and Jefferis, 2016) to rotate,translate, and scale landmark configurations to unit centroid size(CS), the square root of the sum of squared distances of thelandmarks from their centroid (Bookstein, 1991). To visualize themultivariate ordination of the aligned specimens, we performed a

Table 2Definitions of basicranial (1e26) and facial (27e51) landmarks.

Number Landmark Definition

1 Foramen caecum Most anterior inferior midline point of anterior cranial base2 Posterior cribriform Midline point at the posterior end of the cribriform plate3 Sphenoidale Most superior and posterior midline point on the jugum sphenoidale4 Tuberculum sellae Most superior and posterior midline point on the tuberculum sellae5 Sella Midline point at the center of the sella turcica6 Posterior dorsum sellae Midline point of the suture between the sphenoid and the basilar part of the occipital7 Basion Most anterior and inferior midline point on the margin of the foramen magnum8 Opisthion Most posterior and inferior midline point on the margin of the foramen magnum9, 10 Anterior clinoid process Most superior, posterior, medial point of the anterior clinoid process11, 12 Optic canal Most superior, anterior, lateral point of the optic canal13, 14 Anterior sphenoid Most anterior point of the middle cranial fossa on the ridge of the great wing of the sphenoid15, 16 Posterior frontal Point at where the posterior border of the anterior fossa fuses with the endocranial lateral wall17, 18 Foramen ovale Most superior, posterior, lateral point of the margin of the foramen ovale19, 20 Petrous apex Most superior, anterior, medial point of the margin of the apex of petrous part of the temporal bone21, 22 Pyramidal root Point where the posterior pyramidal ridge meets the temporo-occipital suture23, 24 Internal accoustic meatus Most inferior, anterior, medial point of the margin of the internal acoustic meatus25, 26 Occipital condyle Most lateral and inferior point on the margin of the foramen magnum27 Glabella Most anterior midline point on the frontal bone at the level of the supraorbital torus28 Nasion Midline intersection of nasal and frontal bones29 Rhinion Midline point at the inferior end of the internasal suture30 Nasospinale Most anterior midline point on nasal spine31 Prosthion Most anterior midline point of the maxillary alveolar process32 Incisive canal Point in the center of the incisive canal33 Staphylion Midline point on interpalatal suture corresponding to deepest point of notches at the rear of the palate34, 35 Superior margin of orbit Most superior point of the superior margin of the orbit36, 37 Frontomalare orbitale Point where the frontozygomatic suture crosses the inner orbital rim38, 39 Dacryon Most superior point at which the lacrimomaxillary suture meets the frontal bone40, 41 Zygoorbitale Point where the zygomaticomaxillary suture meets the orbital rim42, 43 Zygomaxillare Most inferior point of the zygomaticomaxillary suture44, 45 Alare Most lateral point on the margin of the nasal aperture46, 47 Alveolar Canine Point in the center of the lateral border of the canine alveolus48, 49 Jugale Point in the depth of notch between the temporal and frontal processes of the zygomatic bone50, 51 Posterior alveolar Most posterior point of the alveolar process on the inferior surface of the maxilla

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e5546

between-group PCA (bgPCA) from the package ‘Morpho’ (Schlagerand Jefferis, 2016) on the averaged Procrustes coordinates,considering the clades as groups. The bgPCA provides a projectionof the data onto the principal components of the group means,resulting in an ordination of the shape variables between thegroup means. The new axes are orthogonal and can be computedeven when the per group data matrices are not of full rank. Thismethod performs well when the number of observations in eachgroup is smaller than the number of variables (Boulesteix, 2005;Mitteroecker and Bookstein, 2011), which is usually the case forgeometric morphometric studies (Maiorino et al., 2015; Sansaloneet al., 2018). The significance of the observed shape changes be-tween clades was evaluated by performing a Procrustes analysis ofvariance (Procrustes ANOVA; Goodall, 1991) on aligned Procrustescoordinates using the function procD.lm() included in the Rpackage ‘geomorph’ (Adams et al., 2017). Pairwise comparisonswere performed using the function advanced.procD.lm() includedin the R package ‘geomorph’ (Adams et al., 2017). We removed allspecies represented by only one specimen from the pairwisecomparison.

2.5. Objective #1

Closely related species tend to be morphologically more similarto each other than to more distantly related taxa (Felsenstein,1985). Therefore, the specimens cannot be treated as indepen-dent units of information (Garland and Ives, 2000). We used theKmult statistic (Adams, 2014), a multivariate extension of Blom-berg's K (Blomberg et al., 2003), and the associated p-values, ob-tained via permutations of the data among the tree tips, to providea metric of the strength of the phylogenetic signal on the shape ofthe BFC, the basicranium and the face.

We assessed the covariation between basicranial and faciallandmarks using partial least squares (PLS) analyses (Bookstein,1991; Rohlf and Corti, 2000) from the ‘geomorph’ R package(Adams et al., 2017). PLS is suitable for the study of covariationbetween two sets of variables in several groups (McNulty, 2009;Bastir et al., 2010; Singh et al., 2012; Neaux et al., 2015a; Neaux,2017). We quantified the covariation for each pair of axes by acorrelation coefficient, which is supported by a permutation test forthe null hypothesis that the distribution of specimens on one axishas no bearing on the distribution on the other axis. We alsocomputed phylogenetically-informed PLS to estimate the degree ofmorphological covariation between the basicranium and the facewhile accounting for phylogeny (Adams and Felice, 2014). Theorientation of integration patterns in space can be interpreted asthe shape changes rate in one module relatively to the shapechanges in the other. This aspect is very important as it may revealwhether a common pattern of modules shape changes exists be-tween clades. In fact, groups may show similar integration co-efficients but have different integration patterns (Piras et al., 2017).In order to investigate this issue, we performed separate major axis(MA) analyses on the different clades shapes on the space identifiedby the first pair of PLS axes (Piras et al., 2017). MA is particularlyfitting because of its ‘symmetry,’ i.e., residuals are computedorthogonally to the line of best fit and coherently with PLS. It doesnot require the classic assumption of dependence-independencerelationship (Piras et al., 2017). MA slopes were then comparedthrough pairwise ANOVA, using clades as groups. We alsocomputed PLS for each studied clade in order to assess for differ-ences in the level of integration between clades. In order to define ifsexual dimorphism influences morphological integration, we alsotested for morphological integration in males and females sepa-rately. Additionally, we assessed the overall modularity between

Figure 2. a) Principal component analysis showing the repartition of the specimens inthe PC1ePC2 shape space. b) Phylogenetic morphospace representation of the 54studied species superimposing the branching patterns of the phylogeny (black lines)on the plot of PC1ePC2.

Figure 3. Wireframes showing the shape changes along PC1 and PC2. Shape changesare depicted in superior, frontal, and lateral views.

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e55 47

these structures using covariance ratios (Adams, 2016; Adams andCollyer, 2016). Phylogenetic versions of each analysis were per-formed on species averages.

2.6. Objective #2

We tested the relationship between ECV, positional behavior,and diet on one hand, and BFC, basicranial and facial morphologieson the other hand by performing a multivariate regression of shapeon each of these covariates using the ‘geomorph’ R package (Adamset al., 2017). We also used a phylogenetic generalized least squares(PGLS) linear model (Rohlf, 2001; Zelditch et al., 2012; Adams andCollyer, 2016) from ‘geomorph’ (Adams et al., 2017) to account fornon-independence among observations due to phylogenetic his-tory. Phylogenetic versions of each analysis were performed onspecies average.

2.7. Objective #3

We calculated the mean clade disparity through time for BFC,basicranium, and face shape variables. We compared themorphological disparity across our tree with that expected under apure Brownian process by simulating the traits evolution 10,000times across our tree. The mean disparity values for the observedand simulated data were plotted against the node age. We calcu-lated themean disparity through time using the function dtt() fromthe R package ‘geiger’ (Harmon et al., 2015). We also computed themorphological disparity index (MDI), quantifying the overall dif-ference in the relative disparity of a clade compared with theexpectation under the null Brownian motion model (McPeek, 1995;Harmon et al., 2003; Slater et al., 2010; Pearman et al., 2014).Negative MDI values indicate a lower clade disparity than expectedunder Brownian motion and are a common property of adaptivelyradiating clades. Positive MDI values indicate a higher subcladedisparity than expected under Brownian motion that is typical of acharacter evolution independent from time (Slater and Pennell,2014).

We evaluated the s2 evolutionary rates, defined as net rate ofphenotype change over time along a phylogeny, in the BFC, basi-cranium, and face shape variables using the time-calibratedphylogenetic tree. Rate differences between the basicranium andface, and between the taxonomic groups within the BFC, basicra-nium and face were tested using the function compare.evol.rates()of the R package ‘geomorph’ (Adams et al., 2017). Moreover, welooked for shifts in the rates in the phylogeny using the traitMEDUSA approach (Thomas and Freckleton, 2012). This methodallows one to detect where accelerations or slowdowns in the rateof phenotypic evolution occur within the phylogeny. This wasachieved by using the transformPhylo.ML() function of the Rpackage ‘MOTMOT’ (Thomas and Freckleton, 2012). The functionfirst fits a constant-rate Brownian model to the data, and thenworks iteratively through the phylogeny fitting a two-rate model ateach node in turn. Each two-ratemodel is compared to the constantrate model and the best two-rate model is retained. Keeping thelocation of this rate shift intact, it then repeats the procedure for athree-rate model and so on. Because we considered six differentclades, we searched for six major shifts across the phylogenetictree.

3. Results

3.1. Error test

Measurement errors show no significant differences betweenthe repeated samples (Wilk's l ¼ 0.99, F[2915] ¼ 0.55, p ¼ 0.76).

3.2. Shape variation analyses

In the bgPCA, the first two principal components (PC1 and PC2)explain, respectively, 66.20% and 21.00% of the total variance(Fig. 2a). Only PC1 and PC2 are represented here, as they are theonly two significant PCs according to scree test (Cattell, 1966). OnPC1, toward positive scores, the face is superoinferiorly shorter andmediolaterally wider, and the face and the palate are ante-roposteriorly longer (Fig. 3). The amount of orbital frontation (i.e.,the degree of verticality of the orbits) and orbital convergence (i.e.,the degree to which the right and left orbits face in the same di-rection) is lower (Ross, 1995). These changes are associated with amediolaterally narrower basicranium. The foramen magnum isdisplaced posteriorly. The face is also higher relative to the basi-cranium. These changes correspond mostly to Lemuriformes and

Table 3p-values of the non-parametric pairwise MANOVAs of Procrustes coordinates between the six taxonomic groups.

Cercopithecinae Colobinae Platyrrhini Lemuriformes Lorisiformes

Hominoidea <0.01 0.02 <0.01 <0.01 <0.01Cercopithecinae <0.01 <0.01 <0.01 <0.01Colobinae <0.01 <0.01 <0.01Platyrrhini <0.01 <0.01Lemuriformes 0.15

Figure 5. Wireframes showing shape changes along the singular axes of first pair(block 1 and block 2) of partial least squares analysis axes. Shape changes are depictedin superior, frontal, and lateral views.

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e5548

Lorisiformes (Fig. 2b). On PC2, toward higher scores the subnasalprognathism is more marked. The palate is also longer. The basi-cranium is anteroposteriorly longer. The orbits are smaller relativeto the size of the face. These changes correspond mostly to threecercopithecine genera belonging to the subtribe Papionina sensuStrasser and Delson (1987): Theropithecus, Mandrillus, and Papio(Fig. 2b). There are significant pairwise differences between all thetaxonomic groups in the shape space except between the twostrepsirrhine groups: Lemuriformes and Lorisiformes (Table 3).Shape variations on PC1 and PC2, for the face and the basicraniumseparately are presented in the supplementary information (SOMFig. S3).

3.3. Objective #1

The Kmult values indicate significant phylogenetic signal forthe BFC (Kmult ¼ 1.00; p < 0.01), basicranium (Kmult ¼ 1.40;p < 0.01), and face (Kmult ¼ 1.22; p < 0.01). The correlation co-efficient of the first pair of PLS axes (PLS1) between the basicra-nium and face is high and significant (r ¼ 0.87; p < 0.01). PLS1accounts for 76.9% of the total covariance. The correlation coeffi-cient of PLS1 is also significant for the phylogenetically-informedPLS (Fig. 4; r ¼ 0.88; p < 0.01). As covariation patterns are verysimilar between PLS and phylogenetically-informed PLS, we choseto present the latter here. Toward positive scores, the face issuperoinferiorly longer and mediolaterally narrower (Fig. 5). Thelower part of the face (i.e., prosthion to rhinion) is anteriorlyprojected relative to the upper part, increasing the subnasalprognathism. The orbit size increases relative to the size of theface. The orbital frontation and convergence are reduced. Thesechanges are associated with an anteroposteriorly longer andmediolaterally narrower basicranium. They are especially pro-nounced at the anterior and middle cranial fossae. The foramenmagnum is also displaced posteriorly. Finally, the cranial base issuperoinferiorly shorter in the midsagittal region that is thereforemore flat. Table 4 resumes the results from the MA analysis.

Figure 4. Scatter plots of the first partial least squares analysis axes between basi-cranial and facial shape.

Overall, the slopes are significantly different (p ¼ 0.004). Pairwisecomparisons reveal that Hominoidea possess significantlydifferent integration orientation from Platyrrhini and Lemur-iformes. In Colobinae, integration patterns are also significantlydifferent from Platyrrhini and Lemuriformes. The others cladesshow a common orientation of integration patterns. PLS computedfor each studied clade shows high and significant level of inte-gration for the Hominoidea (r ¼ 0.91; p < 0.01), the Cercopithe-cinae (r ¼ 0.97; p < 0.01), the Colobinae (r ¼ 0.86; p < 0.01), thePlatyrrhini (r ¼ 0.97; p < 0.01), the Lemuriformes (r ¼ 0.89;p < 0.01), and the Lorisiformes (r ¼ 0.97; p < 0.01). The correlationcoefficients of PLS1 for the phylogenetically-informed PLS withmales only (r ¼ 0.88; p < 0.01) and females only (r ¼ 0.88;p < 0.01) shows no difference from the one with both sexes,indicating that sexual dimorphism is not affecting the integrationpatterns described above. The covariance ratio value is betweenzero and one (CR ¼ 0.86; p < 0.01), characterizing a significant

Table 4Significance of the analysis of variance (ANOVA) of major axes (MA) slopes betweentaxonomic groups.

Group1 Group2 p

Cercopithecidae Colobinae 0.24Cercopithecidae Hominoidea 0.12Cercopithecidae Lemuriformes 0.05Cercopithecidae Lorsiformes 0.53Cercopithecidae Platyrrhini 0.05Colobinae Hominoidea 0.92Colobinae Lemuriformes 0.02Colobinae Lorsiformes 0.15Colobinae Platyrrhini 0.02Hominoidea Lemuriformes 0.01Hominoidea Lorsiformes 0.10Hominoidea Platyrrhini <0.01Lemuriformes Lorsiformes 0.46Lemuriformes Platyrrhini 0.99Lorsiformes Platyrrhini 0.46

Figure 6. Disparity-through-time plots for the basicranium-face complex (BFC, A), thebasicranium (B), and the face (C). The solid line represents the empirical data, and thedotted line represents the simulated data under Brownian motion. The grey shadedarea indicates the 95% disparity through time for the simulated data.

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e55 49

modularity between the two structures (Adams, 2016). Thephylogenetically-informed PLS gives a very similar covariance ra-tio (CR ¼ 0.84; p < 0.01) value.

3.4. Objective #2

Both multivariate and PGLS regressions show a significant in-fluence of ECV on the shape of the BFC, the basicranium, and theface (Table 5). The influence of positional behavior on the shape ofthe BFC, the basicranium, and the face is significant for all, exceptfor the PGLS regression with basicranial shape. Finally, the influ-ence of diet on the shape of the BFC, the basicranium, and the face issignificant for all regressions, but not significant for all PGLSregressions.

3.5. Objective #3

The morphological disparity through time (Fig. 6) is not signif-icantly different to that expected under the null model of Brownianmotion for the BFC (MDI ¼ �0.15; p ¼ 0.65), the basicranium(MDI ¼ �0.14; p ¼ 0.80) or the face (MDI ¼ �0.19; p ¼ 0.61). Adiversity peak, outside the range of what is expected underBrownianmotion is observable at relative time 0.93 for the BFC andface (about 5e6 Ma).

Morphological s2 evolutionary rates are significantly higher inthe primate face than in the basicranium (ER ¼ 7.08E-06;ER ¼ 3.84E-06, respectively; p < 0.01) at the order level. Evolu-tionary rates are, also, significantly different (p < 0.01) betweentaxonomic groups within the BFC, the basicranium, and the face.They are particularly high within the BFC and the face for theHominoidea and the Cercopithecinae, and within the basicraniumfor the Hominoidea (Table 6). Two positive shifts were detected inthe BFC and in the face (Fig. 7a, b), corresponding to the subtribePapionina (ES ¼ 4.04 and 3.98, respectively) and to the Hominidae(ES ¼ 4.22 and 3.54). In the basicranium, one positive shift corre-sponding to the Hominidae was detected (ES ¼ 7.04; Fig. 7c).

4. Discussion

4.1. Integration, modularity, and shape variations

Our morphological integration tests revealed highly significantintegration between the basicranium and face across primates. Theintegration patterns show that a longer and narrower face corre-spondwith a longer, narrower, and flatter cranial base. In contrast, asuperoinferiorly shorter andmediolaterally wider face is associatedwith an anteroposteriorly shorter and mediolaterally wider, androunder cranial base. These patterns correspond, respectively, to

Table 5Regression and phylogenetic regression (PGLS) analyses testing the influence ofendocranial volume, locomotor behavior, and diet on the shape of the basicranium-face complex (BFC), the basicranium, and the face.

R2 p PGLS-R2 p

Endocranial volumeBFC 0.10 <0.01 0.07 <0.01Basicranium 0.15 <0.01 0.07 <0.01Face 0.11 <0.01 0.16 <0.01Locomotor behaviorBFC 0.43 <0.01 0.11 0.02Basicranium 0.38 <0.01 0.02 0.59Face 0.42 <0.01 0.11 0.04DietBFC 0.22 0.01 0.05 0.19Basicranium 0.18 0.04 0.08 0.06Face 0.23 <0.01 0.06 0.12

the dolichocephalic and brachycephalic conditions that have beenpreviously described in the Hominoidea (Enlow and Hans, 1996;Lieberman et al., 2000a; Bastir and Rosas, 2004; Mitteroecker andBookstein, 2008; Singh et al., 2012; Neaux, 2017). In terms of pat-terns of integration, Hominoidea as well as Colobinae differsignificantly from Lemuriformes and Platyrrhini. Even if it is

Table 6Evolutionary rates (s2) of each taxonomic groups within the BFC, the basicraniumand the face.

BFC Basicranium Face

Hominoidea 9.31E-06 8.94E-06 9.69E-06Cercopithecinae 9.59E-06 5.12E-06 1.42E-05Colobinae 3.21E-06 1.47E-06 5.03E-06Platyrrhini 4.03E-06 3.63E-06 4.45E-06Lemuriformes 2.60E-06 1.49E-06 3.75E-06Lorisiformes 2.69E-06 1.73E-06 3.69E-06

57

58

59

60616263

6465

66

6768

69

7071

7273

74

75

767778

7980 81

82

83

84 85

868788

89

9091 92

94

9596 97

98

99100101

102103

104

105

106 107

Allenopithecus nigroviridisCercopithecus mitisErythrocebus patasChlorocebus sabaeusMiopithecus talapoin

Cercocebus torquatusMandrillus leucophaeusLophocebus albigenaTheropithecus geladaPapio anubis

Macaca fascicularisPiliocolobus badiusNasalis larvatusPygathrix nemaeusRhinopithecus roxellanaSemnopithecus entellusTrachypithecus cristatusPresbytis comataBunopithecus hoolockHylobates larSymphalangus syndactylusNomascus leucogenys

Gorilla beringeiHomo sapiensPan troglodytes troglodytesPongo abelii

Alouatta carayaAteles geoffroyiLagothrix lagotrichaAotus trivirgatusCallithrix argentataLeontopithecus rosaliaCebus capucinusSaimiri sciureusCacajao calvusChiropotes satanasPithecia pitheciaCallicebus molochMicrocebus murinusMirza coquereliLepilemur mustelinusAvahi lanigerPropithecus verreauxiEulemur fulvus fulvusHapalemur griseusLemur cattaVarecia variegata variegataArctocebus aureusPerodicticus pottoLoris lydekkerianusNycticebus coucang

Euoticus elegantulusGalago senegalensisOtolemur crassicaudatus

55

56

93

BFC

80 81

Allenopithecus nigroviridis

Symphalangus syndactylusGorilla beringeiHomo sapiensPan troglodytes troglodytesPongo abelii

Varecia variegata variegata

Otolemur crassicaudatus

55

56

57

58

59

60616263

6465

66

6768

69

70717273

74

75

767778

79

82

83

8485

868788

89

9091 92

93

94

9596 97

98

99100101

102103

104

105

106107

Cercopithecus mitisErythrocebus patasChlorocebus sabaeusMiopithecus talapoinCercocebus torquatusMandrillus leucophaeusLophocebus albigenaTheropithecus geladaPapio anubis

Macaca fascicularisPiliocolobus badiusNasalis larvatusPygathrix nemaeusRhinopithecus roxellanaSemnopithecus entellusTrachypithecus cristatusPresbytis comataBunopithecus hoolockHylobates larNomascus leucogenys

Alouatta carayaAteles geoffroyiLagothrix lagotrichaAotus trivirgatusCallithrix argentataLeontopithecus rosaliaCebus capucinusSaimiri sciureus

Cacajao calvusChiropotes satanas

Pithecia pitheciaCallicebus molochMicrocebus murinusMirza coquereliLepilemur mustelinusAvahi lanigerPropithecus verreauxiEulemur fulvus fulvus

Hapalemur griseusLemur catta

Arctocebus aureusPerodicticus pottoLoris lydekkerianusNycticebus coucang

Euoticus elegantulusGalago senegalensis

56

57

58

69

7071

7273

74

75

767778

7980 81

82

83

84 85

8687 88

89

9091 92

94

9596 97

98

99100101

102103

104

105

106 107

Papio anubisMacaca fascicularisPiliocolobus badiusNasalis larvatusPygathrix nemaeusRhinopithecus roxellanaSemnopithecus entellusTrachypithecus cristatusPresbytis comataBunopithecus hoolockHylobates larSymphalangus syndactylusNomascus leucogenys

Gorilla beringeiHomo sapiensPan troglodytes troglodytesPongo abelii

Alouatta carayaAteles geoffroyiLagothrix lagotrichaAotus trivirgatusCallithrix argentataLeontopithecus rosaliaCebus capucinusSaimiri sciureusCacajao calvusChiropotes satanasPithecia pitheciaCallicebus molochMicrocebus murinusMirza coquereliLepilemur mustelinusAvahi lanigerPropithecus verreauxiEulemur fulvus fulvusHapalemur griseusLemur cattaVarecia variegata variegataArctocebus aureusPerodicticus pottoLoris lydekkerianusNycticebus coucang

Euoticus elegantulusGalago senegalensisOtolemur crassicaudatus

55

59

60616263

6465

66

6768

93

Allenopithecus nigroviridisCercopithecus mitisErythrocebus patasChlorocebus sabaeusMiopithecus talapoin

Cercocebus torquatusMandrillus leucophaeusLophocebus albigenaTheropithecus gelada

Face

Basicranium

Figure 7. Phylogenetic trees. Transformed tree with branch lengths proportional to morphological evolutionary rates for the basicranium-face complex (BFC), the basicranium, andthe face. Red numbers indicate acceleration. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e5550

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e55 51

difficult to provide a solid interpretation concerning these specificdifferences, this result is potentially important as it points out thepresence of different patterns of cranial integrationwithin primates(Esteve-Altava et al., 2015). In several clades of primates, cranialvariations may therefore be related to different and possibly uniquemodels of integration between basicranial and facial structures. Interms of integration level, previous studies found a pervasiveintegration within the cranium, notably between the basicraniumand face, in Homo (Bastir and Rosas, 2006, 2016; Gkantidis andHalazonetis, 2011), in the Hominoidea (Singh et al., 2012; Neauxet al., 2013; Neaux, 2017), and in the Platyrrhini (Marroig andCheverud, 2001; Marroig et al., 2004; Makedonska, 2014). Our re-sults confirm that it is also the case when the whole order isconsidered. We also found significant modularity between thestudied structures, in line with the recent body of work by Esteve-Altava and colleagues (Esteve-Altava et al., 2013, 2015; Esteve-Altava, 2017), corroborating the presence of two independentphenotypic modules in the cranium of primates: one facial and onebasicranial. Our results confirm that, if the basicranium and the facecan be considered as two distinct modules (i.e., integration isstronger within these structures than between them), there is still asignificant relationship between them that can be defined as inter-module integration (Esteve-Altava et al., 2013; Klingenberg, 2013).

Concerning shape variation analyses, we found trends similarto those described by Fleagle et al. (2010, 2016). An increase inorbital frontation and convergence is associated with a moreflexed, larger, and shorter cranial base. In our study, it is also linkto a short and more orthognathic face. An increase in palate andsnout lengths is associated with a reduction of the size of theorbits relative to the size of the face. The Strepsirrhini differ fromthe Haplorrhini by the presence of a superoinferiorly shorter facelocated higher relative to the basicranium, a longer palate, largerorbits with a lower amount of frontation and convergence, and aposteriorly displaced foramen magnum. Despite considerableoverlap, significant interspecific differences in BFC shape exist inHaplorrhini, as well as in Anthropoidea. This result corroboratesprevious studies based on external cranial shape (Fleagle et al.,2010, 2016; Bennett and Goswami, 2012). We also found that,contrary to what is observed in the Haplorrhini, or even theAnthropoidea, there are no significant differences between thestrepsirrhine clades, Lemuriformes and Lorisiformes, based on ourlandmark data.

4.2. Correlation of basicranium and face with endocranial volume,positional behavior, and diet

Endocranial volume Our results support the hypothesis that ECVsignificantly influences BFC, basicranial and facial shape, evenwhen phylogeny is taken into account. The significant influence ofECV on basicranium morphology is in line with Aristide et al.(2015), who found that encephalization has a significant,although limited, influence on basicranial shape in thePlatyrrhini. The influence of ECV on basicranial shape alsocorroborates the hypothesis that brain size increase plays animportant role in midsagittal flexion (Ross and Ravosa, 1993;Strait and Ross, 1999; Lieberman et al., 2000b; Bastir et al., 2010)and, to a lesser extent, in the overall morphology of thebasicranium (Neaux et al., 2013; Bastir and Rosas, 2016; Neaux,2017). The significant interaction between ECV and the face islikely an indirect consequence of the integration linkingbasicranial and facial structures. It has been hypothesized thatbrain size increase led to the midsagittal flexion of the cranialbase, which caused a ‘mechanical’ downward rotation of the face,as the angle between the anterior part of the cranial base (i.e., theanterior cranial fossae) and the face is constant, around 90�

(Enlow and Azuma, 1975; McCarthy and Lieberman, 2001; Neauxet al., 2015b).

Positional behavior Our results do not support the hypothesis thatpositional behavior has a significant influence on basicranial shape,while it is significant for BFC and facial shape, evenwhen phylogenyis taken into account. The non-significant relationship betweenpositional behavior and the basicranium is in line with previousstudies showing that, except for bipedal Homo sapiens, the varietyof positional behaviors cannot explain the position of theforamen magnum within extant hominoids (Dean and Wood,1981; Neaux et al., 2017). Indeed, these studies found similarforamen magnum positions in Gorilla and Pongo, two taxapossessing very different positional behaviors (Remis, 1998;Thorpe and Crompton, 2006). Our results underline the proposalthat, in other primate clades, the relationship between basicranialshape and positional behavior is also not significant. Our findings,therefore, confirm that positional behavior is not the main factorinfluencing basicranial flexion (Ross and Ravosa, 1993; Strait andRoss, 1999). As we showed above, the relationship betweenbasicranium shape and ECV is highly significant. This strongcorrelation may overshadow the link between basicranium shapeand positional behavior (Ross and Ravosa, 1993; Strait and Ross,1999; Bastir et al., 2010). The significant influence of positionalbehavior on facial shape agrees with previous studies finding arelationship between the orbital plane (i.e., the plane formed bythe upper and lower margins of the orbit in sagittal view) andhead posture (Ross and Ravosa, 1993; Strait and Ross, 1999). Thislink can be explained by the necessity for primates to move intheir environment while keeping orbital planes approximatelyperpendicular to the ground, regardless of their positionalbehavior (Ross, 1995; Zollikofer et al., 2005; Lieberman, 2011).

Diet Our results show a significant interaction between diet andshape. However, this effect disappears when phylogeny is takeninto account. This result differs from what is observed in themandible, where the influence of diet on morphology has beendefined as significant, although weak, in the primate order as awhole, as well as in the Strepsirrhini and the Platyrrhini (Baab et al.,2014; Meloro et al., 2015). This difference is potentially explainedby the multiplicity of functions the cranium must perform (e.g.,vision, respiration, mastication, or brain protection), which affectsgreatly basicranial and facial shape evolution (Lieberman, 2008,2011). In contrast, the mandible performs fewer functions and itsmorphology is perhaps more closely related to diet and feedingbehaviors (Daegling, 1992; Taylor, 2006a, 2006b; Wroe et al.,2010). However, unlike the close link between diet and dentalmorphology (Kay, 1975; Kinzey, 1992; Ledogar et al., 2013), therelationship between diet, feeding behavior, andcraniomandibular morphology is poorly defined (Ross et al., 2012;Ross and Iriarte-Diaz, 2014).

Our finding of a non-significant relationship between cranialstructures (basicranium and face) and diet corroborate the asser-tion that the shape of the primate cranium is not strongly influ-enced by dietary ecology. However, mechanical data for primatefoods are all but entirely lacking and we are limited by broad di-etary categories, such as ‘frugivore’ and ‘folivore’ (Meloro et al.,2015). These categories fail to capture the true dietary diversityexhibited by primates. Species assigned to the same dietary cate-gory often exploit foods with drastically different mechanical and/or chemical properties, leading to diversification in dietary adap-tation (Van Roosmalen et al., 1988). Further study is thereforerequired to more comprehensively assess the relationship betweendiet and craniofacial shape in primates. Additionally, future studiesthat more closely examine the influence of food mechanical prop-erties on patterns of integration within the facial skeleton (e.g.,

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e5552

Makedonska et al., 2012) will also help improve our understandingof primate cranial evolution.

4.3. Influence of morphological integration on disparity throughtime and rates of evolution

Face and basicranium shape diversifications through time didnot show any significant departure from Brownian motion expec-tation, revealing that diversification occurred more within thanbetween clades (Slater et al., 2010). We can therefore hypothesizethat the high morphological integration between basicranium andface, constraining variations in specific direction of the phenotypicshape space, is one of the features that allowed similar disparitypatterns in the two studied structures (Goswami et al., 2014).However, a disparity peak corresponding to a burst in the evolutionof facial shape around 5 to 6 Ma is also noticeable. It broadly cor-responds to differentiations within three clades Homo-Pan, Cerco-cebus-Mandrillus, and Lophocebus-Theropithecus-Papio (Delson,1992; Brunet et al., 2002; Perelman et al., 2011; Liedigk et al.,2014). This evolutionary burst corresponds to the establishmentof a short face in Hominini shortly after the Hominini-Panini split asdescribed in Sahelanthropus tchadensis (Brunet et al., 2002; Guyet al., 2005) and Ardipithecus ramidus (Suwa et al., 2009). It is alsoin line with the evolution of a longer snout in the Papionina whencompared to Macaca, their closest relative (Gilbert, 2013). Previousworks have suggested that the retracted face of mangabeys(Lophocebus and Cercocebus) is a secondarily derived feature, aproduct of convergent evolution (Singleton, 2002; Gilbert, 2013).The convergent evolution of anteroposteriorly shorter faces inthese species has been hypothesized to be functionally related to ahard object (e.g., unripe fruit, hard seeds, and nuts; Fleagle andMcGraw, 1999) feeding niche (Singleton, 2004). This result cor-roborates our findings of a unique burst corresponding with anelongation of the face at the root of Papionina. Our findings,partially, contrast with those of Meloro et al. (2015), who detected aburst in mandible shape evolution during the early Oligocene inprimates, as well as a departure from Brownian motion in thePlatyrrhini. These differences can be explained by the weakermorphological integration linking the cranium and mandible(Bastir et al., 2004, 2005; Neaux et al., 2015a), when compared withthe integration between the basicranium and face (Bastir andRosas, 2016; Neaux, 2017), allowing different disparity patterns inmandibular structures.

Despite being highly integrated structures, the face and basi-cranium show significantly different evolutionary rates in primatesas a whole, with the face having higher rates than the basicranium.These results agree with the findings of Goswami et al. (2014), i.e.,that phenotypic integration does not influence evolutionary rates.Previous authors have suggested that bony structures, such as theface, subject to repeated biomechanical stresses during growthshould be more variable, and therefore more phenotypically plastic(Lycett and Collard, 2005; Collard and Wood, 2007; von Cramon-Taubadel, 2009). In contrast, structures less impacted by mastica-tory strain, such as the inner cranial base, should be less plastic.Also, the cranial base reaches its adult size before the face and itsgrowth is therefore under tighter intrinsic control (Lieberman andMcCarthy, 1999; Bastir et al., 2006; Parsons et al., 2015). This dif-ference in the developmental timing is another potential factorillustrating why the cranial base is less plastic. These findings couldexplain why, in our study, evolutionary rates are higher in the facethan in the basicranium. Also, as previously described, basicranialshape is correlated with ECV, while facial shape is correlated withboth ECV and positional behavior (see Objective #2). The primateorder displays a considerable diversity of locomotor and posturalhabits (Fleagle, 2013) that impact facial and orbital orientations

(Ross, 1995; Zollikofer et al., 2005; Lieberman, 2011). This correla-tion plays a major role in the primate facial diversity and can beanother factor explaining the higher evolutionary rates of thisstructure when compared to the basicranium.

Similarly, we found significantly higher evolutionary rates in theHominoidea and the Cercopithecinae than in the other primateclades, revealing that rates are not constant throughout the order.The positive evolutionary shifts that we found in BFC and in theface, related to the Papionina and the Hominidae, correspond to thedisparity peaks found in the diversification through time analyses.These shifts in the BFC and facial shape are present in two primateclades with remarkably different positional behaviors: terrestrialquadrupedalism in the Papionina (except for mangabeys, which arearboreal quadrupeds, partially for Cercocebus and totally forLophocebus), and bipedalism, knuckle-walking, vertical climbing,and below-branch suspension in the Hominidae (Doran, 1989;Remis, 1998; Schmitt, 1998; Thorpe and Crompton, 2006;Harcourt-Smith, 2007; Schmidt, 2011). This result corroboratesour previous finding of a significant correlation between the BFC,the face, and positional behavior (see Objective #2). It underlinesonce again the fact that modifications in positional behaviors dur-ing primate evolutionmay be one of themain drivers of facial shapechanges related to orbital plane and head posture (Ross and Ravosa,1993; Strait and Ross, 1999).

Many other factors have been linked to facial elongation in thePapionina and facial shortening in the Hominini. For example,Hylander (2013) contrasted these groups by arguing that the longfaces of baboons evolved to increase gape and accommodate tallcanines that were selected for under intense male-male competi-tion, whereas social pressures were relaxed in the Hominini infavor of selection for shorter faces, and increased bite force. Addi-tionally, facial retraction in the Hominini, and particularly theunique facial configuration of modern humans, offers several otherpurported advantages, including an increased range of speechsounds used in vocalization (Lieberman and McCarthy, 1999; butsee Fitch et al., 2016).

The only positive evolutionary shift found in the basicranium,corresponding to the Hominidae may correspond to the setup ofbigger brains in this clade when compared to other primates (Isleret al., 2008; Bienvenu et al., 2011). It underlines the major role ofencephalization in the evolution of the hominid cranium. It alsohighlights the great influence of ECV, along with positionalbehavior, in the evolution of cranial shape in primates.

5. Conclusions

Our results support the hypothesis that the basicranium andface are two significantly integrated structures in primates(Marroig and Cheverud, 2001; Marroig et al., 2004; Bastir andRosas, 2006, 2016; Gkantidis and Halazonetis, 2011; Singh et al.,2012; Neaux et al., 2013; Makedonska, 2014; Neaux, 2017). How-ever, we also found that these two traits can be considered as twodistinct modules (Esteve-Altava et al., 2013, 2015; Esteve-Altava,2017). The relationship between these structures can therefore bedefined as inter-module integration (Esteve-Altava et al., 2013;Klingenberg, 2013). We described ECV and positional behavior astwo major drivers of primate cranial shape evolution, partly influ-enced by morphological integration (Ross and Ravosa, 1993; Straitand Ross, 1999; Lieberman et al., 2000b; Bastir et al., 2010). Themajor disparity peaks and burst in evolution related to ECV and thebasicranium correspond to the great encephalization occurring inthe Hominoidea, and in particular in the Hominini (Isler et al.,2008; Bienvenu et al., 2011). The shifts related to the face can belinked to the simultaneous evolution of short faces in the Homi-nidae (Lieberman, 2011) and long ones in the Papionina (Gilbert,

D. Neaux et al. / Journal of Human Evolution 118 (2018) 43e55 53

2013), as well as the evolution of different positional behaviors. Wedid not find any significant correlation between diet and cranialstructures when phylogeny was taken into account (Ross et al.,2012; Ross and Iriarte-Diaz, 2014), contrary to what has beenfound in the mandible (Meloro et al., 2015). Finally, our results arein line with the hypothesis that morphological integration impactsshape disparity but not rates of phenotypic evolution (Goswamiet al., 2014). Indeed, we found that morphological integration isconstraining the diversification patterns through time, not allowingany significant departure from Brownianmode of evolution, but weshowed that even two highly integrated structures (basicraniumand face) could have different evolutionary rates in response todifferent selection pressures.

Acknowledgments

We thank the Smithsonian's Division of Mammals (Dr. K. Hel-gen) and Human Origins Program (Dr. M. Tocheri) for the scans ofthe National Museum of Natural History specimens used in thisresearch. These scans were acquired through the support of theSmithsonian 2.0 Fund and the Smithsonian's Collections Care andPreservation Fund. We also wish to thank the following institutionsfor allowing us the access to their specimens: the Museum ofComparative Zoology at Harvard University, the Natural HistoryMuseum, and the Duke Lemur Center. We thank three anonymousreviewers for the helpful suggestions and comments that haveimproved this manuscript. We also thank Dr. C.H.R. Goatley for hiscomments on this manuscript. We are grateful to Dr. P. Piras forhelpful comments and discussion on how to analyze the datapresented in the manuscript. This work was supported by anAustralian Research Council (ARC) Discovery grant (DP140102659)to S.W.

Supplementary Online Material

Supplementary online material related to this article can befound at https://doi.org/10.1016/j.jhevol.2018.02.007.

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