Journal of Human Evolution 64 (2013) 300e310

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Understanding the comparative catarrhine context of human pelvic form: A 3D geometric morphometric analysis Stephen J. Lycett*, Noreen von Cramon-Taubadel Department of Anthropology, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NR, UK

a r t i c l e i n f o

a b s t r a c t

Article history: Received 27 August 2012 Accepted 21 January 2013 Available online 26 February 2013

Comparative studies of catarrhine pelvic morphology in an evolutionary framework play an important role in paleoanthropology, especially since this is the context from which human bipedalism eventually arose. Given the abundance of potentially confounding evolutionary and mechanical factors influencing pelvic form, it is important to tease apart the effects of shape and size in the major component of the primate pelvis, the os coxae. However, os coxae form is difficult to assess via traditional morphometric methods. Here, we adopt a 3D geometric morphometric approach to landmark data. Our analyses included data from 30 extant catarrhine taxa. Data were transformed and registered using Procrustes analysis and analyzed via examination of principal components. Two analyses were performed: one excluding Homo sapiens, and a second including them. Results of the first analysis demonstrate that the total diversity of os coxae morphology is significantly greater in hominoids than it is in cercopithecoids. This appears to be driven by the greater effects of size diversity (i.e., allometric effects) in the case of the hominoids. This analysis also revealed a clear taxonomic/phylogenetic distinction between hominoids and cercopithecoids in terms of os coxae shape. The second analysis showed that Procrustes distances in shape space are significantly greater between extant Pan and Homo than they are between any two nonhuman catarrhine taxa. This analysis thus quantifies, on a comparative basis, the dramatic effect that the course of hominin evolution had upon the morphology of the human pelvis, within what is e even by catarrhine standards e a relatively short span of evolutionary time. Ó 2013 Elsevier Ltd. All rights reserved.

Keywords: Os coxae Allometry Pelvis Catarrhines Geometric morphometrics

Introduction Potential sources of size and shape variation in the primate pelvis Size and shape variation in catarrhine pelvic morphology has long been of interest in the study of human evolution (e.g., Waterman, 1929; Reynolds, 1931; Schultz, 1936; McHenry and Corruccini, 1978; Steudel, 1978; Berge, 1984; Tague, 1995; Ward, 2002). This is perhaps unsurprising given that the pelvic girdle is functionally related to numerous different biologically salient factors, including support of the body and internal visceral organs, the biomechanics of locomotion and, in the case of females, parturition. Ultimately, these factors relate to differences in the shape of the os coxae, the degree of isometric scaling (i.e., size), and the complex allometric scaling relationship between pelvic size and shape, all of which are at least potentially amenable to study in fossil taxa. However, the relationship between the size and shape of the pelvis,

* Corresponding author. E-mail address: [email protected] (S.J. Lycett). 0047-2484/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jhevol.2013.01.011

and the relative effects of phylogenetic history and various adaptive pressures in different taxa, is inevitably a complex one. Methodologically, this may be exacerbated by the relatively complex nature of pelvic morphology, which is not readily amenable to traditional morphometric measurement techniques (McHenry and Corruccini, 1978; Weaver and Hublin, 2009). A brief review of how primate pelvic form (i.e., size and shape) relates to issues of biomechanics, obstetric constraints, sexual dimorphism, and phylogenetic history serves to illustrate the complexity of the interaction between these non-mutually exclusive, and potentially confounding, factors. For instance, previous studies have revealed a complex pattern of allometry (size-related shape differences) in the primate pelvis, both between species and between sexes within species (e.g., Black, 1970; Leutenegger, 1973a, 1974, 1978; Mobb and Wood, 1977; Steudel, 1981a,b, 1984; Leutenegger and Cheverud, 1982; Leutenegger and Larson, 1985; Wood and Chamberlain, 1986; Tague, 1989, 1991, 1995, 2005; Ward, 1993; Correia et al., 2005; St. Clair, 2007; Kurki, 2011). In general, female primates have absolutely or relatively larger pelvic girdles than males, at least in the dimensions of the true pelvis relating directly to the passage of neonates during parturition (e.g., Schultz,

S.J. Lycett, N. von Cramon-Taubadel / Journal of Human Evolution 64 (2013) 300e310

1949; Steudel, 1981a; Tague, 1991, 1995, 2005; Arsuaga and Carretero, 1994; Correia et al., 2005; St. Clair, 2007). This is despite the fact that male primates tend to have body sizes equal to, or greater than, those of females (e.g., Wood, 1976; Leutenegger and Larson, 1985; Fleagle, 1999). This converse pattern in sexual size dimorphism is thought to be primarily related to the obstetrical constraints faced by female primates (e.g., Schultz, 1949; Leutenegger, 1974; Mobb and Wood, 1977; Leutenegger and Larson, 1985; Wood and Chamberlain, 1986; Rosenberg, 1992; Rosenberg and Trevathan, 1996). However, the extent of the obstetrical constraint is not equal across all primate taxa since larger bodied genera (such as Gorilla and Pongo) tend not to exhibit the close correspondence between pelvic inlet size and neonatal cranial size shown by smaller bodied primates such as monkeys and the lesser apes (Schultz, 1949; Leutenegger, 1973b, 1974, 1982; Tague, 1995). The exception to this pattern is humans, who despite being relatively large bodied, face the additional morphological constraints associated with being both bipedal and having neonates with larger encephalization quotients (e.g., Krogman, 1951; Rosenberg, 1992; Rosenberg and Trevathan, 1996; Travathan and Rosenberg, 2000; Weaver and Hublin, 2009; DeSilva, 2011). Leutenegger (1974) demonstrated that primate species facing greater obstetrical constraints (i.e., closer correspondence between newborn size and female pelvic size) also showed greater sexual dimorphism in some pelvic dimensions (see also Mobb and Wood, 1977; Wood and Chamberlain, 1986). This result was also supported by Ridley (1995) who reanalyzed the same data as Leutenegger (1974), but controlled for the effects of phylogeny and general body size. However, Tague (2005) found that primate species with greater overall sexual dimorphism in terms of body size (males larger than females) also tended to have greater pelvic size dimorphism (females larger than males), suggesting that the differences between male and female pelvic size are not entirely due to obstetric adaptations (see also Tague, 1991; Travathan and Rosenberg, 2000). The application of Rensch’s Rule (Rensch, 1950) predicts that as primate body size increases, the magnitude of sexual size dimorphism also increases. There is some empirical support for this prediction in haplorrhine taxa (e.g., Leutenegger, 1978; Leutenegger and Cheverud, 1982; Plavcan and Van Schaik, 1997; Smith and Cheverud, 2002) although it does not appear to be the case intraspecifically for the modern human pelvis (Kurki, 2011). Smith and Leigh (1998) also show that sexual dimorphism in primate neonate body mass is positively correlated with adult sexual dimorphism, which in turn is correlated with absolute body size (i.e., Rensch’s Rule [Abouheif and Fairbairn, 1997]). However, general increases in body size are also evolutionarily related to a variety of ecological factors such as relative terrestriality, feeding ecology, locomotor biomechanics, as well as phylogenetic constraints (Fleagle, 1999). Hence, other biomechanical factors not related to obstetrical constraints might also have an important (and potentially confounding) effect on pelvic allometry and sexual dimorphism. Differing locomotor repertoires and positional behaviors can also be expected to drive differences between species in pelvic morphology (Schultz, 1936; Zuckerman et al., 1973; Steudel, 1981b; Yirga, 1987; MacLatchy and Bossert, 1996; Ward, 2002). Indeed, Zuckerman et al. (1973) found interspecific differences in primate pelvic morphology consistent with differences in their locomotory behavior (see also Steudel, 1981b). In addition, the differences between the pelvic shape of humans and other apes due to the obligatory bipedal posture and locomotion of humans have long been noted (e.g., Straus, 1929; Waterman, 1929; Reynolds, 1931; Reynolds and Hooton, 1936; Schultz, 1936; Berge, 1984; Berge and Kazmierczak, 1986; Ward, 2002). However, certain pelvic differences thought to be related to the biomechanics of locomotion may

301

also be related to obstetrical adaptations. For example, Leutenegger (1974) suggested that increased lower iliac height may be advantageous in suspensory primates that spend a considerable proportion of their time in a relatively vertical position, as it reduces torque around the acetabulum. However, lower iliac height is also a proxy for pelvic inlet capacity (Leutenegger, 1974) and, therefore, this particular variable represents a potential confound between locomotory and obstetric adaptations. In particular, there is a mechanical trade-off between having a relatively longer lower ilium in females to increase the size of the pelvic inlet, and reducing the distance between the sacroiliac joint and the femoral head, which is energetically advantageous in leapers (Steudel, 1984), quadrupeds (Leutenegger, 1974) and bipeds (e.g., Leutenegger, 1974; Lovejoy, 1988). Underlying these various and potentially confounding adaptive changes across primates is the pattern of morphological variability due to the evolutionary processes of shared ancestry. It is well understood that failing to recognize the underlying phylogenetic pattern can generate spurious associations between comparative morphology and ecological or adaptive phenomena (e.g., Felsenstein, 1985; Harvey and Pagel, 1991; Ridley, 1995). Yet the extent to which variation in the primate pelvis might be related with phylogenetic history is currently poorly understood. While some studies have used phylogenetically controlled analyses to examine the relationship between sexual size dimorphism and body size (e.g., Cheverud et al., 1985; Plavcan and Van Schaik, 1997; Smith and Cheverud, 2002), comparative multivariate analyses of primate pelvic form (e.g., Steudel, 1981b) have found only limited separation between hominoids and cercopithecoids, with the smaller bodied apes appearing more similar to colobines. However, Young’s (2003) general analysis of the primate postcranium found that all hominoids were distinct from other catarrhines, and recovered the correct phylogenetic relationships between Gorilla, Pan, Pongo, and Hylobates. The challenge of quantifying shape and separating size in the catarrhine pelvis Given the abundance of potentially confounding evolutionary and mechanical factors influencing patterns of primate pelvic shape, size and allometry, it is important to separate the effects of shape and size. Thus far, studies have varied considerably in the methodological approaches taken to scale (i.e., size-adjust) raw pelvic dimensions. Some studies (e.g., Mobb and Wood, 1977; Wood and Chamberlain, 1986; Tague, 1995, 2005; Kurki, 2011) have examined the relationship between the dimensions of the pelvis and other proxies for body size, such as femoral head and shaft dimensions (e.g., Ruff et al., 1991; Ruff, 2003). Earlier studies (e.g., Mobb and Wood, 1977) also used the positive relationship between ischial size and overall body size (Washburn, 1948; Leutenegger, 1970) to scale the length of the pubis and thus create the sexually diagnostic ischium-pubis index. Steudel (1978, 1981a,b) sizecorrected raw pelvic data using two approaches: division of individual variables by the arithmetic mean of selected pelvic variables (Steudel, 1981a), and by employing the residuals from a regression of pelvic dimensions on overall size (Steudel, 1978, 1981b). However, regression-based size-adjustment has been shown to be problematic (Aiello, 1992; Falsetti et al., 1993; Jungers et al., 1995). Moreover, on theoretical and empirical grounds a geometric method of size-adjustment, such as division by the geometric mean of all variables is preferable, as it adjusts for isometric scaling yet preserves shape information (Jungers et al., 1995). Multivariate, landmark-based geometric morphometric methods allow for the precise quantification and separation of (isometric) size and shape, such that the geometric properties of

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complex homologous structures can be compared directly (Bookstein, 1991; Rohlf and Marcus, 1993; Dryden and Mardia, 1998; O’Higgins, 2000; Adams et al., 2004; Baab et al., 2012). Such methods are perhaps particularly appropriate in the case of the pelvis given that linear distances may potentially fail to capture key aspects of shape variation. Indeed, as early as the 1970s, McHenry and Corruccini (1978) pointed out that the complex shape of the os coxae is difficult to capture using conventional linear measurements and provided the first analysis of three-dimensional Cartesian coordinates taken on the pelvis of a sample of hominoids and fossil hominins. Moreover, their data were adjusted for isometric scaling in such a way that the shape of the os coxae could be compared directly (McHenry and Corruccini, 1978). Unfortunately their comparative sample did not extend beyond the hominoids, so the present study represents a broader comparative study of catarrhine pelvic shape and size.

Table 1 Anatomical definitions of pelvic landmarks illustrated in Fig. 1. Landmark 1 2 3 4 5 6

Iliac crest medial Iliac crest superior Iliac crest lateral Auricular superior Auricular inferior Sciatic notch

7 8

Ischial spine Pubic symphysis superior Pubic symphysis inferior Obturator foramen anterior Obturator foramen superior Obturator foramen posterior Ischial tuberosity anterior

9 10 11 12

Aims and objectives 13

Recently, Fleagle et al. (2010) noted that broad analyses of morphological diversity within the primate order are relatively rare, and that use of modern morphometric methods can lead to novel insights in this regard, even for the comparatively wellstudied cranium. Here, using a geometric morphometric (GM) approach to study pelvic (os coxae) variation, we focus on the catarrhines, given their phylogenetic and functional importance for understanding the emergence of human bipedality (e.g., Schultz, 1936; MacLatchy, 1996; Ward, 2002; Lovejoy et al., 2009; Weaver and Hublin, 2009). While the human pelvis has been influenced by several distinct evolutionary factors (e.g., obstetrics, climate, etc.), the fundamental shift toward obligatory bipedalism has been a profound influence on subsequent changes in human pelvic form (Straus, 1929; Waterman, 1929; Reynolds, 1931; Reynolds and Hooton, 1936; Schultz, 1936; Berge, 1984; Berge and Kazmierczak, 1986; Ward, 2002). As Schultz (1936: 425) put it “[c]hiefly due to the special mechanical requirements connected with erect posture the pelvis of man has acquired a general appearance which differs very strikingly from that of the pelves of the other higher primates”. Given the foregoing, the specific discrete aims of the current study are to: (1) quantify the multivariate pattern of isometricallyscaled pelvic (os coxae) shape variation in extant non-human catarrhines; (2) explore the allometric relationship between shape and size in the os coxae of non-human catarrhines, both intrasexually and with the sexes combined; and (3) to quantify the ultimate effect of hominin evolution on the shape of the os coxae of Homo sapiens within the comparative framework of general catarrhine diversity. Materials and methods Materials Materials comprised configurations of 20 homologous landmarks (Table 1, Fig. 1) digitized on the os coxae of specimens representing males and females of 30 extant catarrhine taxa (Table 2), including 13 cercopithecine species, seven colobine species, and six genera of the hominoids. In order to maximize the numbers of taxa included, only two male and two female specimens for each taxon were employed in the current analysis (after Fleagle et al., 2010). However, due to the lack of sufficient male specimens in the case of Mandrillus sphinx, the sample comprised two females and only one male, yielding a total sample of 119 individual specimens. All specimens used were wild shot, with the exception of the Mandrillus sample, which consisted of zoo specimens. Only anatomically complete and adult os coxae were measured. Adult specimens

14 Ischial tuberosity posterior 15 Ischium posterior

Definitionsa The most medial, posterior point on the iliac crest The most superior point on the iliac crest The most lateral, anterior point on the iliac crest The most superior point on the auricular surface The most inferior point on the auricular surface The point tangent to the maximum invagination of the sciatic notch The apex of the ischial spine The most superior, anterior point on the pubic symphysis The most inferior, anterior point on the pubic symphysis The most anterior point on the internal edge of the obturator foramen The most superior point on the internal edge of the obturator foramen The most posterior point on the internal edge of the obturator foramen The most inferior extent of the straight line between the center of the acetabulum and the maximum distance to the ischial tuberosity The most posterior point of the ischial tuberosity

The point of greatest invagination at the posterior of the ischium, lateral to the ischial spine 16 Acetabulum superior The point of intersection of the acetabular margin and the anterior margin of the illium 17 Acetabulum inferior The point on the inferior margin of the acetabulum, which is the maximum distance from acetabulum superior 18 Acetabulum anterior The most anterior point on the margin of the acetabulum, perpendicular to the axis connecting acetabulum superior and inferior 19 Acetabulum posterior The most posterior point on the margin of the acetabulum, perpendicular to the axis connecting acetabulum superior and inferior 20 Acetabulum center The deepest point at the center of the acetabulum a Orientation refers to the morphological orientation used during measurement, as illustrated in Fig. 1.

were identified via examination of all post-cranial elements available. Left os coxae were chosen when both were available, with the right side being measured only in the case of missing, broken or obviously pathological left os coxae. All landmarks were digitized by a single observer (SJL) using a Microscribe 3DXÔ (eMicroscribe) with the bone held in the common orientation shown in Fig. 1. Table 1 details the anatomical definitions of each landmark captured using the orientations shown in Fig. 1 as a guide. Intraobserver digitizing error was tested following the method described by von Cramon-Taubadel et al. (2007). All landmarks were deemed repeatable as they had a measurement error rate of <1 mm. Methods Two main geometric morphometric analyses were performed, first excluding humans from the analysis and thereafter including them. In each case, the original landmark configurations were scaled, rotated and translated using Generalized Procrustes Analysis (GPA) (Gower, 1975; Chapman, 1990), and the resultant Procrustes variables (Slice, 2001) were subjected to tangent space projection (Dryden and Mardia, 1998; Rohlf, 1999; Slice, 2001) and principal components analysis (PCA) in Morphologika 2.5 (O’Higgins and Jones, 1998, 2006). Shape variability was quantified separately for the hominoids and the cercopithecoids (intra- and inter-sexually) by averaging the between-specimens Procrustes

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Table 2 Catarrhine taxa included in the analyses. Abbreviations

Museum collections

Hominoids Gorilla gorilla gorilla Gorilla beringei graueri Pan troglodytes troglodytes Pan troglodytes schweinfurthii Pan paniscus Pongo pygmaeus Pongo abelii Hylobates lar Symphalangus syndactylus Homo sapiens

GorGG GorBG PanTT PanTS PanP PongoP PongoA HyloL SymS HomoS

PC RMCA PC RMCA RMCA BSC, MCZ BSC, MCZ MCZ BSC, SNMNH AMNH

Cercopithecinae Cercopithecus nictitans Cercopithecus mitis Cercopithecus ascanius Cercopithecus cephus Chlorocebus aethiops Erythrocebus patas Papio anubis Papio hamadryas Macaca mulatta Theropithecus gelada Cercocebus agilis Lophocebus albigena Mandrillus sphinx

CerN CerM CerA CerC ChloroA ErythroP PapioA PapioH MacacaM TherG CercoA LophoA MandS

PC SNMNH RMCA PC SNMNH RMCA SNMNH BSC SNMNH SNMNH RMCA RMCA, AMNH RMCA

Colobinae Colobus guereza Nasalis larvatus Piliocolobus faoi Trachypithecus cristatus Trachypithecus auratus Presbytis chryomelas Presbytis frontata

ColobusG NasalisL PiliocF TrachyC TrachyAur PresC PresF

SNMNH, AMNH BSC, MCZ RMCA BSC BSC BSC BSC

Abbreviations are used in Table 6 and Fig. 5. AMNH ¼ American Museum of Natural History (New York), PC ¼ Powell-Cotton Collection (Kent), MCZ ¼ Museum of Comparative Zoology (Harvard), RMCA ¼ Royal Museum of Central Africa (Tervuren), SNMNH ¼ Smithsonian National Museum of Natural History (Washington, D.C.), BSC ¼ Bavarian State Collection for Anthropology and Paleoanatomy (Munich). Taxonomic names according to Wilson and Reeder (2005).

Figure 1. Anatomical locations of the 20 pelvic landmarks captured for each specimen as illustrated on a human (left) and chimpanzee (right) os coxae model. Given that standard anatomical orientations (e.g., superior, inferior, etc.) differ between humans and other non-human primates due to positional behavior, the orientation terms employed in the list of landmark definitions (Table 1) refer to analytical orientations as shown in this figure. Here superior and inferior are used instead of ‘cranial’ and ‘caudal’ respectively, and anterior and posterior instead of ‘ventral’ and ‘dorsal’, respectively.

distances (see also Gunz et al., 2009) based on a single analysis of all (non-human) specimens. Average differences in Procrustes distances among hominoids and cercopithecoids were tested for significance via Student’s t-tests (a ¼ 0.01). Variation was visualized as wireframe diagrams (O’Higgins and Jones, 2006) capturing the main trends in multivariate shape change along individual principal components (PCs). Allometric relationships (i.e., shape changes associated with isometric scaling) were examined by performing multivariate regressions of all PC scores against specimen log centroid size (e.g., Mitteroecker et al., 2004) in Morphologika 2.5. Centroid size is defined as the square root of the sum of the squared Euclidean distances between individual landmarks in a configuration and the centroid of that configuration (Bookstein, 1991; Dryden and Mardia, 1998; Niewoehner, 2005). Thus, the GPA procedure effectively isometrically scales each

os coxae configuration to the same unit centroid size. All allometric analyses were repeated separately for the hominoid taxa, for the cercopithecoid taxa, as well as sex-specific analyses within the hominoids and the cercopithecoids. In the case of the mixed-sex analysis where humans were included, average Procrustes distances between all pairs of taxa in multivariate shape space were calculated in Morphologika 2.5 (O’Higgins and Jones, 2006). These distances quantify the morphological distance between humans and non-human primates in terms of os coxae morphology, relative to the average morphological diversity amongst the non-human primate taxa. Alongside the visualization of wireframe diagrams describing the major axes of shape variation between all taxa (PC1 and PC2), additional wireframes depicting the average os coxae shape of humans, the great apes, the small-bodied apes (hylobatids), the colobines and the cercopithecines were also created, in order to facilitate a direct comparison among the major taxonomic groupings. The relationship between humans and other primate taxa were also visualized as a neighbor-joining (Saitou and Nei, 1987) phenogram based on the matrix of average pairwise taxon Procrustes distances (i.e., total shape variation derived from all principal component scores). The neighbor-joining analysis was conducted using Phylip 3.66 (J. Felsenstein; evolution.genetics.washington.edu) and the phenogram was drawn using TreeView 1.6.6 (Rod D.M. Page; taxonomy.zoology. gla.ac.uk).

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Results Principal components analysis excluding humans Fig. 2 illustrates the main shape changes associated with the first two principal components (PCs), accounting for 59.9% of the total shape variation. Hominoids and cercopithecoids are well separated on PC1 (explaining 49.8% of the total variation), while the great apes are separated from the lesser apes on PC2 (10.1% variation). Taxonomically informative separations are less clear within the cercopithecoids, although colobines and cercopithecines are somewhat distinguished on both PC1 and PC2 (Fig. 2). Taking the morphological orientations depicted in Fig. 1 as a guide, wireframe diagrams illustrate the major shape changes in the landmark configuration captured by PC1 and PC2. Hominoids have relatively broader iliac blades, larger acetabula, more laterally flared ilia, and shorter more inferiorly projecting pubic regions. Cercopithecoids have relatively narrow, elongated iliac blades, relatively smaller acetabula, more superiorly projecting ischia (corresponding to more pronounced ischial callosities), and longer more superiorly projecting pubic bones. PC2 primarily captures shape differences between the great and lesser apes. Compared with great apes, lesser apes are characterized by more medially orientated and anterior-posteriorly shortened pubis and ischium, relative to the ilium and the acetabulum, as well as a relatively narrower (mediolaterally) iliac blade. Visual inspection of the PCA plot (Fig. 2) suggests that hominoids are more variable in the shape of their os coxae relative to the Old World monkeys. Indeed, on the basis of average between-

specimen Procrustes distances (Table 3) hominoids were statistically more variable than cercopithecoids in overall shape for the mixed-sex analysis (one-tailed, t ¼ 4.14, df ¼ 113, p < 0.0001), maleonly analysis (one-tailed, t ¼ 2.55, df ¼ 55, p ¼ 0.007) and femaleonly analysis (one-tailed, t ¼ 4.17, df ¼ 56, p < 0.0001). Hominoids were also found to be statistically more variable in terms of the centroid size of their os coxae (Table 4) compared with the cercopithecoids (F-test, p < 0.0001) as might be expected based on their greater variation in overall body mass (e.g., Fleagle, 1999). Allometric regressions In the case of the non-human catarrhine analysis (Fig. 2), a multivariate regression of all 53 PC scores on log centroid size found a significant allometric relationship (p < 0.001) with 39.22% of total shape variation explained by size. However, given the differences in overall os coxae size between hominoids and cercopithecoids (Table 4), this allometric relationship is likely to be confounded by the taxonomic separation between hominoid and cercopithecoid os coxae shape, as shown on PC1. Only two individual principal component scores were found to be significantly related with log centroid size (PC1: R2 ¼ 0.773, p < 0.001 and PC2: R2 ¼ 0.051, p ¼ 0.015). The relatively strong relationship between PC1 and size can be understood based on the major shape separation between the (relatively small) cercopithecoids versus the (relatively large) hominoids. The weak, although statistically significant, relationship between PC2 and centroid size suggests the possibility of allometric relationships within the hominoids and/or cercopithecoids that could only be teased apart via separate

Figure 2. Plot of the first two principal components (PC) explaining 49.8% and 10.1% of the total variation, respectively, following a PCA of all catarrhines, excluding humans. Hominoid taxa (dark and filled symbols) are clearly separated from cercopithecoids taxa (light and open symbols) on the first PC, while the lesser apes (triangles) are separated from the great apes on PC2. Wireframe diagrams are orientated according to those shown in Fig. 1 and depict the shape configurations expressed at the extreme ends of PC1 and PC2.

S.J. Lycett, N. von Cramon-Taubadel / Journal of Human Evolution 64 (2013) 300e310 Table 3 Average shape variation (average between-specimen Procrustes distances, standard deviations in parentheses) within hominoids and cercopithecoids.

Males and females Males Females

Hominoids

Cercopithecoids

0.1618 (0.0413) 0.1599 (0.0389) 0.1654 (0.0431)

0.1347 (0.0278) 0.1364 (0.0290) 0.1275 (0.0258)

Table 5 Multivariate regressions of shape variables (all principal component (PC) scores) on log centroid size.

Hominoids Multivariate R2 Cercopithecoids

analyses of each group of primates. Therefore, further allometric analyses were conducted on the hominoids and cercopithecoids separately, using both mixed-sex and sex-specific analyses. Hominoids In the case of the hominoid analyses, a significant multivariate regression of all 35 PC scores (shape) on size was found, with 33.0% of total shape variation explained by size (Table 5). Male hominoids also showed strong allometric patterns, with 38.0% of overall shape variation (17 PCS) explained by centroid size. Female hominoids, however, did not show statistically significant allometric patterns (p ¼ 0.246) although the ratio of shape variation (17 PCs) explained by size was relatively high (32.2%). Only PC1, explaining the majority of overall shape variability in each case, was significantly and strongly (R2 values of 0.680e0.913) related to overall size (Table 5). Cercopithecoids The pattern of results in the cercopithecoids differed substantially from those obtained for the hominoids (Table 5). Overall, much less of the total shape variation (53 PCs) was explained by centroid size (10.0%, p < 0.001 for the mixed-sex analysis). As in the hominoids, male cercopithecoids showed significant (but weak) allometric patterns (12.3%, p ¼ 0.006), while females showed a relatively weak non-significant multivariate regression of shape on size (12.3%, p ¼ 0.419). In the case of the cercopithecoids, there were several shape variables (PC scores) significantly correlated with centroid size in all cases (Table 5). However, the overall strength of these regressions was relatively weak in all cases with R2 values ranging from 0.105 to 0.259 for the mixed-sex analysis, 0.123e0.248 for the male-only analysis, and 0.135e0.245 for the female-only analysis. Therefore, cercopithecoids do not show overall strong allometric patterns between overall os coxae shape and centroid size. PCA including humans and comparison of Procrustes differences Fig. 3 shows the pattern of os coxae shape variability for the entire catarrhine sample for the first two principal components, explaining 62.4% of the total variation. The major axis of variation (PC1), explaining 44.8% of the total shape variation, separates the hominoids (including humans) from the cercopithecoids, while humans are noticeably separated from all other primate taxa on PC2 (17.6% of total variation). Therefore, humans are included among the hominoid group on the main axis of variation, despite being highly divergent on the second axis. As in the previous PCA plot (Fig. 2), the main axis of variation is characterized by the relatively more flared iliac blade, larger acetabula and inferiorly projecting pubis of the hominoids, relative to the pronounced ischium and superiorly orientated pubis of the Old World monkeys. Taking the orientation terms provided in Fig. 1 as a guide, human os coxae

Table 4 Average size variation (coefficients of variation) within hominoids and cercopithecoids based on os coxae centroid size.

Hominoids Cercopithecoids

Average centroid size

Standard deviation

Co-efficient of variation

349.07 188.74

100.09 31.79

28.67 16.84

305

Multivariate R2

Male and female

Male

Female

PC1: 0.797 (<0.001) 0.330 (0.090)* PC1: 0.259 (<0.001) PC2: 0.090 (0.007) PC4: 0.105 (0.004) PC5: 0.049 (0.049) PC7: 0.137 (0.001) 0.100 (<0.001)**

PC1: 0.913 (<0.001) 0.380 (0.046)** PC1: 0.253 (0.010) PC2: 0.133 (0.023) PC3: 0.176 (0.008) PC6: 0.110 (0.039)

PC1: 0.680 (<0.001) 0.322 (0.246) PC1: 0.245 (<0.001) PC2: 0.135 (0.020) PC6: 0.223 (<0.001)

0.123 (0.006)**

0.103 (0.419)

*Significant at the a ¼ 0.10 level, **significant at the a ¼ 0.05 level. ‘Multivariate R2’ ¼ percentage of total shape variation explained by size (p-values in parentheses). Individual regression statistics (R2 values with p-values in parentheses) are also given for individual PC scores significantly (a-level ¼ 0.05) explained by size in each case.

shape is characterized (on PC2) by a broad, shorter and anteriorly flared iliac blade, relatively larger and deeper acetabula and an elongated pubic region. The sciatic notch is deeper and more defined and the ischium is more vertically orientated relative to the main axis of orientation (see Fig. 1). Fig. 4 shows two views of the average wireframe shape for humans, the great apes, the smallbodied (hylobatid) apes, the cercopithecines and the colobines. Here, rather than depicting shape changes along each principal component, average shape differences between major taxonomic groupings are illustrated. Relatively little difference can be observed between the average colobine and the average cercopithecine pelvis. However, these wireframe averages do not speak to variability within each of these taxonomic groupings, which may reflect shape differences related to locomotor behavior, overall feeding ecology and sexual dimorphism. Relative to the Old World monkeys, apes have relatively broad iliac blades, inferiorly projecting and shorter pubic bones, and more inferiorly (caudally) orientated ischia. Great apes also have relatively large acetabula and broader ilia compared with lesser apes and Old World monkeys. Humans have markedly broad and anteriorly flared ilia, with an inferiorly (caudally) and medially rotated auricular surface. The iliac blade is also shorter inferiorly-superiorly relative to the pubis and ischium, and the acetabulum is relatively much larger than non-human primates. The entire os coxae is also anteriorlyposteriorly wider in humans with an elongated anteriorly projecting pubis (see Fig. 1 for relative orientation terms). Table 6 presents the average between-taxon Procrustes distances for all catarrhine taxa studied. The average pairwise Procrustes distances between H. sapiens and all other primate taxa (highlighted in bold) are greater than any other pair of non-human taxa examined. Ranking the pairwise distances from largest to smallest found that all pairwise distances involving humans were ranked as largest. Even the morphologically divergent Gorilla species (see Fig. 2) were not more different from any monkey taxon than humans were to all other taxa. In terms of hominoid variability, humans were most different from Hylobates, followed by Symphalangus, Pan, Pongo, and Gorilla. Humans were more different from their molecular sister-taxon (Pan) than any pair of non-human primate taxa are from each other. The three most similar pairs of taxa were all colobine taxa; Nasalis/Piliocolobus, the two species of Trachypithecus and the two Presbytis species. The patterns quantified by the pairwise matrix of between-taxon Procrustes distances

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Figure 3. Plot of the first two principal components (PC) explaining 44.8% and 17.6% of the total variation, respectively, following a PCA of all catarrhines, including humans. Hominoid taxa (dark and filled symbols) are clearly separated from cercopithecoids taxa (light and open symbols) on the first PC, while humans (filled stars) are clearly separated from all non-human primates on PC2. Wireframe diagrams are orientated according to those shown in Fig. 1 and depict the shape configurations expressed at the extreme ends of PC1 and PC2.

can also be seen in Fig. 5 in the form of an unrooted neighborjoining phenogram. The taxonomic split observed in the principal component plot (Fig. 3) is also obvious here (based on total shape variability) with hominoids forming a group to the exclusion of the

cercopithecoid taxa. Hylobates and Symphalangus form a branch intermediate to the great ape and the Old World monkey taxa, as would be expected based on molecular data (e.g., Perelman et al., 2011). As was the case for the PCA plot, there is not a clear taxonomic pattern discernible between the cercopithecines and the colobines, although sister taxa do group together (e.g., Presbytis, Trachypithecus). Humans are grouped amongst the great apes, sharing the strongest affinities with the two Gorilla taxa, although as suggested by PC2 in Fig. 3, their relatively long branch lengths for total os coxae shape are suggestive of the strong divergence of human os coxae shape relative to non-human primate taxa. Discussion

Figure 4. Wireframes depicting the average shapes of humans (A), great apes (B), small-bodied apes (hylobatids) (C), cercopithecines (D) and colobines (E) in frontal (upper panel) and lateral (lower panel) view.

Developing a better understanding of catarrhine pelvic diversity is now all the more important given that the available sample of fossil hominin pelves has increased substantially in recent years (e.g., Simpson et al., 2008; Lovejoy et al., 2009; Bonmatí et al., 2010; Kibii et al., 2011). Hence, the goals of this study were to disentangle the relative patterns of catarrhine os coxae shape and size variability, both inter-sexually and inter-taxonomically. Quantification of the multivariate pattern of isometrically-scaled pelvic shape variation in the catarrhines (with humans excluded), revealed a clear distinction between hominoids and cercopithecoids in terms of os coxae shape (PC1, Fig. 2). Some of these shape differences, such as

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307

Table 6 Average Procrustes distances between all pairs of catarrhine taxa.

GorBG PanTT PanTS PanP PongoP PongoA HyloL SymS HomoS CerN CerM CerA CerC ChloroA ErythroP PapioA PapioH MacacaM TherG CercoA LophoA MandS ColobusG NasalisL PiliocF TrachyC TrachyAur PresC PresF

GorGG

GorBG

PanTT

PanTS

PanP

PongoP

PongoA

HyloL

SymS

HomoS

0.14 0.18 0.19 0.21 0.19 0.18 0.26 0.24 0.37 0.34 0.33 0.32 0.35 0.33 0.30 0.26 0.30 0.32 0.29 0.31 0.31 0.30 0.30 0.27 0.28 0.31 0.31 0.31 0.33

0.16 0.14 0.16 0.15 0.15 0.23 0.21 0.35 0.32 0.29 0.29 0.33 0.29 0.27 0.22 0.27 0.28 0.25 0.28 0.28 0.27 0.27 0.24 0.25 0.28 0.28 0.27 0.29

0.12 0.15 0.16 0.16 0.20 0.18 0.41 0.30 0.27 0.26 0.30 0.26 0.24 0.22 0.27 0.26 0.23 0.26 0.25 0.26 0.25 0.23 0.24 0.25 0.26 0.26 0.28

0.11 0.13 0.15 0.17 0.16 0.39 0.27 0.24 0.24 0.27 0.23 0.21 0.17 0.22 0.22 0.20 0.23 0.22 0.23 0.21 0.19 0.20 0.22 0.23 0.22 0.24

0.15 0.15 0.15 0.17 0.40 0.23 0.20 0.20 0.23 0.19 0.18 0.15 0.19 0.18 0.17 0.19 0.18 0.19 0.18 0.16 0.16 0.18 0.18 0.19 0.20

0.13 0.18 0.17 0.37 0.29 0.26 0.26 0.29 0.25 0.23 0.19 0.24 0.24 0.22 0.25 0.24 0.24 0.23 0.20 0.22 0.24 0.25 0.25 0.26

0.18 0.18 0.38 0.27 0.25 0.24 0.28 0.25 0.23 0.19 0.24 0.24 0.21 0.24 0.23 0.24 0.23 0.20 0.22 0.23 0.24 0.24 0.25

0.12 0.44 0.23 0.19 0.18 0.24 0.18 0.17 0.16 0.20 0.19 0.17 0.17 0.16 0.19 0.18 0.16 0.17 0.18 0.20 0.21 0.21

0.43 0.28 0.24 0.23 0.28 0.23 0.21 0.19 0.24 0.24 0.21 0.22 0.22 0.24 0.22 0.20 0.21 0.23 0.24 0.25 0.26

0.46 0.46 0.45 0.48 0.44 0.44 0.38 0.43 0.45 0.41 0.44 0.45 0.43 0.43 0.41 0.43 0.44 0.45 0.43 0.45

CerN CerM CerA CerC ChloroA ErythroP PapioA PapioH MacacaM TherG CercoA LophoA MandS ColobusG NasalisL PiliocF TrachyC TrachyA PresC CerM CerA CerC ChloroA ErythroP PapioA PapioH MacacaM TherG CercoA LophoA MandS ColobusG NasalisL PiliocF TrachyC TrachyAur PresC PresF

0.13 0.14 0.11 0.15 0.17 0.18 0.14 0.14 0.16 0.14 0.16 0.16 0.15 0.20 0.16 0.14 0.14 0.15 0.12

0.12 0.14 0.12 0.14 0.15 0.14 0.12 0.14 0.12 0.13 0.14 0.12 0.16 0.13 0.13 0.13 0.14 0.13

0.14 0.12 0.14 0.15 0.15 0.13 0.14 0.12 0.12 0.15 0.13 0.16 0.14 0.14 0.14 0.15 0.14

0.15 0.17 0.19 0.14 0.15 0.17 0.14 0.16 0.16 0.16 0.21 0.17 0.14 0.14 0.15 0.12

0.12 0.14 0.14 0.11 0.12 0.11 0.12 0.14 0.12 0.15 0.12 0.14 0.14 0.13 0.13

0.13 0.15 0.13 0.13 0.12 0.13 0.14 0.13 0.16 0.13 0.16 0.16 0.15 0.15

0.13 0.14 0.12 0.14 0.13 0.13 0.12 0.12 0.11 0.15 0.15 0.15 0.15

0.12 0.12 0.13 0.14 0.14 0.12 0.16 0.12 0.12 0.11 0.13 0.11

0.12 0.12 0.12 0.14 0.11 0.15 0.11 0.13 0.12 0.14 0.13

0.12 0.13 0.14 0.12 0.13 0.12 0.13 0.13 0.13 0.14

0.11 0.13 0.11 0.15 0.12 0.12 0.13 0.13 0.13

0.13 0.11 0.14 0.12 0.14 0.13 0.15 0.14

0.12 0.15 0.12 0.14 0.13 0.15 0.14

0.12 0.12 0.12 0.12 0.13 0.14

0.01 0.15 0.15 0.15 0.17

0.12 0.11 0.13 0.12

0.10 0.12 0.11

0.12 0.11

0.10

Distances between Homo sapiens and all other taxa in bold.

the relatively larger acetabulum in hominoids, are consistent with previous studies of femoral head and acetabulum size and shape (e.g., MacLatchy and Bossert, 1996; Ruff, 2002). It has also been noted previously that hominoids have relatively more flaring iliac blades when compared against monkeys (Straus, 1929; Waterman, 1929; Ward, 1993, 2002). However, when considering the multivariate shape of the entire os coxae, the clear taxonomic difference found between hominoids and cercopithecoids contrasts with previous studies (e.g., Steudel, 1981b), which found greater overlap in morphology between the small-bodied hominoids (gibbons and siamangs) and monkey species. Hence, despite the numerous and complex interacting factors potentially affecting pelvic form, our results suggest that there is a substantial taxonomic/phylogenetic signal in the overall shape of the primate os coxae, which needs to be explicitly considered in any future analyses of primate pelvic adaptation (see also Cheverud et al., 1985; Ridley, 1995). This supports previous suggestions (e.g., Young, 2003, 2008) that the

primate postcranium may possess a stronger phylogenetic signal than is often assumed given its relationship with various functional activities. Our results also demonstrate a clear distinction between hominoids and cercopithecoids in the extent of shape variability and overall variation in os coxae size (Tables 3 and 4). The substantial body size variation of hominoids, relative to other groups of extant primates, has been noted previously (e.g., Fleagle, 1999) and here we demonstrate that this variability in body size is mirrored in a statistically greater level of diversity in os coxae shape. In the case of hominoids, there is a strong allometric relationship between overall os coxae shape and size (Table 5) with approximately 40% of overall shape explained by size. Also, in contrast with the cercopithecoids, the shape variable (PC1) explaining the major differences between the great and the lesser apes, was also significantly and strongly related to size, suggesting that a large proportion of hominoid pelvic shape variation is driven by variation in body size.

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Figure 5. Unrooted neighbor-joining phenogram of all catarrhine taxa based on the matrix of pairwise Procrustes distances provided in Table 6.

While other factors that differ between taxa, such as locomotor repertories, positional behaviors and levels of sexual dimorphism, may play a role in determining overall pelvic morphology, the results presented here highlight the need to control for overall scaling effects when investigating these phenomena within hominoids. In the case of the cercopithecoids, however, a very different relationship between pelvic size and shape was revealed, with relatively little overall shape variation (w10%) being explained by centroid size. It has been noted previously that cercopithecoids are, in general, considered to be morphologically uniform (e.g., Fleagle, 1999). This, as our results show, is also true of os coxae shape, which is significantly less variable than hominoid shape (Table 3) and also represents a greater degree of isometric scaling between small and larger-bodied cercopithecoid taxa (Table 5). Therefore, to summarize, hominoids show strong allometric relationships in the os coxae with shape variation being strongly associated with size, while cercopithecoids show weak allometric relationships both intra-taxonomically and intra-sexually. This suggests that future studies of catarrhine obstetric adaptation will need to investigate more clearly whether differences between males and females are related to shape or size dimorphism, because there is clearly a complex relationship between the two. Our final aim was to quantitatively explore the effect that the unique course of evolution within the hominin lineage ultimately

had upon human pelvic shape, relative to catarrhine diversity as a whole. Our results found that, despite the morphological differences between the human bipedal os coxae and the basic pelvic bauplan shared by non-human catarrhines, the human os coxae is still recognizably a hominoid os coxae distinct from the Old World monkeys (Figs. 3 and 5). The analysis of between-taxon Procrustes distances found that humans were most similar to the large bodied Gorilla and Pongo taxa, rather than their molecular sister-taxon e Pan. In a comparison of Homo, Pan and Gorilla, Marchal (2000) also found that human pelvic shape was more similar to Gorilla than to Pan. One possibility for this convergence in pelvic shape may be due to loading factors (i.e., upper body mass in the case of Gorilla and bipedal locomotion in the case of Homo). This speculation aside, the unique course of evolution within the hominin lineage, including selection for bipedalism, has resulted in a human os coxae that is more morphologically distinct from any catarrhine taxon than any two non-human catarrhine taxa are from each other, despite the long-term independent evolution of pelvic form within different groups of catarrhines. This level of morphological divergence is dramatic, both in the scale of shape differentiation, and in the short timeframe within which it took place. Indeed, taking recent estimates of molecular divergence as a guide (Perelman et al., 2011), our results show that there has been greater morphological change in the hominin pelvis in the w6.6 million years since the last

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common ancestor (LCA) of the Pan-Homo clade, than there has been in the pelvis of all other catarrhines during the w31.56 million years since their LCA. Recent studies have suggested low overall levels of morphological integration and high levels of evolvability in the primate pelvis (Grabowski et al., 2011; Lewton, 2012). Grabowski et al. (2011) found that humans possess statistically lower levels of integration and constraint compared with other great apes, and that changes in the magnitude of integration may have facilitated the profound shape changes that occurred in the transition from the ancestral to derived pelvic form seen in humans. Young et al. (2010) found a similar reduction in the level of integration between the hominoid fore- and hind-limbs, relative to other primates, which is indicative of ‘evolutionary experimentation’ in the postcranial bauplan of hominoids. Young et al. (2010) note that in contrast with the more flexible hominoid bauplan, strong integration in monkey taxa limits postcranial diversification to largely size-scaled variants. This is also supported by our allometric regression analyses, which suggest that most shape variation in the cercopithecoid os coxae is actually isometrically, rather than allometrically, scaled. Therefore, despite the large-scale reorganization of the human pelvis in response to a shift toward obligatory bipedalism, this can be seen as part of an ongoing diversification trend within hominoid postcranial evolution, rather than being fundamentally distinct. In this evolutionary context, therefore, the distinction lies between evolvability levels within the hominoids (including humans) compared with cercopithecoids, rather than between humans and other primates. Acknowledgments We thank David Begun, Phillip Gunz and two anonymous reviewers for constructive comments and suggestions that helped strengthen our manuscript. We wish to acknowledge the EU Synthesys initiative (BE-TAF-206) for funding received to undertake this project. We also thank the following museum curators for providing access to the collections in their care: Malcolm Harman (Powell-Cotton, Quex Park), Mike Schweissing (Bavarian State Collection for Anthropology and Paleoanatomy, Munich), Emmanuel Gilissen and Wim Wendelen (Royal Museum Central Africa, Tervuren), Eileen Westwig and Gisselle Garcia (American Museum of Natural History, New York), Linda Gordon (Smithsonian National Museum of Natural History), and Judy Chupasko (Harvard Museum of Comparative Zoology). References Abouheif, E., Fairbairn, D.J., 1997. A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am. Nat. 149, 540e562. Adams, D.C., Rohlf, F.J., Slice, D.E., 2004. Geometric morphometrics: ten years of progress following the ‘revolution’. Ital. J. Zool. 71, 5e16. Aiello, L.C., 1992. Allometry and the analysis of size and shape in human evolution. J. Hum. Evol. 22, 127e147. Arsuaga, J.L., Carretero, J.M., 1994. Multivariate analysis of the sexual dimorphism of the hip bone in a modern human population and in early hominids. Am. J. Phys. Anthropol. 93, 241e257. Baab, K.L., McNulty, K.P., Rohlf, F.J., 2012. The shape of human evolution: a geometric morphometrics perspective. Evol. Anthropol. 21, 151e165. Berge, C., 1984. Multivariate analysis of the pelvis for hominids and other extant primates: implications for the locomotion and systematics of the different species of australopithecines. J. Hum. Evol. 13, 555e562. Berge, C., Kazmierczak, J.B., 1986. Effects of size and locomotion adaptations on the hominid pelves: evaluation of the australopithecine bipedality with a new multivariate method. Folia Primatol. 46, 185e204. Black, E.S., 1970. Sexual dimorphism in the ischium and pubis of three species of South American monkeys. J. Mammal. 51, 794e796. Bonmatí, A., Gómez-Olivencia, A., Arsuaga, J.L., Carretero, J.M., Gracia, A., Martínez, I., Lorenzo, C., Bérmudez de Castro, J.M., Carbonell, E., 2010. Middle Pleistocene lower back and pelvis from an aged human individual from the Sima de los Huesos site. Spain. Proc. Natl. Acad. Sci. 107, 18386e18391.

309

Bookstein, F.L., 1991. Morphometric Tools for Landmark Data: Geometry and Biology. Cambridge University Press, Cambridge. Chapman, R.E., 1990. Conventional Procrustes approaches. In: Rohlf, F.J., Bookstein, F.L. (Eds.), Proceedings of the Michigan Morphometrics Workshop Special Publication No 2. University of Michigan Museum of Zoology, Ann Arbor, pp. 251e267. Cheverud, J., Dow, M., Leutenegger, W., 1985. The quantitative assessment of phylogenetic constraints in comparative analyses: sexual dimorphism in body weight among primates. Evolution 39, 1335e1351. Correia, H., Balseiro, S., De Areia, M., 2005. Sexual dimorphism in the human pelvis: testing a new hypothesis. Homo 56, 153e160. DeSilva, J.M., 2011. A shift toward birthing relatively large infants early in human evolution. Proc. Natl. Acad. Sci. 108, 1022e1027. Dryden, I.L., Mardia, K.V., 1998. Statistical Analysis of Shape. Wiley, Chicester. Falsetti, A.B., Jungers, W.L., Cole III, T.M., 1993. Morphometrics of the callitrichid forelimb: a case study in size and shape. Int. J. Primatol. 14, 551e572. Felsenstein, J., 1985. Phylogenies and the comparative method. Am. Nat. 125, 1e15. Fleagle, J.G., 1999. Primate Adaptation and Evolution, second ed. Academic Press, London. Fleagle, J.G., Gilbert, C.C., Baden, A.L., 2010. Primate cranial diversity. Am. J. Phys. Anthropol. 142, 565e578. Gower, J.C., 1975. Generalized Procrustes analysis. Psychometrika 40, 33e50. Grabowski, M.W., Polk, J.D., Roseman, C.C., 2011. Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism. Evolution 65, 1336e1356. Gunz, P., Bookstein, F.L., Mitteroeker, P., Stadlmayr, A., Seidler, H., Weber, G.W., 2009. Early modern human diversity suggests subdivided population structure and a complex out-of-Africa scenario. Proc. Natl. Acad. Sci. 106, 6094e6098. Harvey, P.H., Pagel, M.D., 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford. Jungers, W.L., Falsetti, A.B., Wall, C.E., 1995. Shape, relative size and sizeadjustments in morphometrics. Yearb. Phys. Anthropol. 38, 137e161. Kibii, J.M., Churchill, S.E., Schmid, P., Carlson, K.J., Reed, N.D., de Ruiter, D.J., Berger, L.R., 2011. A partial pelvis of Australopithecus sediba. Science 333, 1407e 1411. Krogman, W.M., 1951. The scars of human evolution. Sci. Am. 185, 54e57. Kurki, H.K., 2011. Pelvic dimorphism in relation to body size and body size dimorphism in humans. J. Hum. Evol. 61, 631e643. Leutenegger, W., 1970. Das Becken der rezenten Primaten. Morphol. Jahrb. 115, 1e101. Leutenegger, W., 1973a. Sexual dimorphism in the pelvis of African lorises. Am. J. Phys. Anthropol. 38, 251e254. Leutenegger, W., 1973b. Maternal-fetal weight relationships in primates. Folia Primatol. 20, 280e293. Leutenegger, W., 1974. Functional aspects of pelvic morphology in simian primates. J. Hum. Evol. 3, 207e222. Leutenegger, W., 1978. Scaling of sexual dimorphism in body size and breeding system in primates. Nature 272, 610e611. Leutenegger, W., 1982. Encephalization and obstetrics in primates with particular reference to human evolution. In: Armstrong, E., Falk, D. (Eds.), Primate Brain Evolution: Methods and Concepts. Plenum, New York, pp. 85e95. Leutenegger, W., Cheverud, J., 1982. Correlates of sexual dimorphism in primates: ecological and size variables. Int. J. Primatol. 3, 387e402. Leutenegger, W., Larson, S., 1985. Sexual dimorphism in the postcranial skeleton of New World primates. Folia Primatol. 44, 82e95. Lewton, K.L., 2012. Evolvability of the primate pelvic girdle. Evol. Biol. 39, 126e139. Lovejoy, C.O., 1988. Evolution of human walking. Sci. Am. 259, 82e89. Lovejoy, C.O., Suwa, G., Spurlock, L., Asfaw, B., White, T.D., 2009. The pelvis and femur of Ardipithecus ramidus: the emergence of upright walking. Science 326, 71e76. MacLatchy, L.M., 1996. Another look at the australopithecine hip. J. Hum. Evol. 31, 455e476. MacLatchy, L.M., Bossert, W.H., 1996. An analysis of the articular distribution of the femoral head and acetabulum in anthropoids, with implications for hip function in Miocene hominoids. J. Hum. Evol. 39, 159e183. Marchal, F., 2000. A new morphometric analysis of the hominid pelvic bone. J. Hum. Evol. 38, 347e365. McHenry, H.M., Corruccini, R.S., 1978. Analysis of the hominoid os coxa by Cartesian coordinates. Am. J. Phys. Anthropol. 48, 215e226. Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., Bookstein, F.L., 2004. Comparison of cranial ontogenetic trajectories among great apes and humans. J. Hum. Evol. 46, 679e698. Mobb, G.E., Wood, B.A., 1977. Allometry and sexual dimorphism in the primate innominate bone. Am. J. Anat. 150, 531e538. Niewoehner, W.A., 2005. A geometric morphometric analysis of late Pleistocene human metacarpal 1 base shape. In: Slice, D.E. (Ed.), Modern Morphometrics in Physical Anthropology. Kluwer, New York, pp. 285e298. O’Higgins, P., 2000. The study of morphological variation in the hominid fossil record: biology, landmarks and geometry. J. Anat. 197, 103e120. O’Higgins, P., Jones, N., 1998. Facial growth in Cercocebus torquatus: an application of three-dimensional geometric morphometric techniques to the study of morphological variation. J. Anat. 193, 251e272. O’Higgins, P., Jones, N., 2006. Tools for Statistical Shape Analysis. Hull-York Medical School. . Perelman, P., Johnson, W.E., Roos, C., Seuánez, H.N., Horvath, J.E., Moreira, M.A.M., Kessing, B., Pontius, J., Roelke, M., Rumpler, Y., Schneider, M.P.C., Silva, A.,

310

S.J. Lycett, N. von Cramon-Taubadel / Journal of Human Evolution 64 (2013) 300e310

O’Brien, S.J., Pecon-Slattery, J., 2011. A molecular phylogeny of living primates. Plos Genet. 7, e1001342. Plavcan, J.M., Van Schaik, C.P., 1997. Intrasexual competition and body weight dimorphism in anthropoid primates. Am. J. Phys. Anthropol. 103, 37e68. Rensch, B., 1950. Die Abhangigkeit der relativen Sexualdifferenz von der Korpergrosse. Bonner Zool. Beitr. 1, 58e69. Reynolds, E.D., 1931. The Evolution of the Human Pelvis in Relation to the Mechanics of the Erect Posture. In: Pap. Peabody Mus. Am. A, vol. XI, pp. 255e334. Reynolds, E.D., Hooton, E.A., 1936. Relation of the pelvis to the erect posture. Am. J. Phys. Anthropol. 21, 253e278. Ridley, M., 1995. Brief communication: pelvic sexual dimorphism and relative neonatal brain size really are related. Am. J. Phys. Anthropol. 97, 197e200. Rohlf, F.J., 1999. Shape statistics: Procrustes superimpositions and tangent spaces. J. Classif. 16, 197e223. Rohlf, F.J., Marcus, L.F., 1993. A revolution in morphometrics. Trends Ecol. Evol. 8, 129e132. Rosenberg, K., 1992. The evolution of modern human childbirth. Yearb. Phys. Anthropol. 35, 89e124. Rosenberg, K., Trevathan, W., 1996. Bipedalism and human birth: the obstetrical dilemma revisited. Evol. Anthropol. 4, 161e168. Ruff, C.B., 2002. Long bone articular and diaphyseal structure in Old World monkeys and apes. I: locomotor effects. Am. J. Phys. Anthropol. 119, 305e342. Ruff, C.B., 2003. Long bone articular and diaphyseal structure in Old World monkeys and apes. II: estimation of body mass. Am. J. Phys. Anthropol. 120, 16e37. Ruff, C.B., Scott, W.W., Liu, A.Y., 1991. Articular and diaphyseal remodeling of the proximal femur with changes in body mass in adults. Am. J. Phys. Anthropol. 86, 397e413. Saitou, N., Nei, M., 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406e425. Schultz, A.H., 1936. Characters common to higher primates and characters specific for man (continued). Q. Rev. Biol. 11, 425e455. Schultz, A.H., 1949. Sex differences in the pelves of primates. Am. J. Phys. Anthropol. 7, 401e424. Simpson, S.W., Quade, J., Levin, N.E., Butler, R., Dupont-Nivet, G., Everett, M., Semaw, S., 2008. A female Homo erectus pelvis from Gona, Ethiopia. Science 322, 1089e1092. Slice, D.E., 2001. Landmark coordinated aligned by Procrustes analysis do not lie in Kendall’s shape space. Syst. Biol. 50, 141e149. Smith, R.J., Cheverud, J., 2002. Scaling of sexual dimorphism in body mass: a phylogenetic analysis of Rensch’s rule. Int. J. Primatol. 23, 1095e1135. Smith, R.J., Leigh, S.R., 1998. Sexual dimorphism in primate neonatal body mass. J. Hum. Evol. 34, 173e201. Clair St., E.M., 2007. Sexual dimorphism in the pelvis of Microcebus. Int. J. Primatol. 28, 1109e1122. Steudel, K., 1978. A multivariate analysis of the pelvis of early hominids. J. Hum. Evol. 7, 583e595.

Steudel, K., 1981a. Sexual dimorphism and allometry in primate ossa coxa. Am. J. Phys. Anthropol. 55, 209e215. Steudel, K., 1981b. Functional aspects of primate pelvic structure: a multivariate approach. Am. J. Phys. Anthropol. 55, 399e410. Steudel, K., 1984. Patterns of allometry in the pelvis of higher primates. J. Hum. Evol. 13, 545e554. Straus, W.L., 1929. Studies on primate ilia. Am. J. Anat. 43, 403e460. Tague, R.G., 1989. Variation in pelvic size between males and females. Am. J. Phys. Anthropol. 80, 59e71. Tague, R.G., 1991. Commonalities in dimorphism and variability in the anthropoid pelvis, with implications for the fossil record. J. Hum. Evol. 21, 153e176. Tague, R.G., 1995. Variation in pelvic size between males and females in nonhuman anthropoids. Am. J. Phys. Anthropol. 97, 213e233. Tague, R.G., 2005. Big-bodied males help us recognize that females have big pelves. Am. J. Phys. Anthropol. 127, 392e405. Travathan, W.R., Rosenberg, K., 2000. The shoulders follow the head: postcranial constraints on human childbirth. J. Hum. Evol. 39, 583e585. von Cramon-Taubadel, N., Frazier, B.C., Lahr, M.M., 2007. The problem of assessing landmark error in geometric morphometrics: theory, methods and modifications. Am. J. Phys. Anthropol. 134, 24e35. Ward, C.V., 1993. Torso morphology and locomotion in Proconsul nyanzae. Am. J. Phys. Anthropol. 92, 291e328. Ward, C.V., 2002. Interpreting the posture and locomotion of Australopithecus afarensis? where do we stand? Yearb. Phys. Anthropol. 45, 185e215. Washburn, S.L., 1948. Sex differences in the pubic bone. Am. J. Phys. Anthropol. 6, 199e208. Waterman, H.C., 1929. Studies on the evolution of the pelvis of man and other primates. Bull. Am. Mus. Nat. Hist. 58, 585e642. Weaver, T.D., Hublin, J.-J., 2009. Neandertal birth canal shape and the evolution of human childbirth. Proc. Natl. Acad. Sci. 106, 8151e8156. Wilson, D.E., Reeder, D.M., 2005. Mammal Species of the World: a Taxonomic and Geographic Reference. John Hopkins University Press, Baltimore. Wood, B.A., 1976. The nature and basis of sexual dimorphism in the primate skeleton. J. Zool. 180, 15e34. Wood, B.A., Chamberlain, A.T., 1986. The primate pelvis: allometry or sexual dimorphism. J. Hum. Evol. 15, 257e263. Yirga, S., 1987. Interrelation between ischium, thigh extending muscles and locomotion in some primates. Primates 28, 79e86. Young, N.M., 2003. A reassessment of living hominoid postcranial variability: implications for ape evolution. J. Hum. Evol. 45, 441e464. Young, N.M., 2008. A comparison of the ontogeny of shape variation in the anthropoid scapula: functional and phylogenetic signal. Am. J. Phys. Anthropol. 136, 247e264. Young, N.M., Wagner, G.P., Hallgrimsson, B., 2010. Development and the evolvability of human limbs. Proc. Natl. Acad. Sci. 107, 3400e3405. Zuckerman, S., Ashton, E.H., Flinn, R.M., Oxnard, C.E., Spence, R.F., 1973. Some locomotor features of the pelvic girdle in primates. Symp. Zool. Soc. Lond. 33, 71e165.