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Journal of Human Evolution 63 (2012) 191e204

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Journal of Human Evolution

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

Geometric morphometric analysis of mandibular shape diversity in Pan

Chris Robinson

Department of Biology, Bronx Community College, City University of New York, 2155 University Avenue, Bronx, NY 10453, USA article info abstract

Article history: The aim of this research is to determine whether geometric morphometric (GM) techniques can provide Received 27 July 2010 insights into how the shape of the mandibular corpus differs between bonobos and chimpanzees and to Accepted 1 May 2012 explore the potential implications of those results for our understanding of hominin evolution. We Available online 8 June 2012 focused on this region of the mandible because of the relative frequency with which it has been recovered in the hominin fossil record. In addition, no previous study had explored in-depth three- Keywords: dimensional (3D) mandibular corpus shape differences between adults of the two Pan species using Chimpanzees geometric morphometrics. GM methods enable researchers to quantitatively analyze and visualize 3D Bonobos Australopithecus shape changes in skeletal elements and provide an important compliment to traditional two- Three-dimensional shape data dimensional analyses. Mandibular corpora Eighteen mandibular landmarks were collected using a Microscribe 3DX portable digitizer. Specimen configurations were superimposed using Generalized Procrustes analysis and the projections of the fitted coordinates to tangent space were analyzed using multivariate statistics. The size-adjusted corpus shapes of Pan paniscus and Pan troglodytes could be assigned to species with approximately 93% accuracy and the Procrustes distance between the two species was significant. Analyses of the residuals from a multivariate linear regression of the data on centroid size suggested that much of the shape difference between the species is size-related. Chimpanzee subspecies and a small sample of Australopithecus specimens could be correctly identified to taxon, at best, only 75% of the time, although the Procrustes distances between these taxa were significant. The shape of the mandibular symphysis was identified as especially useful in differentiating Pan species from one another. This suggests that this region of the mandible has the potential to be informative for taxonomic analyses of fossil hominoids, including hominins. The results also have implications for phylogenetic hypotheses of hominoid evolution. Ó 2012 Elsevier Ltd. All rights reserved.

Introduction extant great ape genus that researchers agree has multiple species (Badrian and Badrian, 1984; Thomson-Handler et al., 1984; Kano, As the closest extant relatives of humans, great apes are often 1992; Morin et al., 1994; Horai et al., 1995; Takahata et al., 1996; viewed as the most appropriate models for the extent and pattern Burrows and Ryder, 1997; Gagneux et al., 1999; Kaessmann et al., of morphological variation to be expected in early fossil hominin 1999; de Waal, 2001; Stone et al., 2002; Yu et al., 2003). Thus, species (LeGros Clark, 1964; Wolpoff, 1977; Kimbel and White, this taxon is valuable as a comparative model for assessing the 1988; Wood et al., 1991; Daegling, 1993; Shea et al., 1993; taxonomic homogeneity of putative species in the hominin fossil Richmond and Jungers, 1995; Lockwood et al., 1996; Uchida, 1996; record. Lockwood, 1999; Silverman et al., 2001; Guy et al., 2003, 2008; There have been many studies documenting craniodental and Harvati, 2003a; Robinson, 2003; Harvati et al., 2004; Skinner et al., postcranial differences between the two Pan species (Johanson, 2006; Lague et al., 2008; but see Jolly, 2001, 2009; Taylor, 2006 and 1974; Cramer and Zihlman, 1976; Cramer, 1977; Zihlman and references therein). Although some recent, and many earlier, Cramer, 1978; Corruccini and McHenry, 1979; McHenry and studies suggested that all great ape species other than Pan paniscus Corrucini, 1981; Shea, 1983a,b,c, 1984, 1985; Kinzey, 1984; could be split into two or more species (Groves, 1986, 2000, 2001, Laitman and Heimbuch, 1984; Shea and Coolidge, 1988; Groves 2003; Morin et al., 1994; Ruvolo et al., 1994; Grine et al., 1996; Muir et al., 1992; Uchida, 1992, 1996; Shea et al., 1993; Braga, 1995; et al., 1998, 2000; Albrecht et al., 2003; Brandon-Jones et al., 2004; Lockwood et al., 2002, 2004; Guy et al., 2003; Pilbrow, 2006; Thalmann et al., 2007; Bradley, 2008), Pan is currently the only Skinner et al., 2008, 2009; Singleton et al., 2011). Fewer studies have published data on differences between P. paniscus and Pan E-mail address: [email protected]. troglodytes in their mandibular morphology (Andrews, 1978;

0047-2484/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2012.05.003 Author's personal copy

192 C. Robinson / Journal of Human Evolution 63 (2012) 191e204

Brown, 1989; Taylor, 2002; Taylor and Groves, 2003; Schmittbuhl However, the positions of the tori relative to the dentition are et al., 2007; Boughner and Dean, 2008; Lague et al., 2008; strongly influenced by a number of factors, including the inclina- Zihlman et al., 2008). Most of the more recent analyses have used tion of the symphysis. Accounting for symphyseal inclination when multivariate methods to examine whether the mandibular shapes quantifying the size of the tori is difficult using standard techniques of these species could be significantly differentiated from one (Daegling, 1993; Daegling and Jungers, 2000; Robinson, 2003). GM another (Taylor, 2002; Taylor and Groves, 2003; Schmittbuhl et al., methods provide one possible means of documenting variation in 2007; Boughner and Dean, 2008; Lague et al., 2008). However, only these kinds of morphological features. three of these investigations included all three commonly recog- The primary questions to be addressed using these data were: nized subspecies of chimpanzees in their samples (Taylor, 2002; (1) How effectively can the mandibular corpora of P. paniscus and Taylor and Groves, 2003; Schmittbuhl et al., 2007). Sampling all P. troglodytes and those of the three P. troglodytes subspecies be three subspecies provides a more thorough documentation of the differentiated from one another using the 3D shape data derived range of variation in P. troglodytes and improves our confidence in from GM analyses and how does this compare to previous multi- any differences found between chimpanzees and bonobos. variate studies of these taxa? (2) What features on the mandibular Two of the three studies including all three chimpanzee corpus are most useful for distinguishing Pan species from one subspecies described the differences between the two Pan species another? (3) Are shape differences between the two Pan species in their mandibular morphology as less extensive than the differ- and three P. troglodytes subspecies related to differences in the sizes ences in their cranial shapes. These analyses presented data on 13 of their mandibular corpora? (Taylor, 2002) and 17 (Taylor and Groves, 2003) exclusively mandibular linear dimensions scaled to size, with over half of the measurements having at least one of their end points on the ramus. Materials and methods In the third study, Schmittbuhl et al. (2007) explored differences among extant hominoid taxa, including between P. paniscus and Sample P. troglodytes, in the mean outline shapes of their entire mandibles using elliptical Fourier techniques. However, since complete The sample for this study was comprised of 126 mandibular mandibles are rarely found in the hominoid fossil record and the specimens of P. paniscus and all three commonly recognized vast majority of specimens lack rami, it is useful to explore whether chimpanzee subspecies, Pan troglodytes schweinfurthii, Pan troglo- the morphology of the mandibular corpus on its own results in dytes troglodytes and Pan troglodytes verus (Table 1). Males and a similar or reduced ability to discriminate among hominoid females were not sampled equally because at most of the museums species (Robinson, 2003; Lague et al., 2008). Moreover, the results visited all available specimens were digitized. Data were collected of Taylor and Groves (2003) suggest that this region of the only on adult and wild-shot specimens, as determined by fully mandible may be especially important in differentiating bonobo erupted permanent dentition, museum tags, and catalog informa- and chimpanzee mandibles given that most of the significant tion. Specimens showing obvious abnormalities or substantial differences they found between these two taxa were measure- resorption due to antemortem tooth loss were excluded since those ments taken on the mandibular corpus. Lague et al.’s (2008) anal- factors would alter the shape of the mandibular corpus. These ysis included eight linear measurements scaled to the geometric restrictions meant that, despite visiting the collections at nine mean that are found on the more commonly preserved mandibular museums, only six male bonobos could be included in the sample. corpus to explore how effective these data were at grouping extant In addition, four Australopithecus afarensis and three hominoid specimens in the correct genus, species, and subspecies. In the other recent study of Pan mandibular morphology using Table 1 multivariate methods, Boughner and Dean (2008) focused on Number of specimens for each taxon, name of the localities where the hominin documenting ontogenetic changes in the three-dimensional (3D) specimens are derived from, and institutions where the specimens are housed. shape of the mandible in Pan using geometric morphometric (GM) Mandibular specimens techniques and, consequently, they included only a small sample of adults for the two species. Taxon(locality) Museums Sample size This investigation builds on these studies by exploring differ- Pan paniscus AMNH, BMNH, 23 (6M, 17F) ences between the two Pan species in the three-dimensional shape MCZ, MRAC Pan troglodytes schweinfurthii AMNH, BMNH, 29 (21 M, 8F) of the mandibular corpus using geometric morphometric tech- MRAC, NMNH niques. Three-dimensional geometric morphometric methods have Pan troglodytes troglodytes AMNH, NNM, 47 (25M, 22F) been used to quantify variation in modern human mandibular PCM, ZMB morphology, to explore differences among fossil hominin mandi- Pan troglodytes verus AMNH, BMNH, 27 (13M, 14F) bles, and to investigate the ontogenetic development of the NMNH, NNM, PMH Australopithecus afarensis NME 1 (MAK-VP 1/12) mandible in Pan (Rosas and Bastir, 2004; Oettlé et al., 2005; (Maka) Nicholson and Harvati, 2006; Boughner and Dean, 2008), but have Australopithecus afarensis NME 3 (AL 417-1a, not been employed, as of yet, to examine in depth differences (Hadar) 437-1, 438-1g) between adults of the two Pan species in their mandibular shapes. Australopithecus africanus TM, WITS 2 (Sts 7, 52) (Sterkfontein) One of the advantages of using 3D GM techniques is that it enables Australopithecus africanus TM 1 (MLD 2) researchers to document shape differences in morphological (Makapansgat) features that have previously only been qualitatively described, fi Sex, or specimen number in the case of the fossil hominin specimens, is indicated in often because they have been dif cult to accurately quantify using parentheses (M ¼ males, F ¼ females). Abbreviations for institutions: AMNH e traditional instruments (Dean, 1993; Harvati, 2001, 2003b; American Museum of Natural History; BMNH e British Museum of Natural History; Robinson, 2003; Rosas and Bastir, 2004; Nicholson and Harvati, MCZ e Museum of Comparative Zoology, Harvard; MRAC e Musée Royal de l’Afri- 2006). For example, the sizes of the symphyseal transverse tori que Centrale, Tervuren; NME e National Museum of Ethiopia; NMNH e National Museum of Natural History (Smithsonian); NNM e Nationaal Natuurhistorisch have been assessed qualitatively in most studies of extant homi- Museum, Leiden; PCM e Powell-Cotton Museum, Birchington, Kent; PMH e Pea- noids by noting how far they project posteriorly relative to the body Museum, Harvard; TM e Transvaal Museum; WITS e University of the Wits- tooth row (Aitchison, 1965; Brown, 1989, 1997; Singleton, 2000). watersraand; ZMB e Zoologische Museum, Berlin. Author's personal copy

C. Robinson / Journal of Human Evolution 63 (2012) 191e204 193

Australopithecus africanus specimens were included in a separate analysis using a subset of 12 of the 18 landmarks. The selection of these specimens was based on an attempt to minimize the number of landmarks that had to be excluded to avoid missing data and still have a small sample of each species.

Methods

Three-dimensional coordinates of 18 midline and left side mandibular landmarks were collected using a Microscribe 3DX portable digitizer (Table 2, Fig. 1). In geometric morphometrics, landmarks can be defined as ‘biologically meaningful’ points that can be consistently identified in all specimens (Richtsmeier et al., 1995; Valeri et al., 1998). Most of the landmarks digitized in this study were of either Type I or II (Bookstein, 1990; Valeri et al.,1998). Type I landmarks are contact points between structures, such as the intersection of two sutures, or the midpoints of foramina, while Type II landmarks are points at the maxima of curvature, such as points on the maxima of tori and the minima of sulci (Bookstein, 1990; MacLeod, 2001). Points that were digitized along the basal margin of the mandible directly inferior to the alveolar margin interdental septa are Type III landmarks (i.e., those at the ends of diameters). These coordinate points can be included as landmarks in some analyses using geometric morphometric techniques (Slice et al., 1996). To assess whether the coordinate points along the base of the mandible could be reliably identified and, thus, treated as land- marks in this study, data were collected on the same male chim- panzee mandible (L18) from the Mammalogy Department at the American Museum of Natural History ten times following the protocols described above. The Euclidean distance from each landmark to the specimen’s centroid was determined for all repli- cates and the mean-square errors (MSEs) for each landmark were calculated in Microsoft Office Excel 2007 to determine the intra- observer error (Singleton et al., 2011). MSEs ranged from 0.05 mm to 1.64 mm, with an average for the 18 landmarks of 0.45 mm. The average MSE for the four Type III landmarks on the basal margin of the mandible was 0.50 mm, not appreciably larger than the overall mean, suggesting that these landmarks are no more difficult to reliably identify than the Type I and Type II landmarks that were included in this project. A Generalized Procrustes analysis was run so that the relative Figure 1. Occlusal and lateral views of a Pan troglodytes mandible exhibiting all positions of the landmarks could be compared among the speci- landmarks that were digitized. The landmarks represented by the numbers are defined mens. In this method, superimposition of the specimens’ landmark in Table 2. configurations is accomplished by translating and rotating each specimen to a common coordinate system and orientation and Euclidean distances of all landmarks to a specimen’s centroid (Slice scaling it to unit centroid size so that the differences they exhibit et al., 1996). Superimposition of the specimen con figurations was are due to shape (Rohlf, 1990; Rohlf and Marcus, 1993; Slice, 1996). performed using Morpheus (Slice, 1998). Centroid size is defined as the square root of the sum of the squared The Procrustes aligned coordinates were analyzed using prin- cipal components analysis (PCA), which transforms the data to Table 2 a new coordinate system, reducing the dimensionality of the List of mandibular landmarks digitized on each specimen. Landmarks 5, 6, 9, 10, 14, dataset to focus on combinations of variables that are most infor- and 17 were removed in the fossil hominin analyses. mative for explaining the variation present within the sample. PCA Mandibular landmarks was also used to graphically demonstrate how effective these data 1e6. Medial alveolus interdental points were at separating the various groups from one another. Changes in 7e10. Basal margin points directly inferior to alveolar the relative positions of the landmarks along each PC axis were interdental landmarks 3e6 exhibited by linking the landmarks together using a wireframe in 11. Most projecting point of lateral prominence Morphologika (O’Higgins and Jones, 2004)(Fig. 2). A multivariate 12. Deepest point in lateral intertoral sulcus 13. Foramen mentale analysis of variance (MANOVA) was run on the PC scores to 14. Infradentale determine whether sex, subspecies, and species membership, and 15. Gnathion the interaction between these variables contributed significantly to 16. Mandibular orale variation on each PC axis. 17. Most projecting point of superior transverse torus To determine whether overall shape differences between the 18. Most projecting point of inferior transverse torus subspecies and species, and between males and females of each Author's personal copy

194 C. Robinson / Journal of Human Evolution 63 (2012) 191e204

study (86.8 and 104.2, respectively, p < 0.0001), it was important to assess whether the differences identified below between the groups were size-related. To accomplish this, a multivariate linear regression of the data from all PC scores together on centroid size was performed. All statistical analyses were then re-run on the residual data for each specimen. Finally, a preliminary analysis using the methods described above on the Pan specimens and a small sample of seven Austral- opithecus specimens (see Table 1) was run to assess whether these data could be used to accurately identify mandibles of A. afarensis and A. africanus to species. So as to have a representative sample of landmarks but still include a small sample of each species, six landmarks were removed from the dataset to avoid missing data (see Table 2). The DF analyses and permutation tests were run using the remaining 12 landmarks and including the seven hominins in the dataset. All statistical analyses were run using SAS 9.2 (SAS Institute Inc.).

Results

Principal components analysis

PC 1 accounted for 24.3% of the total variance and was signifi- cant for species (p < 0.0001) and sex (p < 0.01) effects, but not subspecies or interaction effects (p > 0.05). Bonobos tended to have more positive scores on PC 1, although their range overlapped that of chimpanzees (Fig. 3). Female P. troglodytes specimens tended to be located closer to the positive end of this axis and, thus, closer to P. paniscus, than male P. troglodytes specimens. No differences were readily apparent between male and female bonobo specimens on PC 1. Figure 2. Lateral view of a Pan troglodytes mandible exhibiting all landmarks that were digitized and a wireframe connecting the landmarks. The wireframe is used to help The shape differences between the wireframes at the extreme visualize shape differences along each principal components axis in Morphologika ends of PC 1 included a deeper mandibular corpus and symphysis, (e.g., Fig. 3). a less projecting superior transverse torus, a more posteriorly oriented symphyseal axis, a more anteriorly positioned lateral intertoral sulcus, and a more elongated postincisive planum for species, were significant, two group random permutation tests specimens closer to the negative end of this axis (i.e., P. troglodytes) were run on the Procrustes distances between the group mean than for those closer to the positive end of this axis (i.e., P. paniscus). configurations of the taxa and sexes using adaptations of SAS codes PC 4 was significant for species (p < 0.001), but not subspecies, written by Kieran McNulty (2005). In each permutation, specimens sex, or interaction effects (p > 0.05) and accounted for 6.5% of the were randomly placed into one of the two groups and the total variance. P. paniscus specimens tended to be located nearer to Procrustes distances between the resulting groups were then the negative end of this axis compared with those of P. troglodytes, calculated. This process was repeated 1000 times and the frequency although there was substantially more overlap in their ranges on (a) at which the permuted distances were less than the actual this axis than on PC 1 (Fig. 3). The shape differences between Procrustes distances (r) between the taxa or sexes was determined specimens on the positive end of PC 4 (P. troglodytes) and those on (Singleton et al., 2011). the negative end (P. paniscus) included a more posteriorly oriented A discriminant function (DF) analysis using cross-validation was symphyseal axis, a more elongated postincisive planum, and a more performed on a subset of the principal components to explore how posteriorly positioned mental foramen for those on the positive accurately mandibular specimens could be classified to the correct end of this axis. sex, subspecies, and species using these data. All groups were PC 2, accounting for 17.2% of the total variance, did not exhibit assigned equal prior probabilities and only the results for cross- significant taxonomic, sex or interaction effects (p > 0.05) and the validation classification were reported below. To determine the two Pan species and three P. troglodytes subspecies overlapped number of principal components to include within the DF analysis, extensively on this axis. a scree plot of the eigenvalues was created. This plot graphically PC 3, which accounted for 8.7% of the total variance, only exhibits the proportion that each principal component contributes exhibited significant subspecies effects (p < 0.0001) with all other to the overall variance. As is typical, the scree plot showed a steep categories non-significant (p > 0.05). PC 5 was also significant for drop over the first few PCs, with the percentage variance leveling subspecies effects and also sex effects (p < 0.0001), but not for any off after PC 9. Thus, only the first nine PCs, which accounted for other categories (p > 0.05). This axis accounted for 5.8% of the total approximately 78% of the variance, were employed in the DF variance. P. t. schweinfurthii specimens tended to be located closer analyses. to the positive end of PC 3, while P. t. verus specimens were Although geometric size is removed during Procrustes super- primarily located on the opposite end of this axis. On PC 5, P. t. verus imposition, size-related shape differences remain and can be specimens were mostly placed on the positive end while specimens important in differentiating taxa from one another. Since P. paniscus of the other two subspecies, particularly males, were typically had a significantly smaller centroid size than P. troglodytes in this located on the negative end (Fig. 4). Author's personal copy

C. Robinson / Journal of Human Evolution 63 (2012) 191e204 195

P. paniscus females

P. paniscus males

P. t. schweinfurthii females

P. t. schweinfurthii males

P. t. troglodytes females

P. t. troglodytes males

P. t. verus females

P. t. verus males

Figure 3. Scatterplot of the principal components scores for each specimen on PC 1 and PC 4. Lateral views of the wireframe shape configurations representing the extreme shapes along each axis are provided. Black squares e Pan paniscus females; black triangles e Pan paniscus males; white diamonds e Pan troglodytes schweinfurthii females; grey diamonds e Pan troglodytes schweinfurthii males; white circles e Pan troglodytes troglodytes females; grey circles e Pan troglodytes troglodytes males; black Xs e Pan troglodytes verus females; shaded grey Xs e Pan troglodytes verus males.

Permutation tests though the means of the individual subspecies were not particu- larly close to that of P. paniscus. This hypothesis was assessed by re- The Procrustes distances between the mean mandibular shapes running the permutation tests on the residual data and deter- of all species and subspecies were significant. As expected, the mining the Procrustes distances between P. paniscus and each of the shape differences were greatest between P. paniscus and P. troglodytes subspecies individually. In these tests, the pairwise P. troglodytes (r ¼ 0.0952). The Procrustes distance between the distances between bonobos and each of the chimpanzee subspecies mean shapes of P. t. schweinfurthii and P. t. troglodytes (r ¼ 0.0339) were significantly different (a < 0.05) and the distances were was just barely significant (a ¼ 0.035) and their mean shapes were similar to or greater than the pairwise distances between the much more similar to one another than either was to P. t. verus P. troglodytes subspecies. However, the distances between (Table 3). The mandibular shape of P. t. verus could be easily P. paniscus and the three subspecies were still quite reduced differentiated from those of the other subspecies (a ¼ 0) (Table 3). compared with the Procrustes distance between the species that The Procrustes distances between males and females were was found using the original dataset. This suggests that size-related similar for the two Pan species, although it is interesting to note shape differences are important in differentiating P. paniscus and that the Procrustes distance was greater between males and P. troglodytes. The multivariate regression of all PC scores together females of P. paniscus than between the P. troglodytes sexes on centroid size found that size was significantly associated with (Table 3). However, males and females of P. paniscus could not be the data (p < 0.001). The correlation coefficient (r2) was 0.7338, significantly differentiated from one another (a ¼ 0.075) while showing that size accounts for a substantial amount of the variance P. troglodytes sexes could be (a ¼ 0.023). These results were likely in the dataset. influenced by the small sample of male bonobos included in this The Procrustes distances between the P. troglodytes subspecies study. using the residual dataset were also less than those using the The Procrustes distance between bonobos and chimpanzees original data, although the most substantial reductions were in the using the residual data was substantially reduced compared to the pairwise distances between P. t. verus and the other two subspecies. distance between them using the original size-adjusted dataset The reduction in Procrustes distance was such that P. t. verus and (Table 3). The two taxa could no longer be significantly differenti- P. t. schweinfurthii were no longer significantly different. These ated and, in fact, their distance was less than all pairwise distances results suggest that shape differences between P. t. verus and the between the P. troglodytes subspecies. It seemed possible that the other two subspecies are, to some extent, size-related. reason for this result was that the dispersion of individuals of the Procrustes distances between males and females, particularly chimpanzee subspecies was such that they generated a mean value between male and female chimpanzees, were also reduced using for the species as a whole that was similar to that of bonobos, even the residual dataset. The sexes could not be significantly Author's personal copy

196 C. Robinson / Journal of Human Evolution 63 (2012) 191e204

P. paniscus females

P. paniscus males

P. t. schweinfurthii females

P. t. schweinfurthii males

P. t. troglodytes females

P. t. troglodytes males

P. t. verus females

P. t. verus males

Figure 4. Scatterplot of the principal components scores for each specimen on PC 3 and PC 5. Lateral views of the wireframe shape configurations representing the extreme shapes along each axis are provided. Symbols as in Fig. 3. differentiated in either species using these data. These results also the species extensively overlap and cannot be differentiated from imply that size is an important factor in shape differences between one another on Canonical 2 or 3 (Fig. 6). males and females, especially for P. troglodytes. Only 52.9% of female and 33.3% of male bonobos were identified to the correct sex, while 65.9% of chimpanzee females and 67.8% of Discriminant function analysis males were correctly identified to sex. For the chimpanzee subspecies, 44.8% of the P. t. schweinfurthii, In the discriminant function analysis, all of the P. paniscus and 59.6% of the P. t. troglodytes, and 74.1% of the P. t. verus specimens 91.3% of the P. troglodytes specimens were correctly identified to could be accurately identified. Only 10.3% and 17.0% of the mis- species. Nine chimpanzee specimens were misclassified as bono- identified P. t. schweinfurthii and P. t. troglodytes specimens were bos: one P. t. schweinfurthii female, four females and one male P. t. classified as P. t. verus specimens, respectively. Thus, just as in the troglodytes, and two females and one male P. t. verus. When the permutation tests, the most substantial differences among the linear discriminant scores are plotted, there is only a slight overlap P. troglodytes subspecies were between P. t. verus and the other two between P. paniscus and P. troglodytes on Canonical 1 (Fig. 5), while taxa.

Table 3 Results from two group random permutation tests.

Two group random permutation tests

Pairwise comparison Original data Residuals

Procrustes distance (r) Frequency (a) Procrustes distance (r) Frequency (a) P. paniscus e P. troglodytes 0.0952 0.000 0.0284a 0.141 P. t. schweinfurthii e P. t. troglodytes 0.0339 0.035 0.0326 0.026 P. t. schweinfurthii e P. t. verus 0.0541 0.000 0.0313 0.052 P. t. troglodytes e P. t. verus 0.0472 0.000 0.0317 0.014 P. paniscus males e females 0.0373 0.673 0.0371 0.660 P. troglodytes males e females 0.0306 0.023 0.0261 0.111

The Procrustes distances (r) between the taxa using both the original size-adjusted data and the residual data derived from the linear regression of the data from all PC scores combined on centroid size are provided, along with the frequency (a) at which the Procrustes distances between 1000 randomly selected groups are less than that between the taxa. a The Procrustes distances between Pan paniscus and Pan troglodytes schweinfurthii, P. t. troglodytes, and P. t. verus using the residual dataset are 0.0364, 0.0323, and 0.0468, respectively (a < 0.05). Author's personal copy

C. Robinson / Journal of Human Evolution 63 (2012) 191e204 197

P. paniscus females

P. paniscus males

P. t. schweinfurthii females

P. t. schweinfurthii males

P. t. troglodytes females

P. t. troglodytes males

P. t. verus females

P. t. verus males

Figure 5. Scatterplot of Can 1 and Can 2 for the linear discriminant scores. Symbols as in Fig. 3.

When the DF analyses were run on the residuals, only 60.9% of misclassified as a chimpanzee instead of none of them being mis- the bonobo specimens and 59.2% of the chimpanzee specimens identified. All of the hominin fossils were classified as hominins. could be correctly identified to taxon. The discriminatory power However, only 75% of the A. afarensis and 33% of the A. africanus also decreased in the P. troglodytes subspecies analysis with only specimens were accurately allocated to their putative species. 24.1%, 51.1%, and 44.4% of the P. t. schweinfurthii, P. t. troglodytes, and Further tests were run that included additional A. afarensis speci- P. t. verus specimens, respectively, correctly allocated to subspecies. mens by reducing the number of landmarks further, but this did not These results suggest that, similar to the permutation test results, substantially improve the classification accuracy for the hominin shape differences among these taxa, are, to some degree, size- specimens. related. In the DF analyses of males and females of the two Pan species Discussion using the residual data, 61.4% of P. troglodytes females and 72.9% of males could be correctly identified to sex. For bonobos the Interspecific differences percentages correctly allocated were 64.7% for females and 33.3% of males. These figures are similar to those reported above using the In the PCA, the mandibular corpus specimens of P. paniscus and non-residual data. P. troglodytes were significantly separated from one another on PCs 1 and 4, although there was some overlap of the species’ ranges on Fossil hominin results both axes. Previous multivariate analyses of Pan mandibular morphology also were able to clearly discriminate between In the permutation test using the subsample of 12 landmarks, P. paniscus and P. troglodytes (Taylor, 2002; Taylor and Groves, 2003; the Procrustes distance between the P. paniscus and P. troglodytes Schmittbuhl et al., 2007; Boughner and Dean, 2008; Lague et al., mean mandibular shapes was still significant and was, in fact, 2008). slightly greater than when all 18 landmarks were included in the Using 11 of their 17 linear mandibular measurements scaled to analysis (r ¼ 0.103; a ¼ 0). The Procrustes distance between the size, Taylor and Groves (2003) were able to accurately identify 76% A. afarensis and A. africanus mean shapes was similar to, but greater of their P. paniscus and 96% of their P. troglodytes specimens. They than, that between the two Pan species and the two fossil hominin were able to achieve 100% discrimination for both taxa by including species could be significantly differentiated from one another even the additional six variables in the analysis, but argued that doing so with the small sample size (r ¼ 0.136; a ¼ 0.023). led to problems with multicollinearity. Schmittbuhl et al. (2007) Even after removing six of the landmarks, chimpanzees and did an elliptical Fourier analysis of the entire mandibular outline bonobos were identified with nearly the same accuracy as with the scaled to size. They were able to correctly allocate approximately full complement of landmarks in the discriminant function anal- 97% of their P. paniscus and 91e98% of their P. troglodytes specimens ysis, with the only difference being one bonobo that was to the correct species in their discriminant function analysis using Author's personal copy

198 C. Robinson / Journal of Human Evolution 63 (2012) 191e204

P. paniscus females

P. paniscus males

P. t. schweinfurthii females

P. t. schweinfurthii males

P. t. troglodytes females

P. t. troglodytes males

P. t. verus females

P. t. verus males

Figure 6. Scatterplot of Can 2 and Can 3 for the linear discriminant scores. Symbols as in Fig. 3. cross-validation. In their discriminant analysis, Lague et al. (2008), another. Moreover, Taylor and Groves (2003) found that most of the using data from eight linear measurements only on the mandibular significant differences between P. paniscus and P. troglodytes corpus scaled to the geometric mean, were able to allocate subspecies for size-adjusted linear measurements were on the approximately 91% of their specimens to the correct Pan species. It mandibular corpus, with few significant differences between those should be noted that unlike the current study and that of Taylor and taxa for measurements that included a point on the ramus. The Groves (2003), Lague et al. did not include P. t. verus in their sample, results of Schmittbuhl et al. (2007) could be viewed as evidence which, according to genetic analyses of chimpanzees (Morin et al., against this hypothesis since they were able to achieve the most 1994; Horai et al., 1995; Gonder et al., 1997, 2006; Gagneux et al., accurate classification of bonobo and chimpanzee mandibles 1999; Guy et al., 2003; Taylor and Groves, 2003; Caswell et al., although they included data from the ramus in their analyses. 2008; Fischer et al., 2011), is more distantly related to the other However, their classification accuracy was only slightly better than two subspecies than they are to one another. Given that this study that of this study and that of Lague et al. (2008) suggesting that and others (Taylor and Groves, 2003; Schmittbuhl et al., 2007) most of the important differences between these species are on the found P. t. verus to have the most distinct mandibular morphology mandibular corpus. of the three chimpanzee subspecies, including western chimpan- It may be that the ability to significantly differentiate bonobos zees in a dataset is likely to increase the extent of intraspecific and chimpanzees in this study was influenced by the substantially variation in the chimpanzee sample and could make it more diffi- larger number of female, compared with male, bonobo specimens. cult to differentiate chimpanzees from bonobos. In the MANOVA, the overall female mean PC score was found to be In the above DF analyses, using data from only the mandibular significantly different from that of males on PC 1 and it could be corpus, like Lague et al. (2008), bonobo and chimpanzee specimens that if more male bonobos were included in the analysis, the were identified to species with approximately 93% accuracy after interspecific differences would have been less evident. However, the data were scaled to unit centroid size. Thus, the discriminatory when the MANOVA was run on the species separately, no signifi- power of these data was similar to those of previous multivariate cant differences were found between the mean PC scores of males studies that included data from the ramus (Taylor and Groves, and females of either species on this axis. While female chimpan- 2003; Schmittbuhl et al., 2007). These results and those from zees tended to be located closer to the bonobos on PC 1, the six male most of the other research cited above would appear to suggest that bonobos were not positioned any closer to the chimpanzee speci- the shape of the mandibular corpus may be more effective for mens on this axis than female bonobos were (see Fig. 3). Moreover, discriminating between these taxa than the ramus. Unlike the the Procrustes distance between male and female bonobos was not current study and that of Lague et al. (2008), approximately half of significant and in the DF analysis male and female bonobos could be Taylor and Groves’ (2003) linear measurements included at least differentiated at only slightly better than chance. This result is not one endpoint on the ramus and their dataset provided the lowest surprising given the recent studies showing a lack of significant discriminatory power for differentiating the Pan species from one sexual dimorphism in P. paniscus for any measurements taken on Author's personal copy

C. Robinson / Journal of Human Evolution 63 (2012) 191e204 199 the mandibular corpus or for any shape ratios derived from those and P. t. troglodytes. However, the current study was undertaken to measurements (Taylor, 2006) and no significant differences explore whether shape differences in the mandibular corpus could between the outline shapes of the mandibles of male and female be used to differentiate fossil species, not subspecies. Consequently, bonobos (Schmittbuhl et al., 2007). This suggests that it is unlikely the rest of the discussion will be focused on species-level that the skewed sex ratio of bonobos is the factor that led to the differences. finding of significant interspecific diversity in mandibular morphology documented above. If bonobos are ‘essentially Mandibular shape differences between Pan species monomorphic’ in mandibular size and shape (Taylor, 2006), then including more males should not alter the results significantly. In the principal components analysis, shape differences It should be noted that Taylor and Groves (2003) and between the two Pan species remained after specimens were scaled Schmittbuhl et al. (2007) in their discriminant function (DF) anal- to unit centroid size. In particular, variation on PCs 1 and 4 was yses separated the P. troglodytes specimens into subspecies for related to mandibular shape differences that included P. troglodytes comparison with P. paniscus, while in this study and that of Lague having a deeper, more posteriorly inclined mandibular symphysis et al. (2008) all P. troglodytes subspecies were grouped together. with a longer postincisive planum, a less projecting superior To test whether this difference could influence the results of the transverse torus, a mandibular corpus that deepens more current analysis, a DF analysis was run with four groups (i.e., substantially anteriorly, a more posteriorly positioned mental specimens of the three P. troglodytes subspecies separated from one foramen, and a more anteriorly positioned lateral intertoral sulcus. another). In this re-analysis, the data were slightly better at allo- These differences are demonstrated graphically in Fig. 7, which cating specimens to the correct species with 93.2% of the superimposes the mean shapes generated in Morpheus (Slice, P. troglodytes and 95.7% of the P. paniscus specimens correctly 1998) for the bonobo and chimpanzee specimens in this study. identified. Thus, this methodological difference would not seem to Most of these differences are due to characters that are present be an influence on the ability of this study to allocate a specimen to on the mandibular symphysis. Guy et al. (2008) contended, as the correct species. a number of other researchers have suggested (Biegert, 1963; Researchers have found in some studies that 3D landmark- Schultz, 1963, 1969; Simons and Pilbeam, 1965; Simons, 1972; based methods were more effective than using size-adjusted Andrews, 1978; Logan et al., 1983; White et al., 2000), that variation linear data for identifying and quantifying morphological differ- in the symphysis is such that using symphyseal morphology alone ences among species (Hartman, 1989; Adams et al., 2004; Singleton to allocate specimens to taxon is unsatisfactory and that misclas- et al., 2011). This study does not refute that hypothesis and, if sification should be expected. This was based on their only being anything, provides tentative support for it. More importantly, it able to allocate approximately 87% of their gorilla and orangutan demonstrates that 3D GM studies are important for providing specimens to the correct genus using data from an elliptical Fourier complementary data to results derived from 2D linear measure- analysis of the outline of the mandibular symphysis. It may be that ments to help better understand morphological differences among it is necessary to include data from the rest of the mandibular taxa. corpus to more accurately identify hominoid mandibular species to taxon or that, as suggested previously (Daegling and Jungers, 2000; Subspecific differences Sherwood et al., 2005), particular morphological characters, or combinations of characters, on the symphysis are useful for allo- In the above analysis, P. t. verus specimens could be accurately cating fossil specimens to the correct species. Further exploration of identified to taxon almost 75% of the time, while fewer than 60% of this issue is currently being undertaken in a separate project using the other two subspecies could be correctly allocated, with most of a larger and more taxonomically diverse sample (Robinson et al., them incorrectly identified as P. t. schweinfurthii or P. t. troglodytes 2012). specimens. Moreover, the Procrustes distances between P. t. verus Some of the morphological traits found to distinguish chim- and the other two subspecies were considerably greater than the panzees from bonobos in the above analyses have not previously distance between P. t. schweinfurthii and P. t. troglodytes. This is been studied in both of these species (e.g., symphyseal axis orien- consistent with genetic evidence suggesting that P. t. schweinfurthii tation and postincisive planum length). For other mandibular and P. t. troglodytes are more closely related to one another than features it is possible to compare these results with those from either is to P. t. verus (Morin et al., 1994; Horai et al., 1995; Gonder et al., 1997, 2006; Gagneux et al., 1999; Caswell et al., 2008; Fischer et al., 2011). The percentage of P. t. verus specimens that were correctly identified in this study is nearly identical to that of Taylor and Groves (2003) and greater than that of Schmittbuhl et al. (2007). However, Taylor and Groves’ (2003) data were somewhat more accurate at allocating P. t. troglodytes and P. t. schweinfurthii to their correct groups than either this study or that of Schmittbuhl et al. (2007), with P. t. schweinfurthii being the most difficult subspecies to place in the correct taxon in all three studies. It is worth noting that Lague et al. (2008) had much greater success differentiating P. t. schweinfurthii and P. t. troglodytes from one another (80% accuracy) than any of the other three studies. This could potentially be because they did not include P. t. verus in their analysis given that over 10% of P. t. schweinfurthii and P. t. troglodytes specimens in the Figure 7. Superimposition of the mean landmark configurations of the Pan troglodytes other three studies were misidentified as P. t. verus specimens. (filled circles) and Pan paniscus (open circles) specimens in this study (‘MF’ e the mean position of the mental foramen landmarks for P. paniscus and P. troglodytes; ‘IS’ e mean Overall, multivariate analyses using linear measurements were position of the intertoral sulcus landmarks; ‘LP’ e mean position of the lateral prom- somewhat more effective at correctly identifying mandibular inence landmarks). The wireframes do not represent data and are added only to aid in specimens of the two closely related subspecies, P. t. schweinfurthii visualizing differences between the taxa. Author's personal copy

200 C. Robinson / Journal of Human Evolution 63 (2012) 191e204 other studies. For example, other researchers have also found that features in taxa of varying sizes (Shea, 1983a,b,c) and morpholog- bonobos and chimpanzees are significantly different from one ical differences between the two Pan species have often been another for relative symphyseal depth, with chimpanzees having attributed to allometric effects (Corruccini and McHenry, 1979; a deeper symphysis (Taylor and Groves, 2003; Boughner and Dean, McHenry and Corruccini, 1981; Shea, 1983a,b,c, 1985; Shea et al., 2008; Lague et al., 2008). Taylor and Groves (2003) also found that 1993; Uchida, 1996; Taylor and Groves, 2003; Singleton et al., P. paniscus could be differentiated from males and females of some, 2011). Since, as expected, the centroid size of P. paniscus in this but not all, P. troglodytes subspecies for relative corpus height at M1, study was significantly smaller than that of P. troglodytes,itwas while for relative corpus height at M2 of the six pairwise compar- important to explore whether the differences described above isons only P. t. schweinfurthii males were significantly different from between P. paniscus and P. troglodytes in the three-dimensional P. paniscus males. This is consistent with the above results that shape of the mandibular corpus might be size-related. found differences between the two Pan species for relative corpus Using the residual data approximately 60% of the Pan specimens depth to be more pronounced anteriorly. could be correctly identified to species, a substantial loss of In the above analyses, P. paniscus was also found to have a rela- discriminatory power compared with the results from the original tively shorter postincisive planum and a relatively more projecting dataset. Moreover, the Procrustes distances between P. paniscus and superior transverse torus than P. troglodytes. Singleton (2000) the P. troglodytes subspecies were reduced, with differences in their coded the position of the superior transverse torus as the same mean shapes being significant for only two of the three pairwise relative to the dental arcade in P. paniscus and P. troglodytes. comparisons. Finally, the linear regression of the combined PC However, if the symphyseal axis is inclined postero-inferiorly, scores on centroid size found a significant correlation between the a more posteriorly positioned torus can result from a number of data and size, with a high correlation coefficient (r2 ¼ 0.7338). different factors including a longer postincisive planum, a more These results would seem to indicate that the mandibular corpus posteriorly inclined symphysis, a deeper symphysis, and an shape differences captured by these landmarks between the Pan increase in the size of the torus relative to the midline of the species are, to some extent, size-related shape differences. Size is symphysis (i.e., a more projecting torus). The results of the current clearly an important factor in differentiating the mandibles of these study confirm Singleton’s (2000) characterization of the position of two species, although there are some shape differences between the torus relative to the dentition as the same in P. paniscus and them that are not related to size. This is consistent with the results P. troglodytes. However, the way in which the torus comes to be of Boughner and Dean (2008) who argued that chimpanzee positioned in the same place is different in P. paniscus and mandibles are not just scaled up versions of bonobo mandibles and P. troglodytes. In chimpanzees, the postincisive planum is more also with those of other studies that found similar scaling patterns elongated and the symphysis more posteriorly inclined than in for many, but not all, bonobo and chimpanzee mandibular bonobos, while in bonobos the projection of the torus relative to measurements (Taylor, 2002; Taylor and Groves, 2003). As noted by the midline symphyseal axis is greater than in chimpanzees. These Shea et al. (1993), the finding that some of the shape differences results support the suggestions by Daegling (1993) and Daegling between the two Pan species are due to ontogenetic scaling does and Jungers (2000) that differentiation of hominoid taxa using not in any way change the validity of the taxonomic assignment of symphyseal toral morphology may be possible (contra Simons, P. paniscus. By contrast, it underscores the importance of size and 1972) using a quantitative approach. allometry in differentiating closely related species. A lateral hollow (or intertoral sulcus) lies between the lateral superior torus and the marginal torus on the lateral corpus of most Australopithecus results hominoids. It is bounded posteriorly by the lateral prominence. Anteriorly, it is frequently delimited by the canine or P3 jugum. A number of studies have described differences between the Studies of this structure in hominoids have qualitatively described mandibular morphologies of A. afarensis and A. africanus (Johanson the depth and extent of this hollow on the lateral corpus without et al., 1978, 1982; Johanson and White, 1979; White et al., 1981; mention of any differences between the two Pan species (White, White and Johanson, 1982; Kimbel et al., 1984, 1994; Chamberlain 1977; Brown, 1989; Kramer, 1989; Strait et al., 1997; Singleton, and Wood, 1985, 1987; Kramer, 1986; Kimbel and White, 1988; 2000). The finding above that the deepest point of the lateral Daegling and Grine, 1991; Wood, 1991; Wood and Richmond, 2000; intertoral sulcus tends to be more posteriorly positioned in Ward et al., 2001). In this study, nearly 60% (four out of seven) of the P. paniscus may suggest that its sulcus extends further posteriorly fossil hominin species were allocated to the correct putative species than that of P. troglodytes. However, this merits a more detailed in the DF analysis, with all specimens correctly identified as hom- quantitative analysis. inins, even with a reduced set of 12 landmarks. It is possible with Variation on PC 4 was in part related to the mental foramen a larger sample size, particularly including additional specimens being relatively more posteriorly positioned in P. troglodytes. from both species that these methods could be used to accurately Qualitative studies have typically described the modal position of place specimens into the correct taxon. This hypothesis is sup- the mental foramen along the dental arcade as the same (inferior to ported by the two groups’ random permutation test, which shows P4) in all great ape species and modern human populations their Procrustes distance to be greater than that between the two (Simonton, 1923; Schulz, 1933; Tebo and Telford, 1950; Wood and Pan species and finds them to be significantly different from one Chamberlain, 1986; Brown, 1989; Trinkaus, 1993). However, another. Further study of differences in the 3D shape of fossil a quantitative analysis of mental foramen position relative to dental hominin mandibles using larger extant and fossil hominoid data- arcade length found significant differences among great apes, with sets is currently being undertaken (Robinson et al., 2012). P. troglodytes exhibiting a relatively posteriorly positioned mental foramen compared with other hominoids (Robinson and Williams, Implications for fossil hominin studies 2010). Other than teeth, mandibles are the most common skeletal Size and scaling in Pan mandibular morphology elements recovered at most hominin-bearing localities, and most of these specimens lack rami (White,1977; White and Johanson,1982; It has been argued that much of the diversity in skeletal shape Tobias, 1991; Wood, 1991; Ward et al., 2001; Robinson, 2003). among great apes is due to allometric scaling of morphological Because of this, characters on the mandibular corpus have been Author's personal copy

C. Robinson / Journal of Human Evolution 63 (2012) 191e204 201 important in both taxonomic and phylogenetic analyses of fossil was shown above for the two Pan species in the analysis of the hominins (Johanson et al., 1978, 1982; Johanson and White, 1979; reduced landmark dataset that included fossil hominins. Also, it is Tobias, 1980; White et al., 1981; Skelton et al., 1986; Wood and possible to use subsets of landmarks to explore variation in specific Chamberlain, 1986; Chamberlain and Wood, 1987; Wood, 1991, morphological features on the mandibular corpus that have been 1992; Skelton and McHenry, 1992, 1998; Leakey et al., 1995; Brunet identified as potentially useful for assessing fossil hominoid et al., 1996; Strait et al., 1997; Strait and Grine, 1998, 2001, 2004; taxonomy (e.g., Robinson and Williams, 2010). Other options for Senut et al., 2001; Ward et al., 2001; Robinson, 2003; Schmittbuhl dealing with missing data that have been suggested in the litera- et al., 2007; Guy et al., 2008; Lague et al., 2008). Improving our ture are to substitute species-specific mean values for the missing understanding of mandibular corpus variation in the only two data (Slice, 1996; Singleton et al., 2011), to use various algorithms, extant hominoid species that researchers agree are congeneric has information on structural constraints and morphological integra- the potential to improve our models of the extent and pattern of tion, and data from more complete specimens to reconstruct variation to be expected in the mandibular corpora of fossil hom- missing or deformed areas of a specimen (Gunz et al., 2004, 2009; inin species. One cannot necessarily make the assumption that the Mitteroecker and Gunz, 2009), or to use regression equations to features of the mandibular corpus that are found to differentiate estimate landmark coordinates (Adams et al., 2004; Gunz et al., extant hominoid species will be the same as those that are effective 2004; Bastir et al., 2008). for attributing fossil hominin mandibular specimens to species. Analyses of great ape skeletal morphology have been important in However, this study, and that of Lague et al. (2008), provide helping researchers reconstruct the phylogenetic relationships of fossil evidence that the extent of intraspecific variation in the mandibular hominin taxa by providing data to aid in the determination of character corpus of Pan is not so great that it is difficult to differentiate these polarity and mandibular features have frequently been included in the species from one another. This suggests that the mandibular corpus lists of characters used by researchers to test phylogenetic hypotheses is potentially informative for studies of fossil hominin taxonomy. (Skelton et al.,1986; Chamberlain and Wood,1987; Wood,1991; Groves This also supports the research of Collard and Lycett (2009), and et al., 1992; Skelton and McHenry, 1992, 1998; Lieberman et al., 1996; contrasts with that of Wood and Lieberman (2001), who argued Strait et al., 1997; Strait and Grine,1998, 2001, 2004; Wood and Collard, that removing characters, such as most of those on the mandible, 1999). Thus, studies like this one that document which features of the based on their likelihood of being phenotypically plastic does not mandible differ significantly among extant hominoid species could also necessarily lead to more reliable taxonomic hypotheses. help in refining phylogenetic hypotheses of fossil hominins. For Taylor (2006) has argued that using great apes as models for the example, if the two Pan species are found to exhibit shape differences extent of variation to be expected in the mandibles of fossil hom- for a particular morphological feature on the mandibular corpus, it inins seems ill-advised, given her study of great apes showing that wouldbeusefultore-examinehowthegenusPan, one of the outgroups the dimorphism patterns of mandibular dimensions and ratios in almost any hominin phylogenetic analysis, should be coded for that based on those dimensions exhibit great variability even among character. subspecies of the same species. Using extant hominoids as exem- In the present study, one of the shape differences identified plars for resolving whether fossil hominin samples are taxonomi- between P. paniscus and P. troglodytes was the more posteriorly cally heterogeneous has been questioned for a number of reasons, inclined symphyseal axis of chimpanzees. Phylogenetic analyses of including the relative paucity of comparative extant ape species, by fossil hominins have typically coded all great apes as having other researchers (Martin, 1991; Grine et al., 1996; Kelley and receding symphyses (Skelton and McHenry, 1992; Strait et al., 1997; Plavcan, 1998; Jolly, 2001, 2009). However, most studies continue Strait and Grine, 2001, 2004). While extant hominoids generally to use extant hominoids as the most appropriate model taxa for have more receding symphyses than most hominins, this study fossil hominins, principally because their phylogenetic proximity demonstrates that there is diversity among hominoid taxa that makes it more likely that they share similar patterns of variation could prove informative if taken into account in phylogenetic (Wood et al., 1991; Daegling, 1993; Shea et al., 1993; Richmond and analyses that include this character. As noted by White et al. (2000), Jungers, 1995; Lockwood et al., 1996; Uchida, 1996; Silverman et al., there is substantial variation for this character in extant hominoid 2001; Guy et al., 2003; Robinson, 2003; Harvati, 2003a; Harvati species that encompasses the range supposedly separating some et al., 2004; Skinner et al., 2006; Lague et al., 2008). Exploring putative fossil hominin species (e.g., Australopithecus bahrelghazali this topic in any depth is beyond the scope of this paper as the and A. afarensis). Some fossil hominins, particularly some of the theory behind allocating fossils to particular species is a complex early Pliocene specimens (e.g., the Australopithecus anamensis and contentious subject. However, to address specifically using our mandibular specimens, LH 4, and a number of the Hadar mandi- understanding of great ape mandibular variation to allocate fossil bles), have symphyseal axes that are similar to, or more receding hominin mandibular specimens to species, Taylor (2006: 94) quite than, those of extant hominoids (Robinson, 2003). Thus, it would appropriately suggests that particular “combinations of mandibular seem that a re-examination of the coding scheme for this character variables may fare better” in taxonomic analyses. This is one of the is warranted. For most fossil specimens preserving the mandibular potential advantages of 3D multivariate analyses: to identify such symphysis, the data for this character could be readily collected combinations of variables, including ones that are difficult to using 3D GM since only four landmarks would need to be preserved quantify using traditional morphometrics, that may be useful for for a specimen to be included in the analysis. differentiating taxa. The above results using 3D geometric Another example of a character whose coding in phylogenetic morphometrics suggest regions of the mandibular corpus that may analyses of hominins might be affected by the results of this study be especially informative for taxonomic analyses (e.g., the shape of is the depth of the mandibular corpus. Lucas et al. (2008) charac- the mandibular symphysis) and should be studied in more detail in terized the mandibular corpus height as ‘tall’ in both P. troglodytes extant and fossil hominoids. and in the last common ancestor (LCA) of humans and Pan. It is important to emphasize that fossil hominin specimens are However, given that P. paniscus was found to have a relatively frequently fragmentary and do not typically retain all of the land- shallower mandibular corpus than P. troglodytes in this study and marks used in this study. Like other multivariate methods, GM that of Taylor and Groves (2003) and that stem hominins are coded techniques cannot include specimens with missing data. However, as having a ‘moderately tall’ mandibular corpus by Lucas et al. sometimes similar discriminatory power can be achieved even (2008), it may be that it is more parsimonious to code the LCA as when removing some of the landmarks because of missing data, as having a ‘moderately tall’ corpus. 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202 C. Robinson / Journal of Human Evolution 63 (2012) 191e204

By undertaking additional studies of hominoid skeletal variation Museum, Harvard University. Drs. Michelle Singleton, Terry Harri- and diversity, researchers can further refine the character states son, Steven Frost and, especially, Kieran McNulty provided impor- and polarities of morphological characters, likely leading to more tant and welcome advice on the statistical methods used in this accurate phylogenies. Criticisms of hominoid phylogenetic study and the interpretations of the resulting data. Special thanks hypotheses that are based on skeletal data (e.g., Collard and Wood, to Dr. Katerina Harvati for her help with many aspects of this 2000, 2001) have often made an implicit assumption that project. I also thank the editor, associate editor, and two anony- morphological diversity among extant hominoids was well docu- mous reviewers for their insightful comments and suggestions, mented. However, it would seem that more extensive research on which helped to substantially improve this paper. This research was intraspecific variation and interspecific diversity in extant homi- supported by NSF (NYCEP RTG) and the James Arthur Fellowship for noid skeletal morphology is likely to improve our understanding of the write-up of doctoral research at New York University. This is hominin evolution. NYCEP morphometrics contribution No. 27.

Conclusions References Significant differences in the three-dimensional form of the Adams, G.L., Gansky, S.A., Miller, A.J., Harrell Jr., W.E., Hatcher, D.C., 2004. mandibular corpus were documented in this study between Comparison between traditional 2-dimensional cephalometry and a 3- P. paniscus and P. troglodytes after scaling the specimens for size. dimensional approach on human dry skulls. Am. J. Orthod. Dentofacial The following features were found to differentiate bonobos from Orthop. 126, 397e409. Aitchison, J., 1965. Contrasts in the mandibles and mandibular teeth of the chim- chimpanzees: a more vertical symphyseal axis, a more projecting panzee, orangutan and gorilla. Dent. Mag. Oral Top. 81, 105e108. superior transverse torus, a reduced postincisive planum, a shal- Albrecht, G.H., Gelvin, B.R., Miller, J.M.A., 2003. 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