Michelle Singleton Patterns of cranial shape variation in the Department of Anatomy, Papionini (Primates: Cercopithecinae) Midwestern University, 555 31st Street, Downers Grove, Traditional classifications of the Old World monkey tribe Papionini Illinois 60515, U.S.A. (Primates: Cercopithecinae) recognized the mangabey genera E-mail: Cercocebus and Lophocebus as sister taxa. However, molecular studies [email protected] have consistently found the mangabeys to be diphyletic, with Cercocebus and Mandrillus forming a clade to the exclusion of all other Received 10 January 2001 papionins. Recent studies have identified cranial and postcranial Revision received features which distinguish the Cercocebus–Mandrillus clade, however 26 October 2001 and the detailed similarities in cranial shape between the mangabey accepted 12 December 2001 genera are more difficult to reconcile with the molecular evidence. ff Keywords: Papionini, Given the large size di erential between members of the papionin molecular clades, it has frequently been suggested that allometric mangabey diphyly, cranial ff homoplasy, allometry, e ects account for homoplasy in papionin cranial form. A combina- geometric morphometrics. tion of geometric morphometric, bivariate, and multivariate methods was used to evaluate the hypothesis that allometric scaling contributes to craniofacial similarities between like-sized papionin taxa. Patterns of allometric and size-independent cranial shape variation were subsequently described and related to known papionin phylogenetic relationships and patterns of development. Results confirm that allometric scaling of craniofacial shape characterized by positive facial allometry and negative neurocranial allometry is present across adult papionins. Pairwise comparisons of regression lines among genera revealed considerable homogeneity of scaling within the Papionini, however statistically significant differ- ences in regression lines also were noted. In particular, Cercocebus and Lophocebus exhibit a shared slope and significant vertical displacement of their allometric lines relative to other papionins. These findings give no support to narrowly construed hypotheses of uniquely shared patterns of allometric scaling, either between sister taxa or across all papionins. However, more general allometric trends do appear to account for a substantial proportion of papionin cranial shape vari- ation, most notably in those features which have influenced tra- ditional morphological phylogenies. Examination of size-uncorrelated shape variation gives no clear support to molecular phylogenies, but underscores the absence of morphometric similarities between the mangabey genera when size effects are controlled. Patterns of allometric and size-uncorrelated shape variation indicate conserva- tism of cranial form in non-Theropithecus papionins, and suggest that Papio represents the primitive morphometric pattern for the African papionins. Lophocebus exhibits a divergent morphometric pattern, clearly distinguishable from other papionins, most notably Cercocebus. These results clarify patterns of cranial shape variation among the extant Papionini and lay the groundwork for studies of related fossil taxa.  2002 Elsevier Science Ltd

Journal of Human Evolution (2002) 42, 547–578 doi:10.1006/jhev.2001.0539 Available online at http://www.idealibrary.com on

0047–2484/02/050547+32$35.00/0  2002 Elsevier Science Ltd 548 . 

Introduction either within individual clades or across all papionins. The second was to describe The Old World monkey tribe Papionini patterns of allometric and residual (size- (Primates: Cercopithecinae) comprises a uncorrelated) cranial shape variation and monophyletic group of six extant genera. interpret these patterns in the light of While Macaca is widely acknowledged as prior studies of papionin ontogeny and representing the sister taxon to the African phylogeny. papionins (Strasser & Delson, 1987; Morales & Melnick, 1998), relationships among the latter taxa have been a source Background of controversy. Traditional classifications recognized the mangabey genera Cercocebus The Old World monkey tribe Papionini and Lophocebus as sister taxa and frequently Burnett, 1828 (Primates, Cercopithecinae) accorded them congeneric status on the encompasses six extant genera: Macaca, the basis of shared morphological traits macaques; Cercocebus and Lophocebus, the (Thorington & Groves, 1970; Szalay & mangabeys; Mandrillus, including mandrills Delson, 1979). However, molecular studies and drills; Papio, the savannah baboons; have consistently found the mangabeys to be and Theropithecus, the gelada baboon. The diphyletic, with Cercocebus and Mandrillus papionins have long been recognized as a forming a clade to the exclusion of all other monophyletic group on the basis of shared papionins (Harris, 2000). Recent studies traits including relatively flaring molars, have identified a number of features which broad nasal apertures, relatively long faces, distinguish the Cercocebus–Mandrillus clade a tendency toward terrestriality, and a (Fleagle & McGraw, 1999; Groves, 2000); diploid chromosome number of 42 (Kuhn, however the detailed similarities in cranial 1967; Hill, 1974; Delson, 1975a,b; Szalay shape between the mangabey genera have & Delson, 1979; Dutrilleaux et al., 1982; yet to be reconciled with molecular phylog- Strasser & Delson, 1987). Macaca, which enies. Because of the large size differential lacks well-developed maxillary and man- between members of the papionin molecular dibular facial fossae and is thought to retain clades, it frequently has been suggested a number of primitive cercopithecine mor- that allometric effects might account for phological features, is considered the sister homoplasies in papionin cranial shape (Shah taxon to the African papionins (Szalay & & Leigh, 1995; Lockwood & Fleagle, 1999; Delson, 1979; Strasser & Delson, 1987; Harris, 2000; Ravosa & Profant, 2000). Morales & Melnick, 1998). This relation- In an effort to circumvent certain limi- ship is confirmed by an array of molecular tations of traditional allometric studies, a evidence including immunological dis- geometric morphometric study of papionin tances, protein polymorphisms, DNA–DNA craniofacial morphology was undertaken. A hybridization, amino acid sequences, and combination of geometric morphometric, nuclear and mitochondrial genetic studies bivariate, and multivariate techniques was (Disotell, 1994; van der Kuyl et al., 1995; applied in order to identify multivariate scal- Harris & Disotell, 1998; Harris, 2000). ing patterns not discernable by conventional The resolution of phylogenetic relation- bivariate regression analysis. The objectives ships among the African papionins has been of this study were twofold. The first was to more problematic. The mangabeys were evaluate the supposition that homoplasy in often classified in a single genus, Cercocebus, papionin craniofacial shape is attributable on the basis of shared morphological to shared patterns of allometric scaling, features including moderate body size,     549

Cercocebus Papio Lophocebus Mandrillus Papio Theropithecus Mandrillus Cercocebus Theropithecus Lophocebus (a) Macaca (b) Macaca

Papio Lophocebus Theropithecus Papio Lophocebus Theropithecus Cercocebus Cercocebus Mandrillus Mandrillus (c) Macaca (d) Macaca Figure 1. Cladograms depicting alternate hypotheses of phylogenetic relationships among the Papionini. Traditional phylogenies exemplified by (a) Strasser & Delson (1987) and (b) Delson & Dean (1993) recognized the mangabey genera Cercocebus and Lophocebus as sister taxa. Molecular phylogenies, including (c) Disotell (1994) and (d) Harris & Disotell (1998), reconstruct mangabeys as diphyletic, with Cercocebus most closely related to Mandrillus. relatively short muzzles, excavated sub- the earliest protein electrophoresis and orbital fossae, and retention of a long tail immunological studies (Barnicott & Hewett- (Thorington & Groves, 1970; Hill, 1974; Emmett, 1972; Cronin & Sarich, 1976; Szalay & Delson, 1979). However, consist- Hewett-Emmett et al., 1976), analyses ent morphological and behavioral differ- of chromosome structure, amino acid ences were noted between two recognized sequences, mitochondrial and nuclear DNA species groups—a semi-terrestrial torquatus– have all linked Cercocebus and Mandrillus galeritus group and a highly arboreal to the exclusion of Lophocebus, Papio and albigena–atterimus group (Schwarz, 1928; Theropithecus (Dutrilleaux et al., 1979, 1982; Jones & Sabater Pi, 1968; Hill, 1974)— Disotell et al., 1992; Disotell, 1994; van which were sometimes accorded subgeneric der Kuyl et al., 1995; Harris & Disotell, status (Szalay & Delson, 1979). Groves 1998; Page et al., 1999; Harris, 2000). (1978) resurrected the genus Lophocebus Cladistic relationships among the latter Palmer, 1903, to receive the albigena– taxa are somewhat less clear. Trees based atterimus species group, which he diagnosed on immunological distances and certain on the basis of skeletal, behavioral, and DNA sequences (CO II and
-globin) reproductive traits. Still, Cercocebus and support a Papio–Theropithecus sister relation- Lophocebus were generally considered closely ship (Cronin & Sarich, 1976; Disotell, related (Kuhn, 1967; Szalay & Delson, 1994; Page et al., 1999). Three of the four 1979; Strasser & Delson, 1987), and many nuclear sequences (- globin intergenic phylogenetic hypotheses reconstructed the region;  1,3 GT; IRBP) analyzed by Harris mangabeys as sister taxa to the exclusion of & Disotell (1998) support a Papio– the remaining African papionins [Figure Lophocebus sister relationship. In a recent 1(a), (b)]. synthesis of published molecular data, By contrast, molecular studies have con- Harris (2000) found that both molecular sistently indicated that mangabeys are consensus and total molecular evidence diphyletic [Figure 1(c), (d)]. Beginning with trees supported the Lophocebus–Papio clade, 550 .  although a Lophocebus–Papio–Theropithecus Groves (1978) and Kingdon (1997) have trichotomy could not be rejected statisti- proposed that long faces are primitive for cally. This point of uncertainty notwith- African papionins. In this scenario, the standing, mangabey diphyly appears well Cercocebus and Lophocebus lineages would supported. have experienced parallel reductions in The obvious discrepancy between mol- facial length, with the excavated suborbital ecular and morphological classifications of fossae found in these taxa perhaps resulting the papionins has led to renewed interest in from this secondary facial shortening (Harris the behavior, ecology, reproductive biology, & Disotell, 1998; Harris, 2000). and especially the comparative morphology Allometric scaling of cranial proportions of this group. Nakatsukasa (1994, 1996) is well-documented within the Papionini. identified a number of postcranial features Freedman (1962) showed that adult facial distinguishing Cercocebus from Lophocebus, length scales positively relative to calvaria and Fleagle & McGraw (1999) established length both between males and females and that Cercocebus more closely resembles across (sub)species of Papio. He subse- Mandrillus in these same features. They also quently related differences in cranial propor- noted the presence of enlarged fourth tions among Papio varieties to clinal trends premolars in this clade in comparison with in body size (Freedman, 1963). Ontogenetic Papio and Lophocebus. Based on outgroup studies of macaques have consistently comparisons with Macaca nemestrina, they shown that males and females follow a judged the postcranial traits primitive and common trajectory characterized by positive the dental dimensions derived, and they facial allometry, negative allometry of attributed this suite of features to a shared neurocranial dimensions, and dorsal ro- ecological adaptation, namely terrestrial tation of the maxilla and palate, with foraging and hard object feeding in a tropi- sexual dimorphism between adult cranial cal forest milieu (Fleagle & McGraw, 1999). form resulting from male hypermorphosis More recently, additional qualitative cranial (MacNamara et al., 1976; Bookstein, 1985; features have been put forward as potential Cochard, 1985; Cheverud & Richtsmeier, synapomorphies of a Cercocebus–Mandrillus 1986). Comparative developmental studies clade (McGraw & Fleagle, 2000; Groves, have found Papio and Macaca to have simi- 2000). lar craniofacial growth rates and a common The marked similarities in cranial shape ontogenetic trajectory characterized by and proportion which distinguish Cerco- progressive increase in cranial base angle, cebus and Lophocebus from other African relatively rapid forward growth of the papionins have proven less tractable to muzzle, proportional increase in lower analysis, giving rise to evolutionary scenarios facial height, and decelerating neuro- invoking various combinations of primitive cranial growth (Swindler & Sirianni, 1973; retention and parallel evolution within the Swindler et al., 1973). Thus, many observed two African molecular clades. Based on out- differences in adult cranial morphologies of group comparisons, it has been suggested macaques and baboons are construed as that the moderate facial length seen in allometric consequences of Papio’s larger mangabeys—like moderate body size and absolute body size. the presence of a long tail—is primitive for It has frequently been suggested that all papionins (Disotell, 1994; Harris & allometric effects might also account for Disotell, 1998; Harris, 2000). This would homoplasies in mangabey cranial shape imply that Papio and Mandrillus experienced (Shah & Leigh, 1995; Lockwood & Fleagle, parallel increases in facial length. However, 1999; Harris, 2000; Ravosa & Profant,     551

2000). Comparing adult male body weights, permitting the simultaneous analysis of Mandrillus sphinx averages 34 kg; M. dimension and relative position, i.e., size leucophaeus, 20 kg; and Papio hamadryas and shape (Rohlf & Marcus, 1993). By subspecies range from a mean weight of relating geometrically derived shape vari- 16 kg (P. h. kindae)to31kg(P. h. anubis) ables to cranial size, it might be possible (Delson et al., 2000). By comparison, males to identify global scaling patterns not dis- of the larger Cercocebus varieties average only cernable by traditional allometric analyses. 12 kg (C. torquatus torquatus); and Lophoce- Geometric analysis has the additional bus males average no more than 9 kg (L. advantage of permitting direct visualization albigena zenkeri)(Delson et al., 2000). Given of shape trends—both allometric and this marked size difference, it is highly nonallometric—in the original specimen plausible that craniofacial similarities space, thus facilitating description of results. between like-sized members of disparate The present study applies geometric tech- papionin clades can be explained in terms of niques to the description of allometric and interspecific allometric scaling. In particular, size-uncorrelated cranial shape variation in it has been suggested that ontogenetic adult papionins. Following Cheverud’s scaling—whereby adults of papionin sister (1982) demonstration that patterns of static taxa occupy different points along a shared adult allometry cannot be assumed to reflect growth trajectory (Shea, 1985)—may be a ontogenetic processes, ontogenetic studies major factor in mangabey cranial homoplasy have come to be viewed as the allometric (Shah & Leigh, 1995). Shah & Leigh’s gold standard; however, it remains necessary (1995) initial efforts to test the hypothesis of to document patterns of adult interspecific ontogenetic scaling within the Cercocebus– allometry. Our understanding of the phylo- Mandrillus clade were inconclusive. They genetic affinities of fossil papionins such as found that Mandrillus and Cercocebus shared Parapapio and Paradolichopithecus (Szalay & a common ontogenetic trajectory for neuro- Delson, 1979; Fleagle, 1999) could be sig- cranial dimensions, but facial growth in nificantly improved by interpretation within Mandrillus more closely resembled that of the context of papionin allometric shape Papio. The authors concluded that scaling variation. But, given the rarity of adequate patterns among these taxa were complex, fossil primate ontogenetic sequences, these and that global ontogenetic scaling could forms can only be evaluated on the com- not adequately account for differences in parative basis of adult interspecific scaling cranial shape between Cercocebus and patterns. To this end, this paper documents Mandrillus. adult patterns of cranial shape variation in Minor variations in scaling patterns of papionin primates, interprets these patterns individual linear dimensions within and in light of prior studies of papionin ontogeny between cranial regions can unnecessarily and phylogeny, and considers their impli- complicate interspecific allometric compari- cations for the development and evolution of sons. By design, linear measures reduce papionin cranial form. complex spatial relationships to unidimen- sional values lacking geometric context. The Materials and methods resulting atomization of form can generate apparently contradictory scaling patterns in Data collection what are, by definition, developmentally The sample comprised 238 adult indi- integrated morphologies. By contrast, viduals from all six extant papionin genera landmark-based geometric morphometric (Table 1). The sample was largely limited analysis preserves spatial relationships, to wild-shot adult individuals of known 552 . 

Table 1 Study sample

n Taxon Female Male Collection*

Cercocebus galeritus agilis 10 7 AMNH Cercocebus torquatus torquatus 6 13 AMNH PCM Lophocebus albigena johnstoni 12 21 AMNH Macaca fascicularis 17 26 AMNH UCMVZ Mandrillus leucophaeus 8 19 BMNH FMNH FSM Mandrillus sphinx 8 13 AMNH BMNH FSM PCM Papio hamadryas anubis 21 41 AMNH FMNH NMNH UCMVZ Theropithecus gelada 4 11 AMNH FMNH LHES NMNH

*Collection abbreviations: AMNH=American Museum of Natural History; BMNH=British Museum (Natural History); FMNH=Field Museum of Natural History; FSM=Senckenberg Natural History Museum—Frankfurt; LHES= Laboratory for Human Evolutionary Studies—UC Berkeley; PCM=Powell–Cotton Museum; NMNH=National Museum of Natural History; UCMVZ=University of California Museum of Vertebrate Zoology.

provenience. However, given the scarcity of Silicon Graphics O2 workstation using Theropithecus gelada in museum collections, dedicated software combining UNIX and four zoo specimens (two male, two female) Matlab 4.2c routines (Frost et al., in prep.). lacking obvious pathology and judged to This dorsal–ventral landmark registration present normal, ‘‘wild-type’’ morphology (DVLR) procedure allows all regions of were included in the sample. the skull to be digitized without the use Data consisted of three-dimensional of cumbersome mounting equipment. cranial landmarks recorded using a Micro- Following Frost et al. (in prep.), eleven scribe 3-DX digitizer and InScribe-32 soft- midsagittal and 17 bilateral landmarks were ware (Immersion Corp., San Jose, CA). recorded, yielding a maximum of 45 land- This study was conducted in collaboration marks for each specimen (Figure 2, Table with the Morphometrics Research Group of 2). At present, many geometric morpho- the New York Consortium in Evolutionary metric programs are unable to accommo- Primatology, and cranial landmark data date missing data. Where specimens are were collected by several observers under a missing landmarks, whether due to ante- common protocol developed by Frost et al. mortem pathology or postmortem damage, (in prep.). Each skull was first mounted to it is necessary either to exclude the specimen provide access to its dorsal aspect and osteo- from analysis or to reconstruct the missing metric landmarks recorded followed by four data. For specimens with localized damage, arbitrarily chosen, noncoplanar, noncol- missing values for paired landmarks can be linear registration landmarks. The skull was estimated by ‘‘reflecting’’ the corresponding then remounted to gain access to its ventral landmarks from the opposite side to produce aspect and the remaining landmarks were complete configurations. Specimens with recorded along with the same four regis- missing data were read into GRF-ND (Slice, tration landmarks. The registration land- 1999) and Bookstein shape coordinates marks were used to align the dorsal and (Bookstein, 1991) were computed relative ventral aspects of the skull within a common to an inion–prosthion baseline using bregma coordinate system, yielding a complete con- as the third landmark and invoking the figuration. Realignment was performed on a ‘‘No Scale’’ option to preserve the original     553

Figure 2. Osteological landmarks used in this study mapped on to a representative papionin skull (female Macaca fascicularis). Landmarks are defined following Frost et al. (in prep.); abbreviations follow Table 2. Line drawings of female Macaca fascicularis skull courtesy of J. Michael Plavcan ( J. M. Plavcan) and adapted with artist’s permission. specimen scale. This procedure oriented place all observations in a common frame of each specimen in a coordinate system with reference, and the Euclidean distance of the Z-coordinate axis perpendicular to the each landmark to its respective centroid was specimen mid-sagittal plane and the origin computed. For each observer, landmark located on the specimen midline at inion. deviations were calculated relative to the Coordinates for each missing landmark were observer landmark mean. Mean deviations then taken from those of its antimere by and percentage errors were calculated for reversing the sign of the Z-coordinate. The individual landmarks and subsequently large number of specimens with damage in averaged to give a mean deviation and per- the region of Basion, an unpaired landmark, centage error for each observer across all necessitated its exclusion, leaving a total of landmarks (Table 3). One-way analysis of 44 landmarks for analysis. variance (ANOVA) was conducted for each landmark by observer, and the root mean Precision studies squares were examined (Table 4). In the Data used in this study were collected by context of this analysis, the root of the three observers working under a common within-groups mean squares (root mean data collection protocol. To examine the square error) corresponds to intraobserver effects of intra- and interobserver error, each error (Sokal & Rohlf, 1981), while the root observer collected multiple observations of a of between-groups mean squares corre- single specimen, a male P. hamadryas ursinus sponds to interobserver error. Intraobserver cranium. Raw landmark data were subjected error does not exceed 0·33 mm or 2%. to generalized Procrustes analysis (GPA) Interobserver error averages approximately using GRF-ND (Slice, 1999) in order to 1 mm, again less than 2%, and even the 554 . 

Table 2 Osteological landmarks landmark configurations are scaled to unit centroid size and optimally superimposed so Landmark Abbreviation as to minimize summed squared distances across all landmarks and specimens relative Midsagittal Inion IN to a reference configuration, the Procrustes Bregma BR mean (Slice et al., 1996). Figure 3 shows the Glabella GL Procrustes superimposition of all 238 speci- Nasion NA ff Rhinion RH mens in dorsal view. Di erences between Nasospinale NS forms, indicated by the point scatters at each Prosthion PR landmark, represent pure shape variation. It Opisthion OP should be noted that, by scaling all speci- Basion BA Staphylion ST mens to unit centroid size, the Procrustes Incisivion IV procedure corrects for gross size effects, i.e., Bilateral scale, in a manner analogous to traditional Prosthion-2 PR2 bivariate ratios. But, as with ratios, Pro- 3 Mesial P MP3 crustes analysis does not correct for allo- M1–M2 Contact M12 Distal M3 DM3 metric effects. Therefore, the shape variation Premaxillary suture–inferior PMI summarized by the Procrustes-aligned co- Premaxillary suture–superior PMS ordinates may include both size-correlated, Zygomaxillare inferior ZMI Zygomaxillare superior ZMS i.e., allometric, and size-uncorrelated Dacryon DAC components. Midtorus inferior MTI Procrustes-aligned specimens may be Midtorus superior MTS Frontomalare orbitale FMO represented as points in a curvilinear mor- Frontomalare temporale FMT phospace of dimension 3p–7 for p three- Zygotemporale superior ZTS dimensional landmarks (Dryden & Mardia, Zygotemporale inferior ZTI 1998; Rohlf, 1999a). Because this morpho- Porion POR Postglenion PGL space is non-Euclidean, statistical analysis is conducted using the orthogonal projection Osteological landmarks used in the present study. of points onto a Euclidean space set tangent Landmarks are defined following Frost et al. (in prep.) to shape space at the Procrustes mean and are illustrated in Figure 2. (Dryden & Mardia, 1998; Rohlf, 1999a). In practice, if shape variation is sufficiently most imprecise observations do not exceed small in the vicinity of the reference 5% error. While average interobserver error form, the Procrustes-aligned coordinates are exceeds intraobserver error by approxi- a reasonable approximation of tangent mately 0·66 mm, average percentage errors space coordinates (Dryden & Mardia, 1998; are comparable within and between ob- Rohlf, 1999a). This assumption may be servers. Given the relatively large size of the tested using tpsSmall (Rohlf, 1999b), soft- primate crania in this study, these margins ware which computes the ordinary least of error were considered acceptable. squares regression (through the origin) of Euclidean (tangent space) distances versus Procrustes analysis the corresponding Procrustes (morpho- Raw landmark data were subjected to a space) distances for all possible specimen generalized Procrustes analysis (GPA) using pairs. Analysis of the present data set the Morpheus et al. morphometrics package showed a virtual one to one correspondence (Slice, 1998). GPA is an iterative least between the Procrustes and tangent squares procedure in which individual spaces distances (r=0·9999, slope=0·9967)     555

Table 3 Observer mean deviation and mean percentage error across landmarks

Mean deviations % Errors Observer n Min Max Mean Min Max Mean

1 10 0·07 0·54 0·24 0·07 1·00 0·42 2 8 0·06 0·55 0·16 0·06 1·04 0·26 3 6 0·05 1·42 0·25 0·07 1·77 0·40

Landmark mean deviations are computed as the mean of the absolute deviations of  observations from the landmark mean [ABS(xi x¯)]; values are reported in milli- meters. Landmark percentage error is calculated as the landmark deviation expressed   as a percentage of the landmark mean [ABS(xi x¯)/x¯] 100. Observer mean devi- ations and observer mean percentage errors are calculated as the mean value across all landmarks by observer.

Table 4 Inter- and intraobserver mean errors across landmarks

RMSE % RMSE Level Min Max Mean Min Max Mean

Intraobserver 0·10 1·10 0·31 0·10 1·47 0·51 Interobserver 0·04 2·81 1·05 0·32 4·70 1·70

Root mean square error (RMSE) is calculated as the root of the within-groups (intraobserver) or between-groups (interobserver) mean sums of squares for ANOVA of landmark distances by observer; values are reported in millimeters. Percentage root mean square errors (% RMSE) are calculated relative to the landmark grand mean as [RMSE/Xz ]100. Mean RMSE and % errors are calculated as the mean value across all landmarks.

Principal components analysis Landmark-based morphometrics involves large numbers of statistically interdependent and partially redundant variables. Pro- crustes superimposition—through the con- straints of translation, rotation, and unit scaling—results in the loss of additional degrees of freedom (Dryden & Mardia, 1998). Principal components analysis Figure 3. Dorsal view of Procrustes superimposition of (PCA) of the Procrustes-aligned coordinates 238 papionin crania. Specimens have been scaled to corrects for these spurious dimensions by unit centroid size and optimally superimposed. In reducing the data to a full-rank matrix, theory, all remaining differences between forms, indi- cated by point scatters at each landmark, are due to namely the principal component scores for pure shape variation. axes corresponding to nonzero eigenvectors (Rohlf, 1999a). This procedure both gen- erates a reduced number of statistically indicating that the Procrustes-aligned co- uncorrelated summary shape variables and ordinates are a good approximation for ordinates specimens relative to the major tangent space coordinates. axes of shape variation (Dryden & Mardia, 556 . 

Table 5 PCA of Procrustes-aligned coordinates separates males and females within genera (see below), corresponds to Principal Com- Component Eigenvalue Proportion Cumulative ponent 5 of the initial analysis including all genera. 1 0·01090 0·667 0·667 2 0·00121 0·074 0·741 3 0·00088 0·054 0·794 Regression analysis 4 0·00050 0·030 0·825 To identify allometric effects, principal 5 0·00040 0·024 0·849 6 0·00022 0·014 0·862 component scores were tested for significant 7 0·00018 0·011 0·874 linear relationships with size, represented 8 0·00016 0·010 0·884 here by cranial centroid size. Centroid size is 9 0·00014 0·009 0·892 defined as the square root of the sum of 10 0·00011 0·007 0·899 squared distances of a set of landmarks from Principal Components 1–10 account for approxi- their centroid (Slice et al., 1996); compu- mately 90% of total variance. Principal components 11 tationally, it falls in the class of Mosimann and higher each account for less than 1% of total size variables (Mosimann & Malley, 1979). variance. Centroid size is the preferred size metric for Procrustes-based geometric morphometric 1998). Principal components analysis was analysis (Bookstein, 1996), both because it performed on the covariance matrix of the is the size measure upon which the compu- Procrustes-aligned coordinates using SAS tation of Procrustes distance is based and 6.12 for Windows (SAS Institute, Cary, NC). because it is approximately uncorrelated Inspection of PCA results (Table 5) showed with all shape variables when assumptions of the first principal component to account for homogenous spherical landmark variance fully 67% of total shape variance. Cumu- are met (Slice et al., 1996). In the context of latively, the first ten principal components this study, cranial centroid size provides a accounted for 90% of total variance, while reasonable estimate of cranial size and, given the contributions of individual higher order the scarcity of individual body mass data components were negligible. or associated postcrania, the best available Because principal components analysis surrogate for body size. orients successive components in the Principal component scores were plotted direction of maximum variation (Neff & against log centroid size, Pearson product Marcus, 1980), a single divergent form can moment correlations were computed, and define the extremes of shape variation on regression analyses were performed. As both multiple components, obscuring possible dependent and independent variables were diferences among the remaining taxa. functions of landmark coordinates measured Given the focus of this study on relation- with error, a Type II regression analysis was ships among the mangabeys, baboons, and performed (Sokal & Rohlf, 1981). Reduced mandrills, the inclusion of Theropithecus, major axis (RMA) regression equations which exhibits a unique and highly derived were calculated and pairwise tests for cranial morphology (Szalay & Delson, 1979; homogeneity of slope and elevation were Fleagle, 1999) was found to be counter- performed across genera using Cole’s productive, and principal components were NEWRMA program (Cole, 1996). This recomputed excluding Theropithecus. This program calculates Clark’s (1980) test for had no effect on principal component homogeneity of slope and performs the ordinations, but it did result in a slight nonparametric quick test for differences reordering of the principal component axes in elevation across all pairs of genera such that Principal Component 3, which (Tsutakawa & Hewett, 1977). It also     557 generates bootstrap confidence intervals Visualization for between-group differences in slope and Visualization of shape variation along elevation at the sample grand mean. selected principal component axes was per- formed using Morphologika (O’Higgins & Jones, 1999). Mean male and mean female Influential landmarks configurations were computed for each In classic principal components analysis, taxon using backscaled Procrustes-aligned influential variables are identified by inspec- coordinates, thus summarizing average tion of eigenvectors, with large positive or shape and size for each taxon. Mean forms negative coefficients indicating greater were realigned and subjected to principal influence (Neff & Marcus, 1980). In three- components analysis as above (O’Higgins & dimensional morphometric studies, each Jones, 1999). Inspection of the resulting landmark is represented by three variables, principal component axes showed that the X, Y, and Z coordinates, complicating principal component ordinations of mean the interpretation of eigenvectors and mak- forms corresponded closely to those based ing it difficult to assess the influence of on individual specimens. The ‘‘Explore individual landmarks. To circumvent this Shape Space’’ feature was then used to difficulty, it was convenient to represent graphically explore shape variation along each landmark by a single variable. Thus, selected axes (O’Higgins & Jones, 1999). Procrustes-aligned coordinates were used to Shape variation along a principal com- compute the Euclidean distance of each ponent axis is visualized by adjusting the landmark to the common centroid. This coordinates of the Procrustes mean form yielded 44 distance variables, one per by the coefficients of the corresponding landmark, for each specimen. Principal eigenvector. By generating a series of such components analysis was performed on the forms, each corresponding to a different covariance matrix of these distance variables point along the axis, Morphologika can using SAS 6.12 for Windows (SAS Institute, ‘‘morph’’ the mean form, displayed as a Cary, NC). Principal components based on wireframe diagram, along an axis, thus distances accounted for virtually identical visualizing shape variation summarized by proportions of the total shape variance and that component (O’Higgins & Jones, 1999). produced ordinations similar to those based on aligned coordinates. Having established Canonical variates analysis the comparability of the two analyses, eigen- As an alternate approach to evaluating the vectors from the PCA of distances were size-uncorrelated component of papionin examined. Inspection of eigenvectors cranial shape variation, a canonical variates showed coefficients in the range of 0·40, analysis was employed. Procrustes-aligned with most landmark coefficients in the coordinates were regressed against log cen- range of 0·15. With few exceptions, troid size and the residual values, hereafter paired landmarks showed coefficients of referred to as ‘‘size-adjusted coordinates’’, the same sign and similar magnitude, but were subjected to canonical discriminant values for paired landmarks (right and left) analysis using SAS 6.12 (SAS Institute, tended to diverge as the absolute magnitude Cary, NC). Mahalanobis distances were of coefficients decreased. Based on this corrected for unequal sample sizes and the pattern, landmarks or landmark pairs with large number of variables using the formula coefficient absolute values d0·15 were for unbiased Mahalanobis distance of identified as influential for the component in Marcus (1993). Similarly, significance levels question. for the Mahalanobis distances were adjusted 558 . 

0.2

0.1

0.0 Principle Component 2 –0.1 Cercocebus Lophocebus Macaca Mandrillus Papio Theropithecus

–0.2 –0.2 –0.1 0.0 –0.1 0.2 Principle Component 1 Figure 4. Plot of Principal Component 1 vs. Principal Component 2 based on PCA of Procrustes-aligned coordinate data. Principal Component 1 separates specimens into large-bodied and small-bodied groups, while Principal Component 2 distinguishes genera within the two size groups. to account for multiple comparisons Principal Component 1 was found to be (Marcus, 1993). The resulting distance highly significantly correlated with log matrix was examined to assess the pattern centroid size across all papionins (Pearson’s and magnitude of inter-group distances and r=0·96, P<0·0001), and Figure 5 demon- the canonical variates were plotted. strates a strong linear relationship between these variables across genera. This implies that PC 1 largely summarizes size-correlated Results cranial shape variation and establishes that Scaling relationships allometric scaling is present. The first principal component summarizes Table 6 shows coefficients for the 67% of total shape variation and distin- reduced major axis regression of Principal guishes large-bodied papionins—Papio, Component 1 on log centroid size across all Mandrillus, and Theropithecus—from the papionins and by genus. Within-genus re- smaller taxa (Figure 4). It is common in lationships are weaker than those for the biological studies for the first principal com- pooled sample, with r2 values ranging from ponent to be interpreted as ‘‘size’’ (Neff & 0·68 for Theropithecus to 0·87 for Papio. Marcus, 1980); however, as previously Inspection of Figure 5 suggests that the noted, all specimens were scaled to unit pooled sample regression line is a reasonable size during the initial Procrustes analysis. estimator of genus slopes but not elevations. Nevertheless, PC 1 clearly summarizes To test this impression, the pooled sample differences in shape between large- and regression coefficients were treated as small-bodied papionins, respectively. known values and compared to those for     559

0.20 y = 0.399x -1.371 0.15 r2 = 0.92

0.10

0.05

0.00

–0.05 Principle Component 1 –0.10 Cercocebus Lophocebus Macaca Mandrillus –0.15 Papio Theropithecus

–0.20 2.75 3.003.25 3.50 3.754.00 4.25 Log Centroid Size Figure 5. Reduced major axis regression of Principal Component 1 on log centroid size. The strong linear relationship between PC 1 and log centroid size confirms the presence of allometric scaling for aspects of cranial shape summarized by this component. There is considerable homogeneity of slopes among papionin genera but significant differences in elevation are observed.

Table 6 Reduced major axis regression coefficients for PC 1 on log centroid size across papionins and by genus

Slope 95% CI† Intercept 95% CI† r2

All Papionins 0·399 0·385 to 0·413 1·371 1·422 to 1·321 0·918 Cercocebus 0·402 0·361 to 0·455 1·410* 1·584 to 1·277 0·765 Lophocebus 0·470 0·390 to 0·549 1·628* 1·884 to 1·372 0·702 Macaca 0·367 0·319 to 0·411 1·236* 1·376 to 1·089 0·822 Mandrillus 0·317 0·280 to 0·549 1·062 1·210 to 0·927 0·821 Papio 0·322 0·292 to 0·347 1·085 1·175 to 0·974 0·872 Theropithecus 0·313 0·228 to 0·445 1·081 1·557 to 0·776 0·682

Genus slopes are not significantly different from the pooled papionin slope using the single-sample test of Clarke (1980). *Elevations significantly different from the pooled papionin line (Bonferroni adjusted P=0·05) using a modified quick test (Tsutakawa & Hewett, 1977) as follows: (1) under the null hypothesis that the genus elevation is equal to the pooled sample elevation, the prior probabilities of an individual case falling above or below the pooled regression line should be equal (p=q=0·5); (2) cases falling above and below the pooled sample line were tallied; and (3) the binomial probability of the resulting distribution was determined and the null hypothesis accepted or rejected accordingly. †Bootstrap estimates of 95% confidence intervals generated by NEWRMA (Cole, 1996). individual genera (see Table 6). Compari- nificant differences from the common sons of individual genus slopes to that for regression slope (Bonferroni adjusted the pooled sample found no statistically sig- P=0·05). In comparison with the pooled 560 . 

Table 7 Pairwise comparisons of reduced major axis regression lines for PC 1 on log centroid size

Cercocebus Lophocebus Macaca Mandrillus Papio Theropithecus

Cercocebus — NS/NS NS/† NS/† NS/† NS/† Lophocebus NS/NS — NS/† †/† NS/† NS/NS Macaca NS/* */* — NS/NS NS/NS NS/† Mandrillus */* */* NS/NS — NS/NS NS/† Papio */* */* NS/NS NS/NS — NS/† Theropithecus NS/NS */NS NS/* NS/* NS/* —

Results of Clarke’s (1980) test for homogeneity of slope and the quick test for homogeneity of elevations (Tsutakawa & Hewett, 1977) are shown above the diagonal as slope/elevation, with significance levels adjusted for multiple comparisons. Results for bootstrap analysis (3000 replicates) of intergroup differences in slope and elevation at the pooled-sample grand mean are shown below the diagonal as slope/elevation; significance levels are not adjusted for simultaneous multiple comparisons. NS not significant at Bonferoni adjusted P=0·05; NS not significant at unadjusted P=0·05; †significant at Bonferoni adjusted P=0·05; *significant at unadjusted P=0·05. sample line, Cercocebus, Lophocebus, and and Mandrillus. Regression elevations for the Macaca had highly significantly differ- mangabeys are clearly significantly different ent elevations (Bonferroni adjusted from those of Papio and Mandrillus.In P<<0·001), while the remaining taxa were summary, the papionins show substantial not significantly different. uniformity in the scaling of Principal While the pooled sample regression line Component 1 with respect to log centroid describes a general papionin allometric size overall, but both mangabey genera dis- trend, pairwise testing of regression coef- play significant differences in their scaling ficients reveals statistically significant differ- patterns from the remaining papionins. ences in scaling patterns between genera Principal Components 2 and higher are, (Table 7). Four of the six papionin by definition, uncorrelated with PC 1 (Neff genera—Macaca, Mandrillus, Papio and & Marcus, 1980), and were generally un- Theropithecus—show a common slope for correlated with size. Only PC 5 (analysis Principal Component 1 against log centroid including Theropithecus) was significantly, size. Macaca, Papio and Mandrillus also albeit weakly, correlated with log centroid share a common elevation from which size (r=0·16, P=0·01); however, a bivariate Theropithecus may be offset. The slope for plot of PC 5 against log centroid size (Figure Cercocebus is intermediate between those of 6) revealed linear relationships between Lophocebus and Macaca and is not sig- these variables within genera and within- nificantly different from either taxon; its genus correlation coefficients greater than elevation is likewise intermediate and indis- 0·5 (range 0·52–0·90). Principal Compo- tinguishable from that of Lophocebus but nent 5 separates sexes within genera (see differs significantly from Macaca. Results of below), and the strongest correlations slope comparisons between the mangabeys between PC 5 and size were observed in the and the remaining papionin genera are most dimorphic genera. This could imply contradictory. Under Clarke’s test, only that PC 5 summarizes genus-specific allo- Lophocebus shows a significantly different metric effects different from those sum- slope from any other papionin genus, marized by PC 1. Unfortunately, in highly namely Mandrillus. Bootstrap estimates find size-dimorphic taxa, any shape difference both Cercocebus and Lophocebus to have between the sexes will be correlated with significantly different slopes (unadjusted size whether arising from allometric pro- P=0·05) from the large-bodied taxa, Papio cesses or not. Given the relative weakness of     561

0.06

0.04

0.02

0.00

–0.02

–0.04 Principle Component 5 Cercocebus r2 = 0.34 –0.06 Lophocebus r2 = 0.28 Macaca r2 = 0.58 Mandrillus r2 = 0.81 –0.08 Papio r2 = 0.58 Theropithecus r2 = 0.64

–0.10 2.75 3.003.25 3.50 3.754.00 4.25 Log Centroid Size Figure 6. Plot of Principal Component 5 (analysis including Theropithecus) against log centroid size. PC 5 is significantly correlated with log centroid size within genera and separates males and females. As indicated by the r2 values, this effect is more pronounced in the larger-bodied and most highly sexually dimorphic genera. the observed correlations, it is likely that similar to the combined-sex analysis with PC 5 incorporates both size-correlated and only minor differences in significance levels, size-independent shape variation. all easily attributable to the smaller single- Because of concerns that within-taxon sex sample sizes. In light of these results, it effects might influence interpretations of was concluded that single-sex analysis con- between-group shape variation, separate tributed nothing to the understanding of principal components analyses were con- shape variation among genera and precluded ducted for males and females, respectively, the examination of sexual shape dimorphism and relationships of the resulting principal within genera. Thus, results for combined- components with centroid size were exam- sex analyses are presented below. ined. This procedure had the effect of gen- erating higher-order principal components Shape trends and influential landmarks uncorrelated with centroid size, thus achiev- Figure 7 illustrates the shape differences ing a more rigorous statistical partition of summarized by Principal Components 1–5 shape variation into size-correlated and (analysis excluding Theropithecus). It must size-uncorrelated components. However, be emphasized that, while shape trends the resulting analyses produced principal along principal component axes frequently component ordinations virtually identical correspond with observed morphologies, to those for the combined-sex analysis. they do not represent the actual physical Between-genus comparisons of regression appearance of specific animals. Rather, the lines for PC 1 on centroid size were likewise wireframe diagrams illustrate morphometric 562 . 

Figure 7. (a to c).     563

Figure 7. (d to f). 564 . 

Table 8 Influential landmarks for Principal Components 1–5

PC Positive coefficients Negative coefficients

1 IN, BR, OP, PGL RH, NS, PR, IV, PR2, MP3, PMI 2 GL, NA, DAC, MTI, MTS IN, RH, OP, ST, IV, POR 3 IN, BR, GL, NA, OP, IV, PMS, DAC FMT, ZTS, ZTI 4 IN, BR ZMS, DAC 5 BR, ZMI, MP3 RH, PMS, MTS, ZTI

Influential landmarks and landmark pairs (right and left) are defined as those with absolute coefficients d0·15 for the principal component in question (see text). Figure 8 maps influential landmarks for each component onto a representative papionin skull. Landmark abbreviations follow Table 2. trends along a subset of all possible axes of landmarks of the neurocranium and anterior shape variation. In the following discussions, rostrum [Figure 8(a)]. It is tempting to when a taxon is characterized as having a construe this pattern as signifying ‘‘forward particular trait, it is always relative to all movement’’ of the anterior muzzle and other taxa and with reference to the shape ‘‘contraction’’ of the neurocranium, but it component in question. Table 8 summarizes is ill-advised to give these landmark maps the influential landmarks which drive shape simple, mechanistic interpretations. Instead, trends along Principal Components 1–5, each is best read conservatively as denoting and Figure 8 displays the corresponding regions of greatest morphological variation landmark maps. and, therefore, biological interest. As previously noted, the first principal Principal Component 2 distinguishes component [Figure 7(a)] separates the Macaca and Papio, which exhibit relatively papionin genera by size, with Papio, negative scores, from all other papionins Mandrillus, and Theropithecus (where [Figure 7(b)]. Visualizations show the included) showing large positive scores, former taxa to be relatively klinorhynch, while Cercocebus, Lophocebus, and Macaca showing prominence of the interorbital and have negative scores. The large-bodied taxa supraorbital regions and a ventral deflection are characterized by relatively small and low of the muzzle. By contrast, the remaining neurocrania; relatively small orbits and cor- papionins show a more dorsally oriented respondingly short upper faces; and long, face, producing a straighter profile and less somewhat more dorsally oriented muzzles. projecting superior orbital margins. Princi- Small-bodied taxa exhibit relatively large, pal Component 2 is influenced by rhinion globular neurocrania; large orbits and and landmarks of the ventral neurocranium relatively tall upper faces; and shorter, more and palate, which show strong negative coef- ventrally oriented muzzles. Consistent with ficients, with positively weighted landmarks this pattern, Principal Component 1 was in the interorbital region and along the found to be most strongly influenced by supraorbital margins [Figure 8(b)].

Figure 7. Visualization of shape variation along Principal Components 1–5 (a)–(e). All plots show Principal Component 1 on the X-axis. Wireframe diagrams (frontal and lateral views) illustrate the extremes of shape variation summarized by a given axis (target axis indicated by double-headed arrow). These diagrams represent the transformation of the Procrustes mean form to the maximum and minimum axis values (indicated by single-headed arrows) with the other axis held constant at zero. Data points represent mean male and female forms for each taxon and indicate their positions relative to shape trends defined by each axis.     565

Principal Component 3 (analysis exclud- malar region; and a broader and somewhat ing Theropithecus) separates males, with more parabolic palate. Principal Com- relatively positive scores, from females, ponent 5 is most strongly influenced by which exhibit relatively negative scores bregma and landmarks bracketing the [Figure 7(c)]. This component corresponds maxilla with positive coefficients, while to Principal Component 5 of the original landmarks of the anterior nasal region, analysis and is similarly correlated with log supraorbital margin and zygomatic arch centroid size. Relative to conspecific males, show negative coefficients [Figure 8(e)]. females show more globular neurocrania, relatively larger orbits, a more parabolic Canonical variates analysis palate outline, and narrow zygomatics. The first three canonical variates account Males have lower neurocrania, relatively for 56, 25 and 19% of total among-group smaller orbits, a more parallel-sided palate, variance, respectively for a cumulative total and flaring zygomatics. Principal Com- of over 99%. The fourth canonical variate, ponent 3 is most strongly influenced by which separates males from females, landmarks of the neurocranium and inter- accounts for less than 1% of total variance orbital and supraorbital regions, which and is not statistically significant. Table 9 show positive coefficients, with nega- shows Mahalanobis distances between tively weighted landmarks bracketing the genera; all distances are highly significant zygomatics [Figure 8(c)]. (Bonferroni adjusted P=0·001). Papio con- Principal Component 4 distinguishes sistently showed the smallest distances to Macaca and female Mandrillus from Papio, other groups; Lophocebus, the largest. with the remaining groups occupying Lophocebus showed the smallest distance intermediate positions along this axis to Papio; Cercocebus was next closest to [Figure 7(d)]. Visualizations show the Lophocebus, followed by Mandrillus, and former taxa to be characterized by relatively Macaca. Cercocebus, too, had its smallest tall orbits and posteriorly positioned zygo- distance to Papio, with Mandrillus, Lopho- matic roots. At the opposite extreme, Papio cebus, and Macaca increasingly more distant. exhibits relatively short orbits, a deeper Similarly, Macaca and Mandrillus were each zygomatic, and anteriorly positioned zygo- closest to Papio, and markedly more distant matic roots. Only four influential landmarks from the mangabeys. Papio was least distant were identified for Principal Component 4, from Macaca and farthest from Lophocebus. with inion and bregma having large posi- Notably, Cercocebus and Lophocebus are quite tive coefficients and dacryon and zygo- distant from each other, as are Papio and maxillare superior large negative coefficients Mandrillus. [Figure 8(d)]. Figure 9 shows a three-dimensional plot Principal Component 5 separates Lopho- of the first three canonical axes. Canonical cebus and Cercocebus, while all other taxa Variate 1 separates Macaca from Lophocebus, fall close to the origin. Lophocebus is with Papio, Mandrillus, and Cercocebus characterized by a relatively low and long intermediate. Canonical Variate 2 contrasts neurocranium; supraorbital margins high Papio and Mandrillus. Canonical Variate 3 and arched; elongated and narrow nasals; a separates Lophocebus from Cercocebus.As relatively narrow malar region; and a narrow might be predicted from the Mahalanobis palate [Figure 7(e)]. By contrast, Cercocebus distances, Papio and Macaca show the most shows a shorter and higher neurocranium; similar pattern of residual shape variation supraorbital margins low and relatively with respect to the canonical axes. Cerco- straight; shorter, broader nasals; a broader cebus and Mandrillus show some similarities, 566 . 

Figure 8. (a to c).     567

Figure 8. (d and e). Figure 8. Maps of influential landmarks for Principal Components 1–5 (a)–(e). Maps based on PCA of landmark distances (excluding Theropithecus). Influential landmarks (Table 8) are defined as those with absolute coefficients d0·15 for the principal component in question (see text). These landmarks identify regions of greatest morphological variability and contribute disproportionately to shape trends summarized by the corresponding principal component (see Figure 7). Line drawings of female Macaca fascicularis skull courtesy of J. Michael Plavcan ( J. M. Plavcan) and adapted with artist’s permission. both relative to the canonical axes and to shown) confirms that Mandrillus is most Papio, but superimposition of a minimum similar to Macaca. Lophocebus is widely spanning tree on the canonical clusters (not separated from all other groups. 568 . 

Table 9 Mahalanobis distances between papionin genera

Cercocebus Lophocebus Macaca Mandrillus Papio

Cercocebus — 16·64 20·99 15·00 14·07 Lophocebus 10·01 — 24·51 17·79 15·85 Macaca 12·85 15·07 — 13·45 11·60 Mandrillus 9·02 10·80 8·04 — 14·31 Papio 8·46 9·59 6·88 8·66 —

Mahalanobis distance values (D) are shown above the diagonal; unbiased

Mahalanobis distance values (Du)—corrected for unequal sample sizes and the large number of variables—are shown below the diagonal. All distances are significant at 2 Bonferroni adjusted P=0·001. The unbiased squared Mahalanobis distance Du is computed as:

where N=total sample size; g=number of groups; p=number of variables; and n1 and n2 are the sample sizes of the groups under comparison (Marcus, 1993).

15

10

5

0 Cercocebus Lophocebus –5 Macaca Mandrillus Papio

–10 Canonical Variate 2 Variate Canonical –15

–20 15 20 10 15 Canonical5 Variate 1 10 5 0 0 –5 –5 –10 –10 –15 –15 Canonical Variate 3 Figure 9. Three-dimensional canonical plot based on CVA analysis of size-adjusted landmark coordinates. Macaca and Papio show the most similar pattern of residual shape variation with respect to the canonical axes. Lophocebus is widely separated from all other taxa, including Cercocebus.

Discussion and conclusions advantage of the complementary infor- Combining geometric morphometric tech- mation these methods provide. Principal niques and traditional bivariate and multi- components analysis of aligned coordinate variate statistics, the present study takes data serves the prosaic functions of data     569 reduction and ordination of specimens and animals and possibly Macaca. Results for permits a rough partition of total shape Lophocebus are the most ambiguous. It variation into size-correlated and size- clearly shares a common slope and elevation uncorrelated moieties. Traditional regres- with Cercocebus. Like Cercocebus, it may also sion analysis of morphometrically-derived share a common slope with Macaca, Papio, size and shape variables simplifies the com- and Theropithecus, but not Mandrillus.Inany parison of multivariate allometric relation- case, the mangabeys share a common scal- ships across and among groups, while ing pattern to the exclusion of the remaining Mahalanobis distances and canonical plots papionins. summarize patterns of overall morphological Strictly defined, ontogenetic scaling similarity when size effects are controlled. occurs when observed differences in shape Direct visualization of shape components are ‘‘produced or accompanied by extension allows exploration of allometric shape trends or truncation of common (or ancestral) and patterns of residual shape variation, growth allometries’’ (Shea, 1985:179). A while the corresponding landmark maps finding that adults of closely related species localize shape variation to specific regions of share common allometric patterns is often the skull. indicative of the presence of ontogenetic scaling but never, in itself, conclusive. The Allometric effects present finding of a shared adult allometric Principal Component 1, which summarizes scaling pattern for Macaca and Papio is 67% of total cranial shape variation, is wholly consistent with previous growth highly significantly correlated with cranial studies reporting ontogenetic scaling for size. Thus, craniofacial allometry is present these taxa (Swindler & Sirianni, 1973; in the Papionini; however the precise nature Swindler et al., 1973; Profant, 1995). The of scaling relationships among papionin taxa presence of the same allometric pattern in is complex. Parametric and nonparametric Mandrillus and possibly Theropithecus raises tests for homogeneity of slopes and inter- the possibility that the aspects of cranio- cepts produced broadly similar results, but facial shape summarized by Principal inconsistencies were observed between Component 1 have a common ontogenetic different tests and significance levels were basis in all large-bodied papionins as well as often borderline making some results incon- macaques. Although similar adult inter- clusive. Pairwise comparisons of regression specific scaling patterns may be produced coefficients showed that Macaca, Papio, by functional allometry (Jim Cheverud, Mandrillus, and Theropithecus share a com- personal communication), the prevalence of mon slope for PC 1 on log centroid size. ontogenetic scaling among catarrhine pri- Macaca, Papio and Mandrillus also share a mates renders it the most plausible expla- common elevation, and thus fall on a com- nation for the observed similarities among mon line from which Theropithecus may or adult static allometries. may not be vertically transposed. In the While cranial developmental patterns of latter case, results of the quick test and Macaca and Papio have been intensively bootstrap were contradictory, due in part to studied, ontogenetic trends among the the small sample size and relatively low r2 remaining papionin taxa are less well estab- values for Theropithecus. Larger samples will lished. Profant (1995) found that papionins, be required to adequately assess scaling pat- including mangabeys, conformed closely terns for this taxon. Cercocebus also shares to ontogenetic trajectories established for the common papionin slope; however, its Macaca. However, Shah & Leigh (1995) elevation differs from the large-bodied reported incongruent ontogenetic scaling 570 .  patterns among Cercocebus, Papio, and These results are not surprising given Mandrillus, and Collard & O’Higgins (2000, the extensive literature documenting 2001) describe heterogeneity of multivariate mammalian cranial scaling patterns in growth vectors among African papionins. general, and primate cranial scaling in par- The present study finds significant differ- ticular. Cranial allometry characterized by ences in patterns of adult static allometry positive facial scaling and changes in facial between the mangabeys and the large- orientation is observed across varying time- bodied papionins in that Cercocebus and scales and taxonomic levels in mammalian Lophocebus share a common allometric line groups as diverse as equids (Reeve & which is vertically transposed from that of Murray, 1942; Radinsky, 1984); domestic the remaining taxa. The divergence of adult canids (Weidenreich, 1941); New World scaling patterns in Cercocebus and Lophocebus anteaters (Reeve, 1939); carnivores is inconsistent with models invoking simple (Radinsky, 1981); and titanotheres (Hersh, truncation of common growth vectors and 1934). Within Primates, positive facial argues against the presence of ontogenetic allometry is well documented and suf- allometry, at least in its narrowest sense. ficiently common to be accepted as a general This interpretation is supported by the work trend among non-human catarrhines of Collard & O’Higgins (2001) who report (Biegert, 1963; Vogel, 1968; Ravosa & that significant differences between the Profant, 2000). The ontogenetic basis of ontogenetic trajectories of mangabeys and this pattern has been most intensively large-bodied papionins are already present studied in the extant great apes. In gorillas, early in postnatal development. chimpanzees, and orang-utans, cranial The apparent absence of classic ontogen- growth is dominated by relatively rapid etic allometry notwithstanding, allometric forward growth of the face accompanied by scaling is a major determinant of papionin increased infraorbital facial depth, dorsal cranial shape variation. Principal Compo- rotation of the alveolar process, and nent 1 summarizes a substantial portion of decreased basicranial flexion (Krogman, total shape variation and is strongly linearly 1931a,b,c; Shea, 1983, 1985; Leutenegger related with size across all papionins. & Masterson, 1989). Extension of these Although the small-bodied taxa—Macaca, ontogenetic trajectories produces cranial Cercocebus, and Lophocebus—are transposed sexual dimorphism within species and above and below the common RMA line, differences in cranial form between the genus slopes are not significantly different African apes (Krogman, 1931a,b,c; Giles, from the pooled slope. Despite observed 1956; Shea, 1983, 1985; Leutenegger & heterogeneities among taxa, the pooled- Masterson, 1989; O’Higgins et al., 1990; sample regression line appears to be a O’Higgins & Dryden, 1993). Among cerco- good estimator of this general allometric pithecoids, Shea (1992) documented similar trend. Visualization of the shape variation trends for cercopithecins, where ontogenetic summarized by PC 1 shows positive facial allometry appears to explain the craniofacial allometry, characterized by increased facial proportions of Miopithecus, the smallest prognathism, and negative neurocranial extant catarrhine. allometry as cranial size increases. The cor- Within Papionini, comparative longi- responding landmark map supports this tudinal growth studies of M. nemestrina finding, identifying landmarks on the neuro- and P. (hamadryas) cynocephalus have also cranium, premaxilla, anterior maxilla, described facial ontogenies dominated by and anterior nasals as exerting particular positive forward growth of the rostrum and influence on this component. dorsal rotation of the maxilla and palate     571

(Swindler & Sirianni, 1973; Swindler et al., over equivalent size ranges (Profant & Shea, 1973; McNamara et al., 1976). Differ- 1994; Ravosa & Profant, 2000). It is this ential growth along these shared ontogen- marked divergence of form that is reflected etic trajectories contributes to the shape in traditional morphological classifi- differences observed between macaques cations uniting taxa occupying the extremes and baboons; differences among species and of the papionin size ranges. An emphasis on subspecies of Papio and Macaca; and cranial proportions in general, and relative sexual shape dimorphism within species facial length in particular, resulted in (Zuckerman, 1926; Freedman, 1962, 1963; papionin phylogenies heavily influenced by Albrecht, 1980; Bookstein, 1985; Cochard, size-correlated features. 1985; Cheverud & Richtsmeier, 1986; Leigh & Cheverud, 1991; Ravosa, 1991; Richstmeier et al., 1993). In the present Residual shape variation study, Principal Component 1 summarizes Residual shape variation encompasses shape a pattern of static multivariate cranial differences due to all factors other than allometry across adult papionins which allometry, including phylogenetic effects. closely resembles established patterns of Canonical discriminant analysis of size- catarrhine cranial ontogeny as well as gen- adjusted coordinates and visual exploration eral trends in mammalian cranial allometry. of size-uncorrelated shape components These broader trends, irrespective of their provide complementary information about developmental origins, appear sufficient patterns of residual shape variation. The to account for much of the homoplasy in former summarizes overall morphological papionin cranial form. similarity, while the latter gives insights into If the pattern of cranial allometry within patterns of cranial shape variation which the Papionini is less than noteworthy, the contribute to these similarities. extent to which allometric trends drive over- The Mahalanobis distance matrix based all cranial shape variation is remarkable. on size-adjusted coordinates (Table 9) Profant (1995) found that allometric effects shows little correspondence to common accounted for 98% of cranial shape variation conceptions of papionin cranial form or among Macaca fascicularis, Macaca nemes- phylogenetic relationships. Although trina, and Papio (hamadryas) cynocephalus, Lophocebus has its greatest similarity with taxa known to share a common scaling Papio, the latter actually falls closest to trajectory. Even allowing for a greater diver- Macaca. Cercocebus, too, has its strongest sity of adult morphologies in the current similarity with Papio, while Mandrillus is sample; observed heterogeneities of scaling actually slightly closer to Macaca. In fact, patterns among taxa; and the proportion of the observed pattern of inter-genus dis- Principal Component 1 variance not attribu- tances implies considerable morphological table to cranial size, allometric effects still conservatism in papionin cranial form. account for over 60% of total cranial shape Interestingly, Lophocebus is the most distinct variation. This is consistent with the results of the non-Theropithecus African papionins, of Profant & Shea (1994), who found that consistently showing the greatest pairwise allometric effects explained a preponderance distances. The canonical plot (Figure 9) of craniometric variation within the Cerco- supports this interpretation. With respect to pithecinae, with papionins showing steeper the first three canonical axes, Macaca and allometric trajectories than cercopithecins. Papio are most similar, while Lophocebus is These slope differences resulted in greater clearly divergent from the other taxa and morphological diversification for papionins widely separated from Cercocebus. 572 . 

Visualization of shape variation along 1926; Freedman, 1963), showing markedly Principal Component 5 (analysis excluding greater ‘‘downward bending’’ of the face Theropithecus), whose extremes are occupied than Mandrillus (see illustrations in Hill, by Cercocebus and Lophocebus, respectively, 1974; Maier, 2000). While this feature is not identifies the shape differences which con- ordinarily associated with the relatively tribute to the morphological distance orthognathic macaques, in comparison with between these taxa [Figure 7(e)]. In com- the similar-sized Cercocebus, and particularly parison with Cercocebus, Lophocebus displays Lophocebus, the macaque lower face is, in a lower neurocranium; a narrower and more fact, more ventrally oriented. Thus, Papio dorsally oriented muzzle with relatively pro- and Macaca appear to share a common jecting nasals; and a narrower malar region pattern of facial hafting when allometric with less flaring zygomatic arches. This effects are controlled. agrees with Groves (1978) description of the Principal Component 3 (analysis exclud- ‘‘stretched out’’ appearance of Lophocebus ing Theropithecus) separates males and skulls. Groves (1978) also noted the rela- females and is correlated with centroid size tively shorter and broader orbits of Cerco- within genera. Shape variation along this cebus, which are reflected here in differences axis is similar in some respects to trends in supraorbital configuration along PC 5 along Principal Component 1, probably [Figure 7(e)] and highlighted by the strong reflecting within-taxon allometric effects influence of the mid-torus superior land- (see above). However, patterns of shape mark [Figure 8(e)]. Interestingly, the variation along PC 3 also highlight differ- observed pattern of shape differences ences between sexes which are not directly between Cercocebus and Lophocebus repre- attributable to differences in cranial centroid sents a reversal of the general papionin allo- size [Figure 7(c)]. In particular, female metric trend. Larger papionins typically neurocrania, when scaled to unit size, are show lower and narrower neurocrania and higher and more globular than those of their narrower faces, but Lophocebus is smaller male counterparts but not appreciably than Cercocebus, both in body mass and longer. Males exhibit a more parallel-sided cranial centroid size. palate, while females show a more parabolic The second principal component [Figure palatal outline, a difference clearly related to 7(b)] united Macaca and Papio to the exclu- canine sexual dimorphism. Finally, males sion of other papionins, a result congruent exhibit comparatively broad and flaring with the canonical variates analysis and zygomatics in comparison with females, small Mahalanobis distance between these possibly reflecting differences in the relative taxa. Visualization of shape trends along PC size and orientation of the temporalis and 2 shows Macaca and Papio to be relatively masseter muscles (Swindler & Wood, klinorhynch, with projecting interorbital 1982). and supraorbital regions and procumbent Principal Component 4 separates Macaca (ventrally-deflected) faces relative to other and female Mandrillus from other papionins, taxa. Supporting this, influential landmarks most notably Papio. The canonical dis- are found on the basicranium, anteroinferior criminant analysis likewise places Mandrillus palate, infraorbital region, and supraorbital slightly closer to Macaca than Papio. This margins [Figure 8(b)]. Relative prominence component appears to summarize differ- of the supraorbital region is a discernable ences in the orientation of the zygomatic feature of both Macaca and Papio, and Papio bodies and the relative contribution of the has long been recognized as exhibiting pro- orbit to total facial height; however, these nounced facial procumbence (Zuckerman, differences are extremely subtle. Reference     573 to a small comparative sample found that interpreted as homoplastic and a product of male and female Macaca fascicularis do parallel evolution. However, it must be resemble female Mandrillus sphinx in the noted that Collard & O’Higgins (2001), features highlighted by PC 4. In both, the applying similar methods to a somewhat orbits constitute roughly half of total facial different dataset, have reached exactly the height and the zygomatic bodies are some- opposite conclusion concerning the polarity what ‘‘swept back’’, giving the midface a of papionin cranial allometries. Studies visor-like appearance. This contrasts with including additional taxa occupying the full male (and to a lesser extent female) Papio, range of papionin body sizes may help clarify where the malar regions are more anteriorly the distribution and polarity of cranial scal- oriented and the orbits contribute a smaller ing patterns, but detailed growth studies proportion of total facial height. In contrast in Cercocebus, Lophocebus, and the smaller to other components, which show strong macaques will be required to isolate the agreement between shape component visu- developmental basis for and timing of the alizations and landmark maps, only four initial divergence of allometric trajectories in influential landmarks were identified for this group. At the same time, renewed atten- Principal Component 4 [Figure 8(d)] and tion should be given to identifying ecological these showed no clear correspondence to and functional selective forces contributing visualized shape trends [Figure 7(d)]. Of all to variation in allometric scaling patterns the shape components considered, the among papionin primates. pattern of variation along this component is On first inspection, size-uncorrelated least robustly supported and its significance, shape components are not particularly if any, is unclear. informative concerning phylogenetic re- lationships among African papionins. While Conclusions the second principal component separates Observed patterns of cranial shape variation the outgroup Macaca and, interestingly, among the Papionini indicate that the evo- Papio from all other taxa, no component lution of cranial form within this group is unites members of the African molecular less straightforward than previously thought. clades. Similarly, canonical analysis of size- The presence of a common allometric scal- adjusted coordinates shows no particular ing pattern in Macaca, Papio, Mandrillus, affinity between clade members when size and perhaps Theropithecus, suggests that this effects are controlled. Thus, analysis of size- is a shared feature and represents the uncorrelated shape variation gives no direct primitive condition for African papionins. support to molecular phylogenies. The Outgroup comparisons will be required to results are perhaps more significant for determine whether this pattern is a derived what is not observed. When size-correlated feature for papionins or a retention from shape variation is factored out, the pervasive a more distant cercopithecine ancestor. similarities which have driven traditional The downward transposition of allometric classifications disappear. No shape com- trajectories in Cercocebus and Lophocebus ponent simultaneously unites the two indicates that mangabeys are similar in pos- mangabeys, on the one hand, and baboons sessing enlarged neurocrania and reduced and mandrills, on the other. Rather, muzzles in comparison with comparably Principal Component 2 distinguishes Papio sized macaques, mandrills, and baboons. and Macaca from Mandrillus and the Given the current understanding of mangabeys and Principal Component 5 papionin phylogeny, this shared mangabey separates Cercocebus and Lophocebus. Simi- scaling pattern is most parsimoniously larly, both Mahalanobis distances and 574 .  canonical plots show Cercocebus and implies that similarities in mangabey facial Lophocebus to be clearly separated in canoni- form result from parallel evolution. How- cal space, while Papio has its strongest ever, broader taxonomic samples incor- morphometric affinities with Macaca. porating additional papionin taxa and As in the case of size-correlated shape multiple outgroups are needed to reconcile variation, Macaca and Papio share a com- conflicting results (cf. Collard & O’Higgins, mon pattern of residual shape variation 2001) and more rigorously test hypotheses which is inferred to be the ancestral of polarity for the shape trends observed papionin condition. Further studies includ- here. Analyses of residual (size- ing cercopithecin outgroups are needed to uncorrelated) shape variation reveal an determine whether this pattern is unique to absence of morphometric affinity between the Papionini or part of a common cerco- Cercocebus and Lophocebus when size effects pithecine heritage. The observed pattern of are controlled, but this lack of quantitative Mahalanobis distances suggests that Papio resemblance is belied by similarities in key represents the primitive morphometric qualitative features. Thus, it will be nec- pattern for African papionins, from which essary to clarify the definition, phylogenetic other taxa have diverged to varying degrees. distribution, and functional significance of Although Cercocebus and Mandrillus show distinctive papionin traits, particularly the certain similarities in their overall pattern of presence of excavated facial fossae and the variation with respect to the canonical axes, development of maxillary ridges (McGraw patterns of residual variation do not give & Fleagle, 2000), before the issue of clear support to molecular phylogenies of papionin craniofacial homoplasy can finally the Papionini. Rather, they describe a be laid to rest. These uncertainties notwith- remarkable level of conservatism in cranial standing, the present study significantly form among non-Theropithecus papionins, increases our knowledge of patterns of with individual taxa exhibiting rela- craniometric variation in extant papionin tively minor variations on a common primates. It is hoped these results will pro- morphometric theme. vide a more robust comparative framework The Papionini are often cited as a particu- within which to evaluate fossil papionin larly striking example of morphological taxa and enhance our understanding of homoplasy (Disotell, 1996; Lockwood & the evolutionary history of this fascinating Fleagle, 1999; Collard & Wood, 2000). group. The present study documents patterns of homoplastic similarity in papionin cranial Summary shape due to allometric effects and provides some indication of the processes which may Geometric morphometric analysis of cranial contribute to this similarity. However, this landmark data shows that allometric study raises as many questions as it answers. scaling of cranial shape is present across Results do not resolve the question of all papionins and accounts for certain mangabey cranial homoplasy, but rather craniofacial similarities between like-sized reframe it more narrowly in terms of parallel members of separate clades. Comparisons shifts in allometric scaling patterns. Onto- of regression lines show considerable genetic studies will be required to explicate homogeneity of scaling among papionin the developmental origins of variation genera; however, results give no support to in papionin allometric trajectories. The hypotheses of uniquely shared allometric inference that Papio preserves the primitive scaling patterns either within papionin morphometric pattern for African papionins clades or across all African papionins.     575

Rather, Cercocebus and Lophocebus show his continued interest in and support of minor differences in slope and highly sig- this work. nificant negative displacement of their I am indebted to Steve Frost and Tony allometric lines relative to other papionins. Tosi for their substantial contributions to Nevertheless, allometric trends reflecting the NYCEP-MRG primate cranial data- general patterns of mammalian cranial base, without which this research would not allometry appear to be a major determinant have been possible. I also wish to thank the of papionin cranial shape variation, con- Curators and Collections Managers of tributing considerably to the marked the following institutions: the American divergence of form which is reflected in Museum of Natural History, Department traditional classifications of this group. of Mammalogy; the National Museum of Analysis of size-uncorrelated shape variation Natural History, Department of Mam- gives no clear support to molecular phylog- malogy; the Field Museum of Natural enies, but highlights the absence of morpho- History, Division of Mammalogy; the metric similarity between the mangabey British Museum of Natural History, Depart- genera when size effects are controlled. ment of Zoology; the Powell–Cotton Patterns of allometric and residual shape Museum; the Senckenberg Natural History variation suggest conservatism of non- Museum—Frankfurt; the Laboratory for Theropithecus papionin cranial form, with Human Evolutionary Studies—University of Papio appearing to demonstrate a primitive California Berkeley; and the University of morphometric pattern from which other California Museum of Vertebrate Zoology. African papionins, most notably Lophocebus, I am deeply grateful to Les Marcus, David have diverged. Outgroup comparisons with Reddy, Dennis Slice, and James Rohlf for cercopithecin taxa will be required to deter- their patient guidance as I ventured into the mine whether these trends are unique to brave new world of geometric morpho- the Papionini or inherited from a more dis- metrics. Thanks are also due to Tim Cole, tant cercopithecine ancestor. Descriptions Dennis Slice, Richard Smith, Bill Jungers, of craniometric variation among extant Mike Plavcan, and John Hunter for advice papionins are a necessary basis for assess- on technical and statistical matters, and to ments of morphological and phylogenetic Jim Cheverud for his thoughtful discussion affinities of fossil taxa, and the present study of allometry and the meaning of Cheverud lays the groundwork for future studies of (1982). I wish to thank Dennis Slice and extinct papionins. Paul O’Higgins for making beta copies of their morphometrics packages available and Mike Plavcan for granting permission to adapt his illustration of the female Macaca Acknowledgements fascicularis skull. This work was conducted under the Steve Frost, Les Marcus, Mike Plavcan, auspices of the Morphometrics Research Steve Leigh, and two anonymous reviewers Group of the New York Consortium in provided comments on various drafts of this Evolutionary Primatology and supported by paper which improved the final product con- NSF Research & Training Grant # BIR siderably. Any errors of fact or interpretation 9602234 (NYCEP) and NSF Special are, of course, my own. Program Grant # ACI-9982351 (E. Delson, This paper is NYCEP Morphometrics L. F. Marcus, D. P. Reddy, N. Tyson, and Contribution #3. W. K. Barnett, Principal Investigators). 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