SHAPE MEETS FUNCTION:STRUCTURAL MODELS IN PRIMATOLOGY

Edited by Emiliano Bruner

Proceedings of the 20th Congress of the International Primatological Society

Torino, Italy, 22-28 August 2004

MORPHOLOGY AND MORPHOMETRICS

Introduction

Allometric scaling of craniofacial dimensionsis a general phenomenon in cercopithecine pri-mates, accounting for a significant proportion ofcranial shape variation within and among taxa(Profant & Shea, 1994; Ravosa & Profant,2000). Among cercopithecines, tribe Papionini -the monophyletic group comprising macaques(genus Macaca), mangabeys (Cercocebus andLophocebus), mandrills and drills (Mandrillus),and baboons (Papio and Theropithecus) - isremarkable both for the degree to which allo-

metric scaling determines cranial form (Profant& Shea, 1994; Ravosa & Profant, 2000) and forthe extensive, nonhomologous similaritiesbetween like-sized members of its two Africansub-clades (Fleagle & McGraw, 1999; Lockwood& Fleagle, 1999; Collard & O’Higgins, 2001;Fleagle & McGraw, 2001; Singleton, 2002;Leigh et al., 2003; Singleton, 2005). Specifically,the small-bodied, quasi-arboreal mangabeys arecharacterized by moderate facial prognathism,facial retraction, and deeply excavated sub-orbital fossae (Kuhn, 1967; Thorington &Groves, 1970; Hill, 1974; Szalay & Delson,

JASsJournal of Anthropological Sciences

Vol. 82 (2004), pp. 27-44

Geometric morphometric analysis of functional divergence in mangabey facial form

Michelle Singleton

Department of Anatomy, Chicago College of Osteopathic Medicine, Midwestern University, 555 31stStreet, Downers Grove, IL 60515, USA, e-mail: msingl@midwestern.edu

Summary – Positive facial scaling is a well known phenomenon in Old World monkeys, but non-homol-ogous displacements of facial allometries in mangabeys (Papionini: Cercocebus and Lophocebus) resultin facial shortening and retraction relative to other cercopithecines. Both Cercocebus and Lophocebusare known to feed on a variety of resistant foods, and mangabey facial geometries have been viewed asadapted for the forceful incision and powerful mastication associated with hard-object feeding. Observeddifferences between mangabey genera in the relative frequency of incision and mastication have been linkedto significant differences in mandibular shape, but analogous differences in facial form have yet to be iden-tified. The hypothesis of functional divergence in facial form can be tested relative to criteria derived fromthe constrained lever model of the primate masticatory system. Specifically, if Lophocebus is adapted forforceful incision, facial retraction, reduced molar row length, and expansion of the incisal region are expect-ed. Conversely, if Cercocebus facial form has been optimized for postcanine crushing, medially positionedtooth rows, increased biarticular breadth and decreased tooth row length are expected. These predictionswere tested using geometric morphometric analysis. Three-dimensional craniometric landmarks capturingfunctional aspects of the masticatory complex were recorded for a large sample of cercopithecines and select-ed colobines. Procrustes-aligned coordinates were subjected to principal components analysis, and principalaxes of shape variation were explored statistically and graphically. The hypothesis that the Lophocebus mas-ticatory system is adapted for forceful incisal biting was supported. Cercocebus failed to conform to pre-dictions, despite the fact that it is known to engage in forceful postcanine mastication. It is suggested thatchanges in the relative proportions of the postcanine dentition permit Cercocebus to circumvent function-al constraints on facial retraction and generate large postcanine bite forces while still maintaining struc-tural safety margins.

Keywords – Cercocebus, Lophocebus, mastication, functional allometry, constrained lever model.

1979; Strasser & Delson, 1987). Recent ontoge-netic analyses have demonstrated that Cercocebusand Lophocebus exhibit similar but non-homolo-gous growth allometries distinct from those oftheir respective sister taxa, Mandrillus and Papio,as well as the more distantly related macaques(Collard & O’Higgins, 2001; Leigh et al., 2003).

Whereas ontogenetic scaling in closely relat-ed taxa is typically associated with selection foraltered body size, dissociations of allometric rela-tionships, as observed among the papionins, arefrequently indicative of natural selection fornovel size-shape relationships (Gould, 1966,1971, 1975; Shea, 1983, 1985). Such dissocia-tions may reflect the need to preserve biome-chanical equivalence as species evolve into newsize ranges (Gould, 1971; Shea, 1983; Ravosa,1992; Smith, 1993; Shea, 1995; Vinyard &Ravosa, 1998) or selection for new or enhancedfunctional capacities in response to specific adap-tive challenges (Demes et al., 1986; Ravosa,1990, 1992; Shea, 1995). In the case of themangabeys, allometric dissociation is responsi-ble for the marked facial shortening and retrac-tion that distinguish Cercocebus and Lophocebusfrom most other cercopithecines (Singleton,2005). Under the classic lever model of the mas-ticatory system, facial retraction is linked toincreased mechanical advantage of the masseterand anterior temporalis muscles, thusmangabeys are expected to exhibit increased rel-ative bite forces (Du Brul, 1977; Hylander,1977, 1979b; Ravosa, 1990; Antón, 1996;Singleton, 2005). This functional interpretationof mangabey facial form accords well with avail-able ecological data: both Cercocebus andLophocebus are known to feed on a variety ofresistant foods including sclerocarp fruits andhard seeds and nuts routinely shunned by sym-patric guenons (Haddow, 1952; Tappen, 1960;Chalmers, 1968; Jones & Sabater Pi, 1968;Cashner, 1972; Happel, 1988; Kingdon,1997; Fleagle & McGraw, 1999). Thus,mangabey facial geometries have been interpret-ed as adapted for the forceful incision and pow-erful mastication associated with hard-objectfeeding (Chalmers, 1968; Happel, 1988;Kingdon, 1997).

But despite their many similarities, it hasbeen noted that the two mangabey genera differin the relative frequency of these feeding behav-iors. Specifically, Lophocebus is thought to engagemore frequently in incisal preparation of hard-skinned fruits, whereas Cercocebus engages inmore postcanine crushing of seeds and nuts(Daegling & McGraw, 2000). Consistent withthis hypothesis, Daegling and McGraw (2000)have demonstrated significant differences inmangabey mandibular morphology. TheLophocebus mandible, with its greater relativedepth, is better suited to resist parasagittal bend-ing moments during powerful incision; con-versely, the relatively thicker mandibular corpusof Cercocebus is capable of resisting transversebending moments associated with forceful post-canine biting (Hylander, 1979b; Daegling &McGraw, 2000).

While these findings are persuasive, thehypothesis of functional divergence would besubstantially strengthened by identification ofanalogous differences in facial form. However,the predictions of the simple lever model cannotdistinguish between these functional alternatives.By contrast, the constrained lever model put for-ward by Greaves (Greaves, 1978) and subse-quently modified by Spencer (Spencer & Demes,1993; Spencer, 1998,1999), makes substantiallydifferent predictions concerning the morpholo-gies associated with incision versus mastication.Under this model (Fig. 1), masticatory geome-tries are constrained by the need to avoid poten-tially injurious distractive forces at the balancing-side temporomandibular joint (TMJ). For bitepoints within Region I, corresponding roughlyto the antemolar dentition, predictions are essen-tially identical to those of the classic model.Because Region I bite points define triangles ofsupport enclosing midline muscle resultantforces, mechanical advantage, and thus relativebite force, increases as bite points shift posterior-ly; thus, facial shortening and retraction areexpected to enhance maximum incisal bite forces(Greaves, 1978; Spencer, 1999). At the sametime, compensatory shortening of the molar rowmay be required to avoiding pushing distalmolars into Region III, where TMJ distraction is

30 Mangabey facial form

unavoidable (Hylander, 1977; Spencer &Demes, 1993; Spencer, 1999). Bite points inRegion II, by contrast, are associated with sup-port triangles that cannot enclose a midline mus-cle resultant force (Greaves, 1978; Spencer,1999). To prevent distraction of the TMJ, bal-ancing side muscle activity is decreased, shiftingthe muscle resultant towards the working side(Hylander, 1979a, b; Spencer, 1999). As bitepoints shift posteriorly, any mechanical advan-tage gained is offset by a compensatory reductionin balancing side muscle activity. Thus, facialretraction confers no masticatory benefit.Instead, the constrained model predicts thatselection for increased postcanine bite forces willresult in more medially positioned tooth rowsrelative to biarticular breadth (Hylander, 1977;Spencer, 1999). Because the anteroposteriorlength of Region II decreases medially, a com-pensatory decrease in postcanine tooth rowlength is also expected (Spencer, 1999). Thesecontrasting predictions permit a test of alternatehypotheses of the functional significance ofmangabey facial form. If Lophocebus facial

geometries are principally adapted for forcefulincision, facial retraction, reduced molar rowlength, and expansion of the incisal region areexpected. Conversely, if Cercocebus facial formhas been optimized for postcanine crushing,more medially positioned tooth rows, increasedbiarticular breadth, and decreased tooth rowlength should be observed.

Functional hypotheses of primate facial formare typically tested by regression analysis of lineardistances interpreted within the context of thebivariate allometric model (Huxley, 1932;Gould, 1966). However, geometric morphomet-ric analysis of cranial allometries offers certainadvantages over traditional methods, particularlywhen functional interpretation of allometric dis-sociations is desired (Singleton, 2005). In com-parison with bivariate analyses, which test thescaling of variables individually and sacrificeinformation concerning relative position, land-mark-based geometric analyses permit simulta-neous examination of covariation among all vari-ables (landmarks) while preserving geometricrelationships (Rohlf & Marcus, 1993). By

31M. Singleton

Fig. 1 - Diagram of dental regions defined by the constrained lever model of the masticatory system(Greaves, 1978; Spencer, 1999). See text for discussion of biomechanical differences amongregions. Figure redrawn after Spencer (1999).

describing how the functional geometry of anentire morphological complex changes withchanging size, this approach facilitates function-al interpretations of both allometric and residual(size-independent) shape variation (Singleton,2005). In this study, a comparative geometricanalysis of the cercopithecine masticatory systemis performed to test the hypothesis of functionaldivergence in mangabey facial form.

Materials and methods

The study sample comprised crania of 486adult individuals representing most commonlyrecognized cercopithecine genera and twocolobine outgroups (Tab. 1). The sample waslargely limited to wild-collected specimens ofknown provenience; however, for taxa otherwisepoorly represented in museum collections (e.g.,Theropithecus), zoo specimens lacking obviouspathology and deemed to represent wild-typemorphology were included. Adult status wasdefined by complete eruption of the permanentdentition and closure of the sphenoccipital syn-chondrosis. Following previously published pro-tocols (Singleton, 2002; Frost et al., 2003),three-dimensional landmark coordinates wererecorded using a Microscribe 3-DX digitizer(Immersion Corp., San Jose, CA). Missing datawere estimated either by reflection (bilaterallandmarks) or substitution of sex-specific taxonmean values (unpaired landmarks). A high pro-portion of specimens (19%) exhibited at leastone missing landmark; however, estimated valuesaccount for only 0.01% of data analyzed so arenot expected to affect results. From an originalset of 45 standard osteometric landmarks (seeFrost et al., 2003 for landmark definitions), asubset of eighteen (Fig. 2) was chosen to cap-ture functional aspects of the masticatory com-plex pertinent to the constrained level model,including: 1) the relative positions of the TMJ,zygomatic root, and palate; 2) palate shapeand relative length; and, 3) the positions ofmaxillary bite points.

Masticatory landmark configurations weresubjected to generalized Procrustes analysis - aniterative least-squares procedure that eliminates

the effects of translation, rotation and scale (Sliceet al., 1996; Dryden & Mardia, 1998) - usingMorpheus et al. (Slice, 1998). Principal compo-nents analysis (PCA) of the covariance matrix ofaligned coordinates was performed as a means ofdata reduction and to compensate for the lack ofstatistical independence among landmarks dueto morphological integration and the constraintsof Procrustes superimposition (Dryden &Mardia, 1998; Rohlf, 1999). PCA ordinatesspecimens relative to mutually orthogonal axes ofshape variation, the principal shape components.The resulting shape component (SC) scores arestatistically independent shape variables thatsummarize the majority of sample variation(Dryden & Mardia, 1998; Rohlf, 1999). Itshould be emphasized that because GPA doesnot eliminate allometric effects, shape compo-nent scores incorporate both size-correlated(allometric) and size-independent (residual)shape variation. Patterns of shape variation forselected shape components were explored graph-ically using Morphologika (O’Higgins & Jones,1999) to conduct PCA of sex-specific meanforms and generate wireframe representations ofshape trends along individual axes. In some cases,the resulting mean scores differed slightly fromthose of the full sample analysis, but these devia-tions do not substantively affect interpretationsof functional shape variation.

Results of the full sample PCA were used asthe basis of all statistical analyses. Bivariate scat-terplots of SC scores against log centroid size(Slice et al., 1996) were used to identify potentialallometric relationships, the strengths of whichwere assessed by correlation analysis. Between-species differences in scaling were tested usinganalysis of covariance (ANCOVA) of SC scoresby log centroid size, and differences in regressionelevations were assessed by pairwise comparisonof least-squares means, i.e., species means adjust-ed for the effects of centroid size. Where hetero-geneity of slopes precluded statistical testing ofelevations across the entire sample, ANCOVAanalyses were rerun for the mangabeys alone. Fornon-allometric shape components, differences inshape between mangabey species were testedusing analysis of variance (ANOVA) of SC scores.

32 Mangabey facial form

33M. Singleton

Table 1. Study sample by sex

Fig. 2 - Ventral view of representative cercopithecine skull (female L. albigena johnstoni) showingmasticatory landmarks employed in this study. See Frost et al. (2003) for landmark defini-tions.

34 Mangabey facial form

Results

The first ten principal shape componentsaccount for 90% of total shape variance. Ofthese, only the first four achieve meaningful sep-aration among sample taxa. The 1st PrincipalShape Component (SC1) accounts for 61% oftotal variance and appears to ordinate specimensby size (Figure 3a), with small-bodied taxa(Miopithecus and Cercopithecus) falling at thenegative end of the axis and large-bodied taxa(Papio and Mandrillus) occupying its positiveextreme. Smaller taxa are characterized by rela-tively short, broad palates and anteriorly posi-tioned zygomatic roots; large taxa exhibitdecreased biarticular breadth and narrow, elon-gate palates, which are located well anterior tothe zygomatics. SC1 is significantly correlatedwith log centroid size both across (r = 0.89, p <0.0001) and within cercopithecine species (seeTab. 2). ANCOVA confirms that allometriceffects account for a large proportion of variationin SC1 (adjusted R2 = 0.96, F = 374.95, p <

0.001) and finds significant differences amongspecies in the scaling of SC1 relative to log cen-troid size (Tab. 3). Heterogeneity of slopesamong sample species (p < 0.01) precludes statis-tical comparison of regression elevations. It isnevertheless clear that Cercocebus and Lophocebusregressions are strongly negatively displaced rela-tive to other cercopithecines and exhibit exten-sive overlap with colobines (Figure 4a). As aresult, both mangabey genera are characterizedby decreased palate length, increased palatebreadth, and increased biarticular breadth whencompared with similarly sized cercopithecines.Cercocebus torquatus, by virtue of its greater aver-age size (Delson et al., 2000), shows significantlygreater SC1 scores than either C. galeritis or L.albigena (see Tab. 4). However, when effects ofsize are controlled, it is C. galeritis which differsfrom other mangabey species. It shows signifi-cantly lower least-squares means than either C.torquatus or L. albigena (Tab. 4); the latter taxaare not statistically distinguishable. Thus, at sim-ilar body sizes, C. torquatus and L. albigena are

Table 2. Correlation of SC scores with log centroid size

35

geometrically similar with respect to SC1, whileC. galeritis exhibits a somewhat greater biarticu-lar breadth and a wider and shorter palate.

The 2nd Principal Shape Component (6.4%of shape variance) separates cercopithecins frompapionins and Colobus and describes differencesin palate shape and position (Fig. 3a).Cercopithecins (negative scores) exhibit a short-er, more parabolic palate that is relatively anteri-orly positioned, while papionins (more positivescores) are characterized by palates that arelonger, squarer, and relatively closer to the TMJ.SC2 is uncorrelated with log centroid size acrosstaxa (r = 0.15, p = 0.001), but moderately corre-lated within the majority of species (Tab. 2).Thus, within species, relative distance betweenthe palate and TMJ tends to decrease withincreasing body size. Allometric effects accountfor a smaller proportion of variance in SC2(adjusted R2 = 0.67, p < 0.001). Heterogeneityof slopes (p < 0.001) prevents testing of differ-ences in elevations across cercopithecines; how-ever, the obvious negative displacement of papi-onin trajectories (Figure 4b) implies greaterretraction of the palate relative to TMJ than inlike-sized cercopithecins.

Like other papionins, mangabeys fall towardsthe positive end of SC2 (Figure 3a), butLophocebus shows significantly more positive

SC2 scores than either Cercocebus species(Tab. 4), indicating a relatively more posteriorlypositioned palate. In comparisons restricted tomangabey species, differences in scaling accountfor a relatively small, albeit significant, propor-tion of variance in SC2 (adjusted R2 = 0.23, p <0.001). Homogeneity of slopes is confirmed, andwhen size effects are controlled, Lophocebusshows a more positive estimated marginal mean(Tab. 4) than either Cercocebus species. In sum-mary, both mangabey genera share the papionintendency towards relatively posterior palate posi-tion, but Lophocebus exhibits stronger palatalretraction than Cercocebus, irrespective of size.

The 3rd Principal Shape Component (5.7 %total shape variance) separates males and femaleswithin species (not shown). SC3 is only weak-ly correlated with log centroid size acrossspecies (r = 0.26, p. < 0.0001) and either weaklycorrelated or uncorrelated within the majority ofspecies, and is therefore inferred to summarizenon-allometric sexual shape dimorphism.Within species, males (more positive scores)exhibit more flaring zygomatics and relativelyexpanded canine regions, while females (morenegative scores) show narrower zygomatics andmore parabolic palates.

The 4th Principal Shape Component (4.5%total shape variance) appears to summarize dif-

Table 3. ANCOVA of SC scores

M. Singleton

36 Mangabey facial form

Fig. 3 - Shape variation summarized by principal shape components: a) Plot of SC1 by SC2; b) Plotof SC1 by SC4. Symbols represent male and female mean values for each species.Wireframes represent extremes of shape variation along shape component axes.

37M. Singleton

Fig. 4 - Allometric scaling of principal shape components: a) SC1 by log centroid size; b) SC2 by logcentroid size. Wireframes represent extremes of shape variation for each component

38 Mangabey facial form

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39M. Singleton

ferences in dental arcade proportions (Fig. 3b).Relatively positive scores signify expansion of theincisal region and reduction of the molar rowposterior to M1; more negative scores indicatenarrower incisal regions and relative expansion ofthe tooth row anterior to M2. Lophocebus occu-pies the positive extreme of variation on this axis,and is thus characterized by increased relativebreadth of the incisor row and reduction of theposterior molar row. Cercocebus species exhibitsignificantly less positive scores (Tab. 4), result-ing in decreased incisal breadth and a relativeexpansion of the premolar region relative toLophocebus. SC4 is uncorrelated with log cen-troid size across taxa but strongly correlatedwithin most species (Tab. 2). ANCOVA (Tab. 3)confirms homogeneity of slopes among studytaxa, and comparison of least-squares meansidentifies significant differences in regression ele-vations between the mangabey genera (Tab. 4).At comparable sizes, Lophocebus possesses rela-tively larger incisors and smaller posterior molarswhile Cercocebus species possess relativelyenlarged premolars.

Discussion

The results of the present study are substan-tially similar to those of Singleton (2005), butwith the inclusion of additional landmarks, func-tional distinctions between mangabeys and othercercopithecines are more pronounced and differ-ences among mangabey species are now evident.The first two principal shape componentsdescribe intertaxic differences in relative palateshape and position that contribute to variation infacial prognathism. As is common for such stud-ies, the 1st Principal Shape Component is a com-mon allometric vector describing a pattern ofincreased palate length, decreased palate breadth,and enhanced facial prognathism with increasingsize. ANCOVA of SC1 by centroid size confirmsthis relationship, which is consistent with estab-lished patterns of cercopithecine facial scaling(Zuckerman, 1926; Freedman, 1962, 1963;Swindler & Sirianni, 1973; Swindler et al., 1973;McNamara et al., 1976; Cochard, 1985; Ravosa,1990; Richtsmeier et al., 1993; O’Higgins &

Jones, 1998; Ravosa & Profant, 2000; Collard &O’Higgins, 2001; O’Higgins & Collard, 2002;Leigh et al., 2003). As in the prior study, negativedisplacement of mangabey regression lines resultsin masticatory forms distinct from most cercop-ithecines and similar in many respects tocolobines. That the inclusion of additional land-marks results in more extensive overlap betweenmangabey and Colobus allometric trajectoriessuggests that prior results are not an artifact oflandmark selection but reflect pervasive func-tional differences between mangabeys and othercercopithecines. The 2nd Principal ShapeComponent also summarizes size-correlated dif-ferences in palate shape and position. But scal-ing of SC2 is considerably more complex, with apattern of inter- and intra-tribal differences sim-ilar to - and perhaps functionally linked with -those previously described for relative gape(Singleton, 2005).

Mechanical AdvantageThe first principal shape component

describes variation in relative palate proportionsand the relative position of the zygomatic root,while the second summarizes variation in dentalarcade shape and the position of the palate rela-tive to the TMJ. Considered jointly, these com-ponents permit an assessment of relative mastica-tory advantage. Under the constrained levermodel, reduced facial prognathism providesincreased mechanical advantage at Region I bitepoints and is functionally associated with force-ful incision, while increases in the ratio of biar-ticular breadth to arcade breadth increasemechanical advantage at Region II bite pointsand are linked with powerful molar biting(Greaves, 1978, 1995; Spencer, 1999). Relativeto similarly sized cercopithecines, bothLophocebus and Cercocebus exhibit marked facialshortening and strong facial retraction and aretherefore expected to generate greater relativeincisal bite forces. All mangabey species sampledare characterized by increased biarticular breadthrelative to size, but concomitant increase in rela-tive palate breadth implies no net increase inRegion II mechanical advantage. On the con-trary, because palatal breadth scales with stronger

40 Mangabey facial form

negative allometry than biarticular breadth(Spencer, 1999) - meaning relative molar biteforces increase with increasing size - the negativedisplacement of mangabey trajectories is expect-ed to result in smaller relative bite forces than insimilarly sized cercopithecines.

Small but statistically significant differencesin functional scaling among mangabey speciesare revealed by comparisons of size-adjusted SCscores. Negative displacement of the C. galeritistrajectory results in increased relative interarticu-lar and palatal breadths and more pronouncedfacial shortening in comparison with C. torqua-tus and L. albigena; the latter taxa have similaradjusted mean SC1 values and are not statistical-ly distinguishable. The significantly more posi-tive size-adjusted SC2 mean of Lophocebus signi-fies relatively greater retraction of the palate thanin either Cercocebus species. Based on these find-ings, it is expected that Lophocebus and C. galeri-tis will exhibit relatively greater incisal bite forcesthan C. torquatus, the latter due to more pro-nounced facial shortening, the former because ofstronger facial retraction. For reasons outlinedabove, it is also expected that C. galeritis willexhibit smaller relative molar bite forces.

Dental ProportionsThe 4th Principal Shape Component sum-

marizes allometric variation in relative dentalproportions. Within species, increasing size isaccompanied by increased relative incisal breadthbut relative decrease in the length of the post-M1

molar row. Under the constrained lever model,facial retraction is expected to be accompaniedby a reduction in the length of the posteriormolar row, a necessary accommodation to pre-vent distractive forces at the balancing-side TMJduring posterior molar biting (Greaves, 1978,1995; Spencer, 1999). Increased molar bite force,by contrast, is expected to be accompanied by ashorter postcanine tooth row, a geometric conse-quence of more medial tooth row position(Spencer, 1999). Lophocebus occupies one pole ofvariation with respect to SC4, and is character-ized by relatively enlarged incisors and a relative-ly shortened posterior molar row in comparisonwith most cercopithecids. Comparisons of raw

and size-adjusted mean SC4 scores showLophocebus to have significantly broader incisorsand shorter posterior molar rows than eitherCercocebus species. The relatively more negativemean scores of Cercocebus indicate a relativeexpansion of the tooth row anterior to M2.Differences in the total relative length of thepostcanine tooth row are not apparent on this, orany, principal shape component.

That Lophocebus possesses relatively broadincisors is well-known (Hill, 1974; Swindler &Sirianni, 1975; Groves, 1978; Szalay & Delson,1979; Kingdon, 1997), and relative reductionof the molar row has previously been noted(Hylander, 1979b; Szalay & Delson, 1979).The finding of posterior molar reduction con-forms with biomechanical predictions (Greaves,1978, 1995; Spencer, 1999) and mirrors studiesin which facial retraction has been linked to M3

reduction or loss (Hylander, 1977; Shea, 1992;Spencer & Demes, 1993). Thus, posteriormolar row reduction in Lophocebus is plausiblyinterpreted as a secondary adaptation to avoiddistraction of the balancing-side TMJ duringposterior molar biting. Predictions of tooth rowshortening in Cercocebus are contingent upon amedial shift in tooth row position. Since rela-tive palatal breadths in Cercocebus equal orexceed those of Lophocebus, the absence of a sig-nificant decrease in relative tooth row length isunsurprising. The apparent expansion of thepre-M2 tooth row was not predicted, butaccords with observations that Cercocebus ischaracterized by expanded first molars andmarkedly expanded fourth premolars (Fleagle &McGraw, 1999, 2001).

LophocebusThe functional divergence hypothesis

(Daegling & McGraw, 2000) posits that differ-ences between the mangabeys in the relative fre-quency of specific feeding behaviors are linked tobiomechanical differences in facial form. IfLophocebus is principally adapted for forcefulincision, it is expected to exhibit relative facialshortening and retraction, decreased molar rowlength, and relative expansion of the incisalregion. Consistent with these predictions,

41M. Singleton

Lophocebus exhibits decreased relative palatelength, strong retraction of the palate relative tothe TMJ, a reduction in post-M1 tooth rowlength, and a markedly expanded incisal region.The selective advantage of enlarged incisors foranimals engaging in habitual, forceful incision iswell-established; increased incisor breadth bothextends functional tooth life and increases work-ing surface area, giving maximum return relativeto muscular effort (Hylander, 1975; Eaglen,1984; Ungar, 1998). By increasing mechanicaladvantage, facial shortening and retraction alsoincrease masticatory efficiency, maximizingincisal bite forces relative to muscle force. Thus,the hypothesis that Lophocebus facial form isoptimized for forceful incisal biting is supported.

These results are consistent with previousfindings that the Lophocebus mandible is engi-neered to resist large parasagittal bendingmoments such as are incurred during anteriordental loading (Hylander, 1979b; Daegling &McGraw, 2000). Behavioral data for Lophocebusare sparse, but it is known to feed regularly onlarge, sclerocarp fruits (Haddow, 1952; Tappen,1960; Chalmers, 1968; Happel, 1988). Use ofincisors to crack resistant pericarps has beendirectly observed (Chalmers, 1968), as has incisalbark stripping (Chalmers, 1968; Cashner, 1972).It is thus reasonable to infer that the Lophocebusmasticatory complex is adapted for incisal prepa-ration of the hard-skinned fruits that are a majorcomponent of its diet (Tappen, 1960; Chalmers,1968; Jones & Sabater Pi, 1968; Kingdon,1997). As in the well known case of the Inuits(Hylander, 1977; Spencer & Demes, 1993), thisadaptation appears to come at the cost ofreduced molar row length and, perhaps, surfacearea (Spencer & Demes, 1993). Dental metricstudies are needed to confirm this finding and toassess its implications for masticatory function inLophocebus mangabeys.

CercocebusIf Cercocebus facial form has been optimized

for postcanine crushing, more medially posi-tioned tooth rows, increased biarticular breadth,and decreased tooth row length should beobserved. But contrary to predictions, Cercocebus

exhibits neither medially positioned tooth rowsnor decreased tooth row length. Biarticularbreadth is increased relative to size in C. torqua-tus, but no more so than in Lophocebus. In thecase of C. galeritis, allometric displacement actu-ally produces a less favorable ratio of biarticularbreadth to palatal breadth with the result thatrelative molar bite forces are decreased in com-parison with Lophocebus and other cercop-ithecines. Thus, by the criteria of the constrainedlever model, the hypothesis that Cercocebus facialform is specifically adaptive for postcanine mas-tication is not supported. Yet, the fact remainsthat Cercocebus mangabeys routinely masticateobjects of exceptional hardness and withoutapparent difficulty or ill effects (Happel, 1988;Fleagle & McGraw, 1999, 2001). Biomechanicalevidence, too, suggests that Cercocebus mandibu-lar form has been selected to resist transversebending moments generated during forcefulpostcanine biting (Hylander, 1979b; Daegling &McGraw, 2000).

The answer to this paradox might lie in therelative proportions of the Cercocebus tooth row.Fleagle and McGraw hypothesized that premolarexpansion in Cercocebus is an adaptation to hard-object feeding (Fleagle & McGraw, 1999, 2001),and forceful premolar biting has been reportedby Happel (1988) and McGraw (W.S. McGraw,pers. com.). The constrained lever model permitstwo possible interpretations of these observa-tions. Teeth within Region II are characterized bygreater occlusal surface area, and an abruptdecrease in tooth size typically marks its anteriorboundary (Greaves, 1995). Thus, premolarexpansion in Cercocebus may indicate that theregion of maximum force (Region II) has beenextended to include these teeth. How this exten-sion might have been achieved is not clear. Theconstrained lever model predicts that lateralmovement of the TMJ - as seen in mangabeysgenerally and C. galeritis in particular - will beaccompanied by a reduction in the effectivelength of Region II. Alternatively, it is possiblethat P4 remains within Region I, and thatextreme facial shortening in Cercocebus conferssufficient mechanical advantage to permit force-ful mastication outside the region of maximum

42 Mangabey facial form

force (Greaves, 1995). Studies incorporating theposition of the jaw adductor resultant force areneeded to clarify where the fourth premolar liesrelative to the Region I-Region II boundary andto establish which, if either, of these explanationsmight account for the relatively high bite forcesof which Cercocebus is capable.

Why either of these strategies might havebeen adopted in preference to the expecteddecrease in palate breadth is somewhat puzzlinguntil one recalls that Cercocebus also engages inincisal food preparation, albeit with lower fre-quency and less vigor than Lophocebus(Chalmers, 1968; Happel, 1988; Daegling &McGraw, 2000). Increased jaw breadth is themost efficient means to resist cranial torsionassociated with large anterior dental loads(Greaves, 1995). Thus, medial positioning of thetooth row is achieved only at the cost ofdecreased safety margins during forceful incisalbiting. It seems likely that Cercocebus facial formrepresents a compromise between the functionaldemands of incision and mastication. To avoidstructural failure during anterior dental loading,relative palatal breadth is maintained. But bytransferring forceful mastication to the mesialextent of the postcanine tooth row, Cercocebus isable to generate adequate postcanine bite forceswhile preserving TMJ integrity.

Conclusions and summary

Geometric morphometric analysis offers anefficient and effective means of exploring thefunctional consequences of allometric and size-independent variation in primate facial form. Inthis study, geometric methods were employed totest a hypothesis of functional divergence inmangabey facial form against the predictions ofthe constrained lever model of masticatory func-tion. Consistent with predictions, Lophocebus ischaracterized by marked facial shortening andretraction, increased incisal breadth, and reduc-tion of the posterior molar row. Thus, thehypothesis that Lophocebus facial form is adaptedfor powerful incision is supported. By contrast,the hypothesis that Cercocebus facial form isadapted for postcanine mastication was not sup-

ported, and the predicted morphological patternof increased biarticular breadth, decreased palatalbreadth, and reduced tooth row length was notobserved. Rather, Cercocebus is characterized byincreased interarticular breadth, a relativelyshort, broad palate, and expanded anterior toothrow. This finding is counter to traditional inter-pretations of mangabey facial form and is direct-ly contradicted by behavioral and biomechanicalstudies that confirm the ability of Cercocebus togenerate and safely dissipate large postcanineocclusal loads. To explain this discrepancy, it ishypothesized that Cercocebus facial form repre-sents a biomechanical compromise between thefunctional demands of anterior and posteriordental loading. It is suggested that by transfer-ring forceful mastication to the anterior-mostextent of the postcanine tooth row, Cercocebuscircumvents theoretical constraints on facialretraction while maintaining functional safetymargins. Further studies incorporating the loca-tion of muscle resultant forces will be required toassess this hypothesis. These, it is hoped, willclarify the significance of mangabey facial formand furnish new insights into functional con-straints limiting primate cranial diversity.

Acknowledgements

I wish to thank Emiliano Bruner for organizing thesymposium in which this research was initially pre-sented and for his subsequent work bringing thisproceedings volume to fruition. I am grateful toScott McGraw for sharing with me his observationson mangabey feeding behavior and his insights intomangabey facial biomechanics. I thank Steve Frostand Tony Tosi for their contributions to thePRIMO primate morphometric database and tothe museums, curators, and collections managerswho have made the compilation of this resource pos-sible. I am personally grateful to RichardThorington and Linda Gordon (National Museumof Natural History, Smithsonian Institution) forpermission to photograph specimens in their careand to Lawrence Heaney and William Stanley(Field Museum of Natural History) for ongoing

43M. Singleton

access to facilities and specimens. I wish to thankEric Delson, the late Leslie Marcus, David Reddy,and members of the NYCEP Morphometrics Groupfor their ongoing contributions to this research.Finally, I am grateful to the colleagues whose adviceand insights inform my work on a daily basis: SteveFrost, Kieran McNulty, Katerina Harvati, MichaelPlavcan, Sandra Inouye, Brian Shea, and EdgarAllin.This work was conducted with NSF supportvia the NYCEP Morphometrics Group (Research &Training Grant BIR9602234, Special ProgramGrant ACI-9982351). Travel funding was provid-ed by Midwestern University. This paper isNYCEP Morphometrics Contribution No. 16.

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