Variation in guenon skulls (I): species divergence, ecological and

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Journal of Human Evolution 54 (2008) 615e637

Variation in guenon skulls (I): species divergence,ecological and genetic differences

Andrea Cardini a,b,*, Sarah Elton b

a Dipartimento del Museo di Paleobiologia e dell’Orto Botanico, Universita di Modena e Reggio Emilia, via Universita 4, Modena 41100, Italyb Functional Morphology and Evolution Unit, Hull York Medical School, University of Hull, Cottingham Road, Hull HU6 7RX, UK

Received 1 June 2007; accepted 21 September 2007

Abstract

Guenons are the most diverse clade of African monkeys. They have varied ecologies, include arboreal and terrestrial species, and can be foundin nearly every region of sub-Saharan Africa. Species boundaries are often uncertain, with a variable number of species and subspecies mostlyrecognised on the basis of their geographic distribution and pelage. If guenon soft tissue patterns show high variability, the same does not seemto hold for skull morphology. Guenon skulls are traditionally considered relatively undifferentiated and homogeneous. However, patterns of var-iation in skulls have never been examined using a large number of specimens sampled across the breadth of species diversity. Thus, in the presentstudy, skulls of adult guenons and two outgroup species are analysed using three-dimensional geometric morphometrics. Three-dimensional co-ordinates of 86 anatomical landmarks were measured on 1,315 adult specimens belonging to all living guenon species except Cercopithecus dryas.Species are well-discriminated using shape but the best discrimination occurs when species have either a long evolutionary history (e.g., Alleno-pithecus nigroviridis) or represent extremes of size variation (Miopithecus sp. and Erythrocebus patas). Interspecific phenetic relationships reflectsize differences. Four main clusters are found that mainly correspond to four size groups: the smallest species (Miopithecus sp.), the largest species(E. patas plus the study outgroups), a group of medium-small arboreal guenons, and a group of medium-large arboreal and terrestrial guenons.Correlations between interspecific shape distances and interspecific differences in size are higher than between shape distances and genetic dis-tances. However, if only the component of interspecific shape variation which is not correlated to evolutionary allometry is used in the comparisonwith genetic distances, correlations are up to 1.4 times larger than those including allometric shape. The smallest correlations are those betweenshape and ecological distances, which is consistent with the lack of clusters clearly reflecting broad ecological specialisations (e.g., arborealityversus terrestriality). Thus, size, which is generally considered more evolutionarily labile than shape, seems to have played a major role in theevolution of the guenons. The incongruence between interspecific shape differences and phylogeny might be explained by a large proportionof shape changes having occurred along allometric trajectories that tend to be conserved within this clade.� 2007 Elsevier Ltd. All rights reserved.

Keywords: Allometry; Cercopithecids; Geometric morphometrics; Size and shape; Morphological distinctiveness; Phylogenetic signal

Introduction

The highly speciose guenons (Primates, Cercopithecini),widespread in sub-Saharan Africa, are an ecologically andbehaviourally varied tribe (Butynski, 2002). Their skull mor-phologies, in contrast, appear to be much less diverse. The

* Corresponding author. Dipartimento del Museo di Paleobiologia e

dell’Orto Botanico, Universita di Modena e Reggio Emilia, via Universita 4,

Modena 41100, Italy.

E-mail addresses: [email protected], [email protected] (A. Cardini),

[email protected] (S. Elton).

0047-2484/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.jhevol.2007.09.022

Cercopithecini primarily comprises arboreal species, manyof which are distinguished on the basis of pelage and calls(Kingdon, 1997). Craniodental features are seen as beingpoor species discriminators, at least within the species-rich ge-nus Cercopithecus (Verheyen, 1962; Wood and Richmond,2000), and have been the subject of remarkably few studies.Given the interest in the taxonomy, ecology, behaviour, andbiogeography of guenons, perceptions of craniodental unifor-mity must surely have contributed to this lack of attention.

The most comprehensive study of guenon craniodental mor-phology to date was conducted by Verheyen (1962), who

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616 A. Cardini, S. Elton / Journal of Human Evolution 54 (2008) 615e637

analysed 221 adult specimens of 13 guenon species using linearmeasurements of cranial, mandibular, and dental characters.Along with noting their general uniformity, lack of diagnosticcharacters, and pronounced sexual dimorphism [explored fur-ther in Cardini and Elton (in press)], he found that allometryhad a strong influence on guenon skull morphology. Interge-neric comparisons of the ratio between interorbital width andglabella-prosthion length, which best discriminated amonggenera, indicated roughly parallel size-based trajectorieswithin the majority of the clade (Verheyen, 1962). The links be-tween body size and morphology in guenons were further high-lighted by Martin and MacLarnon (1988), who, after removingthe effects of body size through the use of residual values ofcranial and dental dimensions, found that adults of the smallestguenon, Miopithecus talapoin, grouped with the largest, Eryth-rocebus patas. It thus appears likely that evolutionary or inter-specific allometry (sensu Klingenberg, 1996, 1998) makes animportant contribution to the morphological divergence of gue-non taxa. It has also been suggested that ontogenetic scalingcontributes to differences in skull form within the clade. Ina comparison of M. talapoin and C. cephus, Shea (1992) deter-mined that skull proportions differed significantly between thetwo species, attributing this to a decrease in growth rates andresultant smaller adult body size in M. talapoin.

The effects of allometric scaling on primate skull morphol-ogy have been the focus of considerable research, reviewedextensively elsewhere (Singleton, 2002). Many studies (e.g.Cheverud and Richtsmeier, 1986; Shea, 1992; O’Higgins andCollard, 2001; Leigh et al., 2003; Leigh, 2006) have investi-gated the role of ontogenetic allometry in determining cranialand mandibular form. Others (e.g., Marroig and Cheverud,2001, 2005; Singleton, 2002; Frost et al., 2003; McNulty,2004) have concentrated on assessing how size contributesto interspecific variation within adults of closely related spe-cies. In neotropical primates, allometry was found to accountfor 20e40% of all morphological variation within each genus,with only small divergence (z30�) of allometric vectors be-tween and within genera, despite at least 30 million years ofevolutionary diversification and considerable variation in abso-lute size (Marroig and Cheverud, 2001, 2005). This indicatesthat although phenotypic means changed during the evolutionof South American monkeys, covariance structure of theirskulls remained relatively constant. The diversification of skullshape occurred mainly along lines of least evolutionary resis-tance (Schluter, 2000) defined by size variation, which, in turn,was generally associated with dietary shifts. When evolutiondid not occur along lines of least evolutionary resistance, theamount and pace of morphological changes were, respectively,small and slow. In Old World primates, size also appears tocontribute to shape differences between taxa (Singleton,2002; Frost et al., 2003; McNulty, 2004). However, in contrastto the conserved patterns evident in neotropical primates, thereappears to be significant diversity in morphological scaling,both ontogenetic (O’Higgins and Collard, 2001) and, to a lesserdegree, static (Singleton, 2002), within the sister clade of theguenons, the Papionini. Specifically, ontogenetic scaling ap-pears to differ between mandrills and the other ‘dog-faced’

monkeys (O’Higgins and Collard, 2001), and adult mangabeys(Cercocebus and Lophocebus) may share a divergent staticscaling pattern when compared to larger-bodied papionins(Singleton, 2002). This indicates that the relationship betweensize and shape in primates is not necessarily straightforward orevolutionarily conserved across the majority of taxa. Investi-gating the effects of allometry on the skulls of the behaviour-ally and ecologically diverse guenons, which [as discussed inCardini and Elton (in press)] exhibit a wide range of bodymasses, will therefore help to shed further light on the linksbetween size and shape in primate morphology.

Examining guenon skull morphologies will also assist indetermining whether hard tissue features of the skull maponto the species boundaries that are indicated by calls, ecol-ogy, geographic range, and soft tissue. Geometric morphomet-rics is an ideal tool for this: demonstrated to be powerfulenough to identify and quantify small inter- and intraspecificdifferences in primate morphology (e.g., Frost et al., 2003;Cardini et al., 2007). Nonetheless, traditional morphometricstudies have identified highly divergent taxa, including Alleno-pithecus nigroviridis (Verheyen, 1962; Martin and MacLarnon,1988) and Miopithecus (Verheyen, 1962), found in molecularanalyses to probably be basal members of the guenon clade(Tosi et al., 2005). The patas monkey, which is ecologicallyand morphologically distinctive, tends also to be separated atthe generic level, although recent molecular data suggestthat as E. patas forms a monophyletic group with the other ter-restrial guenons (the Cercopithecus lhoesti group and C. ae-thiops), it would be better placed in a more inclusiveterrestrial guenon genus, possibly Chlorocebus (Tosi et al.,2004). The majority of guenon species are included in the ap-parently cranially homogeneous Cercopithecus. These hardtissue similarities, alongside a sparse fossil record prior to1 Ma (Leakey, 1988), suggest rapid, recent divergence withinCercopithecus and possibly guenons as a whole. However, re-cent genetic studies have indicated that the tribe has a rela-tively long evolutionary history (Tosi et al., 2005). Based onevidence from X-chromosomal DNA, Allenopithecus splitfrom the rest of the guenons at 9.3� 1.0 Ma, with divergenceof Miopithecus, the terrestrial guenons, and the arboreal gue-nons occurring at 8.1� 1.0 Ma (Tosi et al., 2005). At4.8� 1.2 Ma, the three ‘terrestrial’ guenon taxa (E. patas, C.aethiops, and the C. lhoesti group) diverged, followed by theseparation of the major arboreal lineages (the Cercopithecusmona/C. neglectus/C. diana group and the Cercopithecus mi-tis/C. cephus group) at 4.6� 0.7 Ma. Speciation within the ar-boreal guenons probably happened relatively rapidly duringthe Plio-Pleistocene, with the differentiation of C. mona, C.neglectus, and C. diana at 3.5� 0.6 Ma, and C. mitis and C.cephus at 2.2� 0.6 Ma. The Central African forest belt iscommonly seen as the region where much Plio-Pleistoceneguenon evolution took place (Hamilton, 1988), with the subse-quent dispersal of some taxa, including C. aethiops and C. mi-tis, to other parts of sub-Saharan Africa (Elton, 2007).

The study reported here has two main aims. First, similar-ities in skull shape (phenetic analyses) are used to group spe-cies, with similarity relationships of females compared to

617A. Cardini, S. Elton / Journal of Human Evolution 54 (2008) 615e637

those of males. Given the perceived uniformity of the skullalongside the obvious size and ecological differences ofmany guenons, we are interested in examining the relative im-portance of allometry and ecology in determining skull form.Since the clade probably has a relatively long evolutionaryhistory (Tosi et al., 2004, 2005), we also assess whether ge-netic distances are related to differences in skull shape. Thesecond aim is to assess the degree of morphological diver-gence among species, using anatomical landmarks of the skullin discriminant analyses. This will shed light on whether spe-cies boundaries determined by soft tissue features, biogeogra-phy, and behaviour are mirrored by small but significantdifferences in skull shape.

Materials and methods

Sample and data collection

For the purposes of the current study, and partially in rec-ognition of the fact that published classifications have notyet been revised to reflect new molecular evidence, we followthe classification of Grubb et al. (2003) in recognising fourguenon genera (Allenopithecus, Miopithecus, Erythrocebus,and Cercopithecus) and also accept their species-level taxon-omy. The sample comprised 1,315 adult specimens drawnfrom all living guenon species (Grubb et al., 2003) exceptC. dryas (Table 1). Only one specimen of C. solatus, a poorlystudied species that inhabits a small area of Gabon and isconsidered vulnerable by conservationists, was found in thecollections studied. This specimen was included only in the or-dinations with all species and pooled sexes (PCA and ssPCA,see below), and its missing landmarks were estimated usingthe average of males of the closely related C. lhoesti. The Af-rican monkeys Cercocebus atys and Colobus guereza were in-cluded in the whole study sample as outgroups, with C. atysrepresenting the Papionini (sister clade of the guenons) andC. guereza the Colobinae (sister clade of guenons and papio-nins). The maturity of each specimen was assessed on the basisof third molar and canine eruption. The museums from whichspecimens were derived are listed in the Acknowledgements.

Three-dimensional coordinates of anatomical landmarkswere directly collected by the same person on crania and man-dibles using a 3D-digitiser (MicroScribe 3DX, ImmersionCorporation). Landmarks were digitised only on the left sideto avoid redundant information in symmetric structures. Theset (configuration) of 86 landmarks used for the analysis isshown in Fig. 1 and landmarks are listed in Table 2. Measure-ment error and estimates of missing landmarks (on average 1.6landmarks are missing in 11.0% of the specimens) are de-scribed in Cardini and Elton (in press).

Three registration points were digitised on pieces of plasti-cine stuck on the two condyles and below the incisors of themandible of each specimen. These landmarks were recordedtwice: first, the mandible articulated to the cranium (afterthe digitisation of the cranial landmarks) and, then, on the dis-articulated mandible (after the digitisation of the mandibularlandmarks). The three registration points were chosen in the

form of a large triangle with distant vertices in order to mini-mise the measurement error relative to the size of the triangle.Data collected on the mandible were then aligned onto thesame coordinate system as those collected on the craniumby applying a least-squares superimposition (see below) ofthe three points so that the rigid rotation derived from them ap-plies to all landmark coordinates. Software written in VisualBasic (Jones, unpublished) was used for this. The three land-marks used for matching the cranial and mandibular configu-rations were eventually discarded and only the 86 anatomicallandmarks were used in the analyses.

Geometric morphometrics

In landmark-based geometric morphometrics (Rohlf andMarcus, 1993; Adams et al., 2004), the form of an organism(or its organs) is captured by the Cartesian coordinates ofa configuration of anatomical landmarks. Landmarks are topo-graphically corresponding points (Marcus et al., 2000) that canbe precisely located on all individuals. Geometric morphomet-ric analyses were performed using Morpheus (Slice, 1999),Morphologika (O’Higgins and Jones, 1999), TPSSmall 1.20(Rohlf, 2003), NTSYS-pc 2.2c (Rohlf, 2005), and SPSS11.5.0 (SPSS, 2002).

Differences in landmark coordinates due to the position ofthe specimens during the digitisation process were removed,and size was standardised. This was achieved by optimallysuperimposing landmark configurations using a least-squaresalgorithm (Rohlf and Slice, 1990) that scales configurationsto unit centroid size, centres them on their centroid, and rotatesthe configurations to minimise the sum of squared distancesbetween corresponding landmarks. The process is called gen-eralised Procrustes analysis (GPA). Centroid size is a measureof the dispersion of landmarks around the centroid of the land-mark configuration and is computed as the square root of thesum of squared distances of all landmarks from the centroid.The new Cartesian coordinates obtained after the registrationare the aligned coordinates or shape coordinates used for sta-tistical comparisons of individuals. The shape differencesbetween landmark configurations of two individuals can besummarised by their Procrustes distance (PRD), which is ap-proximately the square root of the sum of squared distancesbetween pairs of corresponding landmarks. Henceforth, wewill refer to Procrustes shape distances by simply using theterm ‘shape distances’ or the abbreviation PRD.

Before statistical comparison of shape variables was under-taken, the registered landmark configurations were projectedto an Euclidean space tangent to the shape space. This approx-imation is done because the shape space (Kendall, 1984) iscurved while standard statistical analyses are performed inan Euclidean space. This is analogous to the approximationof the distance relationship between points of a small regionof the Earth’s surface on a flat map (Rohlf, 1998). Thisapproach is satisfactory when variations are small (Rohlf,2003), as in the present data (results not shown).

An extensive introduction to applications of geometric mor-phometrics in biology is provided by Zelditch et al. (2004).

Table 1

Species samples and missing landmarks

Genus Species (abbreviation) and taxonomic authority Sex n NmissL1 missL1

Allenopithecus nigroviridis (nig) (Lang, 1923) female 7 e e

male 8 e e

Cercopithecus aethiops (aet) (Linnaeus, 1758) female 169 27 2.4

male 227 39 1.7

ascanius (asc) (Audebert, 1799) female 37 2 1.5

male 39 6 1.3

campbelli (cam) (Waterhouse, 1838) female 32 e e

male 31 e e

cephus (cep) (Linnaeus, 1758) female 29 5 1.0

male 29 1 1.0

diana (dia) (Linnaeus, 1758) female 32 2 2.0

male 32 1 1.0

erythrogaster (eryg) (Gray, 1866) female 4 1 1.0

male 5 e eerythrotis (eryt) (Waterhouse, 1838) female 4 1 2.0

male 10 e e

hamlyni (ham) (Pocock, 1907) female 15 5 1.6

male 15 2 1.5

lhoesti (lhoe) (Sclater, 1899) female 16 3 1.3

male 18 2 1.5

mitis (mit) (Wolf, 1822) female 67 3 1.3

male 79 8 1.4

mona (mon) (von Schreber, 1775) female 16 2 1.0

male 19 1 1.0

neglectus (neg) (Schlegel, 1876) female 24 4 1.5

male 27 4 1.5

nictitans (nic) (Linnaeus, 1758) female 24 3 1.7

male 23 2 2.0

petaurista ( pet) (von Schreber, 1774) female 16 1 1.0

male 25 e e

pogonias ( pog) (Bennett, 1833) female 38 2 1.0

male 38 6 1.7

preussi ( pre) (Matschie, 1898) female 3 e e

male 5 1 1.0

sclateri (scla) (Pocock, 1904) female 5 e e

male 6 2 1.0

solatus2 (sol ) (Harrison, 1988) female e e e

male 1 1 7.0

Erythrocebus patas ( pat) (von Schreber, 1774) female 9 2 1.0

male 21 1 1.0

Miopithecus ogouensis (ogo) (Kingdon, 1997) female 16 3 2.3

male 11 1 1.0

talapoin (tal ) (von Schreber, 1774) female 2 e e

male 3 1 1.0

Cercocebus atys (aty) (Audebert, 1797) female 23 e e

male 21 e e

Colobus guereza ( gue) (Ruppell, 1835) female 17 e e

male 17 e e

Total pooled 1,315 145 1.7

1 Abbreviations: NmissL, number of specimens with missing landmarks; missL, average number of missing landmarks in specimens with missing landmarks

(pooling all species and sexes: 1,170 specimens have no missing landmarks, 85 have one, 41 have two, nine have three, three have four, four have five, two

have six, and one has seven).


Detailed mathematical descriptions of geometric morphomet-ric methods are available in Bookstein (1991) and Dryden andMardia (1998). Guidelines on how to implement linear statis-tical models in geometric morphometrics can be found inRohlf (1998) and Klingenberg and Monteiro (2005).

Statistics

Statistical analyses were performed using NTSYS-pc 2.2f(Rohlf, 2005) and SPSS 11.5.0 (2002). Principal componentsanalysis (PCA) of shape coordinates was used to extract major

Fig. 1. Landmark configuration. See Table 1 for definitions.


axes of shape variation. Multivariate regressions of shapecoordinates onto sex or centroid size were used to computevectors (trajectories) of shape variation predicted by the ex-planatory variable. The natural logarithm of centroid sizewas used in all regressions of shape onto size following Mit-teroecker et al. (2004, 2005). Matrix correlation was used tomeasure the similarity of two matrices of pairwise distancesbetween the same taxonomic units. Matrix correlation was cal-culated as the Pearson correlation of distances between anypair of taxonomic units in the first matrix and the correspond-ing distances in the second matrix. Significance was tested us-ing 10,000 random permutations, including observed. Thus,the observed correlation was compared with its permutationaldistribution, which was obtained by comparing the first matrixwith all possible matrices in which the order of cases in theother matrix were permuted (Rohlf, 2005).

UPGMA (unweighted pair-group method using arithmeticaverage) phenograms were used to summarise phenetic rela-tionships described by matrices of shape distances. Discussionis confined to results which are consistently found in ordina-tions and phenograms.

Analysis of the pooled sample in the shape space and size-shape space. The variation in shape was examined by exploring

the shape space and the size-shape space (see below) of all spe-cies with pooled sexes. A PCA of shape coordinates was per-formed and scatterplots of the main axes of variation wereexamined. Forms were compared in size-shape space (Drydenand Mardia, 1998; Mitteroecker et al., 2004). Thus, a principalcomponents analysis (ssPCA) was performed on a matrix thatincludes shape coordinates and log-transformed centroid size.Log-centroid size has the largest variance in this matrix andtherefore the first principal component of the analysis (ssPC1)is closely aligned with size. Thus, ssPC1 summarises shape var-iation correlated to size in the pooled sample regardless ofspecies and can be interpreted as the ‘common’ allometric tra-jectory. The inspection of ssPCs other than the first one providesclues as to shape differences along trajectories that do notsimply follow the direction dictated by the main axis of size var-iation across all study species (including within-species size-related shape differences that may not occur along this axis).In this sense, an ssPCA can be seen as a simple but preliminarytechnique to explore patterns of shape variation that can befurther investigated using specific analyses.

Mean shapes relationships and partial disparity. Meanshapes were computed for each species (separate sexes) andused for examining phenetic relationships. One hundred

Table 2

Definition and numbering of landmarks (L). The terms ‘anterior’ and ‘posterior’ are used with reference to Fig. 1. Landmarks 65 to 86 are on the mandible

L Definition

1 prosthion: anteroinferior point on projection of premaxilla between central incisors

2 prosthion2: anteroinferiormost point on premaxilla, equivalent to prosthion but between central and lateral incisors

3 posteriormost point of lateral incisor alveolus

4 anteriormost point of canine alveolus

5 mesial P3: most mesial point on P3 alveolus, projected onto alveolar margin

6e9 contact points between adjacent premolars/molars, projected labially onto alveolar margin

10 posterior midpoint onto alveolar margin of M3

11e14 contact points between adjacent premolars/molars, projected lingually onto alveolar margin

15 posteriormost point of incisive foramen

16 meeting point of maxilla and palatine along midline

17 greater palatine foramen

18 point of maximum curvature on the posterior edge of the palatine

19 tip of posterior nasal spine

20 meeting point between the basisphenoid and basioccipital along midline

21 meeting point between the basisphenoid, basioccipital, and petrous part of temporal bone

22 most medial point on the petrous part of temporal bone

23 most medial point of the foramen lacerum

24 meeting point of petrous part of temporal bone, alisphenoid, and base of zygomatic process of temporal bone

25e26 anterior and posterior tip of the external auditory meatus

27 stylomastoid foramen

28, 30 distal and medial extremities of jugular foramen

29 carotid foramen

31 basion: anteriormost point of foramen magnum

32, 35 anterior and posterior extremities of occipital condyle along margin of foramen magnum

33 hypoglossal canal

34 centre of condylar fossa

36 opisthion: posteriormost point of foramen magnum

37 inion: most posterior point of the cranium

38 most lateral meeting point of mastoid part of temporal bone and supraoccipital

39 nasospinale: inferiormost midline point of piriform aperture

40 point corresponding to largest width of piriform aperture

41 meeting point of nasal and premaxilla on margin of piriform aperture

42 rhinion: most anterior midline point on nasals

43 nasion: midline point on frontonasal suture

44 glabella: most forward projecting midline point of frontals at the level of the supraorbital ridges

45 supraorbital notch

46 frontomalare orbitale: where frontozygomatic suture crosses inner orbital rim

47 zygo-max superior: anterosuperior point of zygomaticomaxillary suture taken at orbit rim

48 centre of nasolacrimal foramen (fossa for lacrimal duct)

49 centre of optic foramen

50 uppermost posterior point of maxilla (visibile through pterygomaxillary fissure)

51 frontomalare temporale: where frontozygomatic suture crosses lateral edge of zygoma

52 maximum curvature of anterior upper margin of zygomatic arch

53 zygo-max inferior: anteroinferior point of zygomaticomaxillary suture

54 zygo-temp superior: superior point of zygomaticotemporal suture on lateral face of zygomatic arch

55 zygo-temp inferior: inferolateral point of zygomaticotemporal suture on lateral face of zygomatic arch

56 posteriormost point on curvature of anterior margin of zygomatic process of temporal bone

57 articular tuber

58 distalmost point on postglenoid process

59 posteriormost point of zygomatic process of temporal bone

60 foramen ovale (posterior inferior margin of pterygoid plate)

61 meeting point of zygomatic arch and alisphenoid on superior margin of pterygomaxillary fissure

62 meeting point of zygomatic arch, alisphenoid ,and frontal bone

63 bregma: junction of coronal and sagittal sutures

64 lambda: junction of sagittal and lamboid sutures

65 anterosuperior point of mandible between central incisors

66 anterosuperior point of mandible between lateral incisors

67 posteriormost point of lateral incisor alveolus

68 anteriormost point of canine alveolus

69 mesial P3: most mesial point on P3 alveolus, projected onto alveolar margin

70e73 contact points between adjacent premolars/molars, projected labially onto alveolar margin

74 posterior midpoint onto alveolar margin of M3

75e78 contact points between adjacent premolars/molars, projected lingually onto alveolar margin

79 superior tip of coronoid process


Table 2 (continued )

L Definition

80e81 most lateral and most medial points on mandible condylar surfaces

82 anteriormost point on roughening for attachment of masseter on inferior margin of the angle of mandible

83 mandibular foramen

84 posteriormost point on superior area of insertion of medial pterygoid

85 region of insertion of genioglossus muscles (midline posteriormost point on upper ‘ridge behind incisors’)

86 region of insertion of geniohyoid muscles (midline posteriormost point on lower ‘ridge behind incisors’)


bootstrap samples were built for each species (separate sexes),and bootstrapped species mean shapes were computed. For in-stance, 100 bootstrap samples of n¼ 37 were built using the37 females of C. ascanius and the mean was computed foreach of them (hence, producing 100 bootstrap means for thisspecies). Thus, for each species (with separate analyses for fe-males and males) 100 means are generated by bootstrappingthe original sample and computing a new mean for each boot-strap sample. In general, the number of independent bootstrapsamples is given by (2n�1)!/n!(n�1) (Zelditch et al., 2004): itis 3 with n¼ 2; 10 with n¼ 3; 70 with n¼ 4; 756 with n¼ 5and so on. The number of unique bootstrap means of thesmallest samples will therefore be smaller than the numberof bootstraps (100). The sample of M. talapoin usefully illus-trates the effect of bootstrapping small samples. Just two spec-imens (tal1, tal2) are available in the female sample andresampling with replacement can only produce three differentbootstrap samples: tal1þ tal1, tal2þ tal2, and tal1þ tal2(hence, three different means). These means might haveshapes identical (e.g., tal1þ tal1) or very similar (tal1þ tal2)to the real specimens. A PCA of observed and bootstrappedmean shapes of each species was performed, and scatterplotsof bootstrap means together with 95% confidence ellipseswere drawn to show the relative position of the means togetherwith the variation around their estimates.

Cluster analyses were performed on the matrix of shape dis-tances of observed means and on bootstrapped species meanshapes. Thus, the mean of the first bootstrap sample for A. nigro-viridis was analysed together with that of the first bootstrap sam-ple of C. aethiops plus that of the first bootstrap sample of C.ascanius and so on for all 23 species. This was done 100 times.Then, pairwise shape distances between the 23 species means ofthe first bootstrap were computed and an UPGMA phenogramcalculated. This was done for all 100 bootstrap samples, produc-ing 100 phenograms. Eventually, a 50% majority rule consensustree of the 100 phenograms (plus the observed) was built andpercentages of phenograms supporting the observed topologywere shown. Bootstrap support of phenogram clusters providesinformation on how consistently a cluster is found in pheno-grams when species means are computed after removing somespecimens and replacing them with others in the same sample.Thus, it indicates how inaccuracies of estimates of mean shapes(based on available samples) might influence the reconstructionof species phenetic relationships.

The contribution of each species (separate sexes) to the gue-non and outgroup shape diversity (disparity) was examined.Shape distances of every species mean to the grand mean of allspecies were computed. The ratio between the squared shape

distance of a species and the sum of squared shape distances ofall species measures the amount of shape disparity in the groupthat is accounted for by said species. This metric is called partialdisparity (Zelditch et al., 2004). For instance, among females, the(squared) shape distance to the grand mean of all species for A.nigroviridis is 0.00256, the C. diana distance is 0.00126, andthe sum of (squared) distances of all species is 0.0633. Thus,A. nigroviridis explains about 4% [(100� 0.00256)/0.0633] ofthe differences between the species mean shapes and their grandmean, whereas C. diana explains about 2%. Although a rigoroususe of the term ‘divergence’ implies a distance between a speciesand its ancestor (which is unknown in the absence of fossils, andwhose estimates based on present species traits and their putativephylogeny can be strongly affected by errors: Martins, 1999),a more relaxed convention is adopted here. We use ‘divergence’to indicate how much a species contributes to total disparity rel-ative to the grand mean of all species. Thus, in the present exam-ple, the divergence in shape of A. nigroviridis relative to the grandmean might be said to be about twice that of C. diana.

The relative position in the shape space of female meanswas compared to that of males. This was achieved by comput-ing a matrix correlation between the matrices of shape dis-tances of the two sexes. Shape distances of mean shapeswere also compared to the genetic distances. Genetic distanceswere reconstructed using the topology of the phylogenetic treeof Tosi et al. (2005: 64, their Fig. 3). Tree branches are propor-tional to the number of substitutions in the sequences of thew9.3 kb frangment of X-chromosomal DNA used by Tosiet al. (2005) for inferring guenon phylogeny. Thus, measuresof branch lengths give a good approximation of the geneticdistances in the tree and can be used to build a matrix of pair-wise genetic distances (COPH module of NTSYSpc, additivedistances options). This matrix was used for comparisonswith shape distances including species in common betweenthe two analyses and using Miopithecus talapoin and Cercoce-bus agilis instead of M. ogouensis and C. atys in the geneticdistance matrix. Miopithecus talapoin and M. ogouensiswere not considered separate species until 1997 (Kingdon,1997) and no information is available in Tosi et al. (2005) toassess whether the zoo specimen used in their genetic samplebelongs to one or the other population. Miopithecus is stronglydivergent for skull shape but M. talapoin and M. ogouensis arerelatively similar to each other. M. ogouensis is included in theshape dataset because of its larger sample. Cercocebus agilisand C. atys are members of a monophyletic group of closelyrelated species together with C. torquatus. Thus, their geneticdifferences should be negligible compared to those betweenCercocebus and the guenons.


Shape distances were also compared to ecological dis-tances. Data on ecology were taken from the literature (Fedi-gan and Fedigan, 1988; Gautier-Hion, 1988a,b; Isbell, 1998;Isbell et al., 1998a,b; Nakagawa, 1999; Chapman et al.,2002; Curtin, 2002; Nunn, 2002; Nunn et al., 2004). Diet (in-sects, flowers/nectar, fruits/seeds, fibrous vegetation/leaves),habitat (tropical rain forest, deciduous forest, woodland,swamps, flooded, forest, gallery forest, scrub, scrub forest, sa-vanna), and locomotion (arboreal, terrestrial) were tabulatedusing categorical variables as in Jernvall and Wright (1998),with the importance of each dietary category, habitat, and lo-comotor mode ranked (up to a maximum of five) for each spe-cies. Euclidean distances based on ecological variables werecomputed and a three-way Mantel test, which calculates thepartial correlation between shape and ecology while holdingthe effect of phylogeny constant, was performed (Legendreand Legendre, 1998; Harmon et al., 2005; Kozak et al.,2005). This was done in order to factor out potentially con-founding effects of the phylogenetic hierarchy. In all cases,significance was assessed by comparing the correlation ofthe actual matrices to those from 9,999 random permutations(Harmon et al., 2005; Kozak et al., 2005; Rohlf, 2005).

Species discrimination. Species discrimination was exam-ined using discriminant analyses (DA) of shape on sampleswith separate sexes. A ‘standard’ DA was performed usingthe first 30 PCs of shape variance to generate Mahalanobis dis-tances, which measure the differences between groups relativeto the within group variation. Mahalanobis distances wereused to compute the number and percentage of specimens cor-rectly classified according to species.

In addition, a DA that used Procrustes shape distances toassign individuals to species was performed. A similar appli-cation of shape distances for classification can be found inMcNulty et al. (2006). This approach does not modify the spa-tial relationships of the specimens in the shape space, and thusrelates differences to their absolute magnitude rather than tothe observed variation (see Klingenberg and Monteiro, 2005,for a discussion of properties of the shape space after theGPA and when GPA coordinates are used in general linearmodels). Congruence of classifications in the transformedshape space of Mahalanobis distances and in the original un-transformed Procrustes shape space suggests robustness of re-sults and their independence of the analytical method. Thus,the following criteria were used for the ‘Procrustes DA’:

A specimen of species X was assigned to species X if:

1) it was closer to the mean of X than to the mean of anyother species;

2) it was closer to the mean of a species Y (other than X) butwithin 95th percentile of distances to the mean shape ofspecies X and outside 95th percentile of distances to themean shape of species Y.

A specimen of species X was assigned to species Y if:

1) it did not satisfy any of the conditions (above) for belong-ing to X;

2) it was closer to the mean of species Y and within the 95th

percentile of distances to the mean shape in species Y;3) it was closer to the mean of species Y and outside the 95th

percentile of distances of both species (X and Y).

Analyses were cross-validated using 50% hold-out samples(Hair et al., 1998). Thus, 50% of the specimens (analysis sam-ple) were randomly selected and used for computing the dis-criminant functions (or the shape distances percentiles) andthese functions used for classifying the remaining 50% of in-dividuals (hold-out sample).

The sample of C. aethiops was much larger than that of anyother species. To test the effects of this large sample on anal-yses, DAs were repeated to include only a random subsampleof C. aethiops of equal size to the average species sample size(20 for females and 22 for males).

Results

Analysis of the pooled sample in the shape space andsize-shape space

The scatterplot (Fig. 2) indicates that those species that rep-resent opposite extremes of guenon size variation (smallestspecies, M. talapoin and M. ogouensis, Fig. 2: line A1; largestspecies, E. patas, Fig. 2: line A2) can be discriminated alongthe first two PCs of shape (Fig. 2). The outgroup specieswere separated from guenons along PC2, a result most clearlyseen in C. guereza (Fig. 2: line A3). In addition, Cercopithecushamlyni, an arboreal species of comparable size to most otherguenons but with a distinctive skull morphology, can also bedistinguished (Fig. 2: line A4).

Examination of the first four axes of the size-shape space(Fig. 3) provides further insights into general patterns of gue-non skull shape variation. To aid the interpretation of the seriesof bivariate plots of Fig. 3, one can imagine ssPC1, ssPC2, andssPC3 as if they were sides of a transparent box full of pointsin which relative distances are proportional to size-shape dif-ferences. Examining variation along ssPC1 and ssPC2 is likelooking through the surface defined by the two longest sidesof the box. Examining ssPC2 and ssPC3 is analogous to look-ing through the top of the box (and so on for other ssPCs).Thus, ssPC1 summarised the common allometric trajectorythat goes from Miopithecus to Erythrocebus (Fig. 3A: linesA1e2). Alternatively, ssPC2, ssPC3 and ssPC4 help visualisethe most evident deviations from this trajectory. That is,ssPC2 separated guenons and outgroups (C. atys, Fig. 3B:line B1; C. guereza, Fig. 3B: line B2) and, to some degree,C. hamlyni from most other guenons (Fig. 3B: line B1). AndssPC3 and ssPC4 showed three main clusters: 1) outgroup spe-cies (Fig. 3C: line C1), 2) C. aethiops (Fig. 3B, C: lines B3eC2), and 3) all other species.

Mean shapes relationships and divergence

Scatterplots of the first two PCs (species means with sepa-rate sexes) summarise similarity relationships of guenons

Fig. 2. Scatterplots of PC1 and PC2 of shape variables of all species with pooled sexes. Percentages of explained variance in parentheses, abbreviations of species

names in this and other figures are given in Table 1. Lines are drawn which emphasise main clusters (lines A1,2,3,4) described in the Results.


(Fig. 4). The PCA of female and male mean shapes indicatedsimilar phenetic relationships. This observation is consistentwith the high correlation between matrices of female andmale mean shape distances (r¼ 0.920, p¼ 0.0001). Ninety-five percent confidence ellipses around means suggested largeerrors in estimates of species mean shapes for the smallestsamples. For instance, large variation in bootstrap mean shapeswas found in C. erythrotis, for which fewer than ten specimensof each sex are available, while variation of means was verysmall in C. aethiops and C. mitis, which represent the largestsamples in the analysis.

The colobine C. guereza was separated completely from allother species (Fig. 4A, B: lines A1eB1). Both Miopithecusspecies were also clearly isolated (Fig. 4A,B: lines A2eB2).In addition, C. atys (the papionin outgroup), E. patas, and C.hamlyni had mean shapes in which the variation did not appre-ciably overlap with that of other species (Fig. 4A,B: lines A3eB3). Miopithecus and E. patas lie at opposite extremes of therange of guenon size variation. Miopithecus is characterisedby a very short face with large orbits and a relatively largeneurocranium (Figs. 5 and 6). This trend is reversed in E. patas(Figs. 5 and 6). C. hamlyni also has a relatively long face.However, compared to E. patas, its face is relatively flatterand its nasals longer.

The remaining species mean shapes cluster in the centralarea of the plot and show partly overlapping ranges. Twomain clusters can be identified (Fig. 4A,B: lines A4e5eB4e5),which largely corresponded to variation in skull size.

Excluding species with extremely small or large body masses(Miopithecus and Erythrocebus), the guenon sample can besubdivided into two size groups. Skulls larger than the medianof species average sizes in both sexes were found in Allenopi-thecus nigroviridis, the terrestrial taxa C. aethiops, C. lhoesti,and C. preussi, and the arboreal C. diana, C. hamlyni, C. mitis,C. neglectus, and C. nictitans. These species usually plot to theleft of the dashed line shown in Fig. 4 (lines A4eB4). All otherarboreal guenons had average skull sizes smaller than the me-dian and are mostly found to the right of the dashed line. Con-sistent with the general trend of allometric shape variation,small and large species of Cercopithecus tend to have skullsof shape intermediate between Miopithecus and Erythrocebus.Thus, the former are somewhat reminiscent of Miopithecusand the latter of Erythrocebus [compare, for instance, C. dianaand C. ascanius in Fig. 3 of the companion paper (Cardini andElton, 2008)].

The discrimination of clusters of species mean shapes andits correlation to size differences is effectively visualised inthe phenograms of female and male mean shapes (Figs. 5and 6). Shape distances between means of any two speciescorrelated to the corresponding absolute differences in skullaverage size (female r¼ 0.842, p¼ 0.0001; male r¼ 0.870,p¼ 0.0001).

The relative contribution of each species to the diversity inspecies mean shapes is shown in Table 3 using percentages ofpartial disparity. Females and males exhibited similar patterns.The most distinctive skull shapes were found in the outgroup

Fig. 3. Scatterplots of the first four principal components (ssPC) of the size-shape space with pooled sexes (percentages of explained variance in parentheses).

A) Variation along the axis of the common allometry (ssPC1). B and C) Variation orthogonal to the axis of the common allometry. Note that axes in A, B,

and C are not on the same scale. Lines are drawn which emphasise main clusters (A1,2; B1,2,3; C1,2) described in the Results.

Fig. 4. Scatterplots of PC1 and PC2 of species mean shapes with separate sexes (percentages of explained variance in parentheses; in both sexes, the correlation of

PC1 with size is larger than 0.94, p< 0.00001, and smaller than 0.18 and not significant for all other PCs). For each species, variation around the mean is illustrated

with 95% confidence ellipses of bootstrap mean shapes (not computed for M. talapoin females because n is too small). A, Female means. B, Male means. Lines are

drawn which emphasise main clusters (lines A1,2,3,4,5; B1,2,3,4,5) described in the Results.


and in the smallest and largest guenons (Erythrocebus andMiopithecus). C. hamlyni and A. nigroviridis also had diver-gent shapes. All other species, arboreal and terrestrial, hadsimilar magnitudes of shape differences to the grand mean.Cercopithecus nictitans, C. campbelli, and C. mona wereamong the least divergent, for both sexes.

Scatterplots of bootstrap mean shapes (Fig. 4), and unre-solved or poorly supported polytomies in phenograms (Figs.5 and 6), indicate that means of species with small sampleswere strongly affected by sampling error. Thus, the smallestsamples (where n< 15) were excluded before comparingshape similarity relationships with phylogeny.

Shape distances were first compared with absolute differ-ences in skull size (Fig. 7A1eB1), to verify that the correlation

between species phenetic relationships and size also holds forthe subsample of 17 species included in the comparison withgenetic distances. Correlations were slightly smaller thanwhen all species were included but still remained high(r� 0.818, p¼ 0.0001). Shape distances were compared to ge-netic distances using a test for matrix correlation (Harmonet al., 2005; Polly, 2005). Thus, the correlation between shapedistances of all pairs of species mean shapes and correspond-ing genetic distances could be calculated (Fig. 7A2eB2).Corrections for possible deviations from linearity of the rela-tionships between shape and genetic distances were not usedbecause nonlinear models (including logarithmic, power, andpolynomial) did not produce large increases in the goodnessof fit of the model (increase in r2� 0.060). Correlations

Fig. 5. Phenogram of the species female mean shapes with ‘bootstrap support’ of clusters (percentages of congruent branches of phenograms computed using mean

shapes of 100 bootstrap samples of the original species sample). Species are subdivided in four groups based on average skull size and groups are shown using

different background colours for species names (small: white; medium: light grey; large: dark grey; ‘extra’ large: black). A representative of each size group (in-

dicated with S, M, L, XL) is shown by the phenogram with both pictures and surface rendering of the skull. The asterisk (*) indicates the outgroup species.


were 0.613 (p¼ 0.0052) for females and 0.544 (p¼ 0.0070)for males. Another test was performed after regressing outshape variance correlated to common evolutionary allometryof mean shapes. A matrix of Euclidean distances was com-puted on the residuals of the regression of shape onto sizeand compared to the matrix of genetic distances. Correlationsbetween ‘nonallometric’ shape and genetic distances were0.695 (p¼ 0.0008) for females and 0.746 (p¼ 0.0003) for

males (Fig. 7A3eB3). Finally, shape distances were comparedto ecological differences with the effect of phylogeny heldconstant (Fig. 7A4eB4). Correlations in the three-way Manteltests were 0.182 for females and 0.343 for males (r¼ 0.362 forfemales and 0.116 for males, if nonallometric shape is used).Tests for correlations between shape and ecology without con-trolling for phylogeny (i.e., simple correlations between matri-ces of shape and ecological distances) produced results very

Fig. 6. Phenogram of the species male mean shapes with ‘bootstrap support’ of clusters. See Fig. 5 for legend.


similar to three-way Mantel tests. None of the correlationswith ecological distances were highly significant (p> 0.01).

Species discrimination

The standard DA and the discrimination based on shapedistances gave similar results (Table 4; Mahalanobis distancesfor comparison are given in Tables 5 and 6). Eighty to ninetypercent of specimens were, on average, classified to the correctspecies. In species with the largest classification errors, each

sex tended to classify relatively poorly. Identification errorswere larger in species with larger shape variance (correlationsbetween average percentages of misclassified specimens andshape variance were �0.487; p< 0.05) and smaller in thosewith strongly divergent shapes [correlations between averagepercentages of misclassified specimens and partial disparities(Table 3) were ��0.423; p< 0.05].

C. diana, C. mona, and C. nictitans had classification errorslarger than 15% in both sexes. In C. ascanius, over 15% of fe-males and close to 15% of males were misclassified. The male

Table 3

Partial disparities (percentages) with standard errors estimated using 100 boot-

straps (Zelditch et al., 2004). Asterisk (*) in this and other tables indicates

small samples (n< 15)

Species Female Male

Allenopithecus nigroviridis 4.0� 0.5 4.3� 0.4

Cercopithecus aethiops 1.8� 0.1 1.5� 0.1

Cercopithecus ascanius 1.6� 0.2 1.9� 0.2

Cercopithecus campbelli 1.2� 0.1 0.7� 0.1

Cercopithecus cephus 1.0� 0.2 1.8� 0.2

Cercopithecus diana 2.0� 0.3 1.3� 0.2

Cercopithecus erythrogaster* 2.6� 0.6 2.7� 0.5

Cercopithecus erythrotis* 3.4� 0.8 0.6� 0.3

Cercopithecus hamlyni 4.8� 0.4 5.9� 0.6

Cercopithecus lhoesti 2.1� 0.2 2.7� 0.3

Cercopithecus mitis 2.2� 0.2 2.1� 0.2

Cercopithecus mona 0.9� 0.2 0.9� 0.2

Cercopithecus neglectus 3.1� 0.2 2.4� 0.3

Cercopithecus nictitans 1.3� 0.2 0.7� 0.2

Cercopithecus petaurista 1.4� 0.2 1.5� 0.2

Cercopithecus pogonias 1.7� 0.2 1.6� 0.1

Cercopithecus preussi* 3.0� 0.8 2.5� 0.6

Cercopithecus sclateri* 2.4� 0.5 3.2� 0.5

Cercopithecus solatus* e e

Erythrocebus patas 6.9� 0.5 10.2� 1.1

Miopithecus ogouensis 16.9� 0.8 16.4� 0.8

Miopithecus talapoin* 10.1� 0.7 14.9� 0.9

Cercocebus atys 7.4� 0.4 7.3� 0.4

Colobus guereza 18.2� 0.7 13.0� 0.6


C. campbelli, C. erythrotis, C. petaurista, and C. pogoniassamples had classification errors in excess of 15%, and thisalso occurred in close to 15% of the females. In addition,over 15% of C. preussi males were misclassified. All thesespecies, except C. preussi, belong to the arboreal guenon cladeand have intermediate skull size.

Results of the classifications of males were validated afterexcluding the five smallest samples (C. erythrogaster, C. eryth-rotis, C. preussi, C. sclateri, and M. talapoin) by repeating theanalysis using a 50% hold-out sample. The percentages of cor-rectly identified specimens (hit ratios) in this sample were verysimilar to or higher than in the analysis that included all species.In the hold-out sample, hit ratios were smaller, and the total per-centage of correctly classified specimens was 88.4% in the DA(first 30 PCs, equal a priori probabilities) and 82.9% using thePRD. Similarly, results of the female classifications were vali-dated after excluding the three smallest samples (C. eryth-rogaster, C. preussi, M. talapoin) by repeating the analysiswith a 50% hold-out sample. As in the males, the hit ratios inthis sample were very similar to or higher than in the analysisof all species, while in the hold-out sample hit ratios weresmaller and the total percentage of correctly classified speci-mens was 82.8% in the DA and 82.5% using the PRD.

Including more than the first 30 PCs produced a negligibleincrease in the hit ratios in all DA (all species or the subsetused for validation). In all cases, the matrix of Euclidean dis-tances computed using only the first 30 PCs had a very highcorrelation (r> 0.994) with the matrix of PRD computed inthe full shape space. Thus, relationships among specimensare accurately summarised in the space of the first 30 PCs.

Also, percentages of misclassified specimens in the DA that in-cluded all individuals versus those with a subsample of C. ae-thiops of equal size to the average species sample size differed,on average, by less than two units (r� 0.946, p< 0.001; differ-ence in means not significant in paired t-tests).

Discussion

Size and shape relationships

Size appears highly influential in determining overall skullshape within the guenon clade. Alongside the strong, allomet-rically conserved sexual dimorphism evident in the sample[discussed in the companion paper (Cardini and Elton,2008)], discrimination between large and small species oc-curred along the trajectory of common allometry summarisedby the first axis of variation in size shape space (ssPC1). In or-dinations and phenograms, species mean shapes clusteredlargely according to size variation, although groups based onphylogeny were also found (for instance, C. campbelli andC. mona or C. ascanius and C. cephus). Clustering of speciesby size might be explained by either homoplasy or symplesio-morphy. Moreover, a propensity to have similar shapes in spe-cies of similar size (‘similarity’) may be present in a cladewhere shape variation has a strong allometric component.Thus, although phenotypic means have changed during the ra-diation of guenons (as shown by high percentages of correctlyclassified individuals in discriminant analyses, discussed fur-ther below), a general pattern of changes in skull proportionscorrelated to size differentiation has been conserved. This isalso suggested by the almost parallel static (intraspecific) al-lometries observed in guenons and reported in the companionpaper (Cardini and Elton, 2008), partly contrasting with stud-ies on the sister clade of guenons, the papionins, in whichintraspecific ontogenetic and interspecific adult scaling pat-terns were found to display a variable degree of divergence(O’Higgins and Collard, 2001; Singleton, 2002).

The high correlation between the mean shape distance ma-trices of males and females indicates that similarity relation-ships are alike in the sexes. Considered in the light of theconserved allometric model of skull shape sexual dimorphism,a simple interpretation for such high congruence rests on thefact that sex trajectories are almost parallel (Cardini and Elton,2008). Thus, female and male mean shapes are different, butrelative positions of species are similar because sexually di-morphic traits are produced by sliding species-specific shapesalong lines of shape variation that are nearly parallel. How-ever, large variation of bootstrap mean shapes around observedmean shapes indicates that similarity relationships might bestrongly affected by sampling error, and inferred patternscould thus be misleading. Interestingly, males seem to bemore strongly affected by uncertainties in patterns of pheneticrelationships. A large number of clusters is weakly supportedin the male phenogram. These are the clusters that are inconsis-tently found in cluster analyses of bootstrapped mean shapes.Males also have slightly lower percentages of correctly classi-fied specimens in discriminant analyses and a larger number

Fig. 7. Matrix correlations between shape distances (in units of Procrustes shape distances), absolute differences in size (mm), genetic distances (arbitrary unit of measure expressing relative lengths of tree

branches from Tosi et al., 2005), and ecological distances (arbitrary units; see Material and methods). All correlations are highly significant (p< 0.01) except those with ecological distances. Scatterplots of shape

distances between all pairs of species mean shapes and the corresponding differences in average size, genetic distances, or ecological distances. A) Females; B) Males. A1eB1: shape (including allometric shape)

onto size; A2eB2: shape (including allometric shape) onto genetic distances; A3eB3: nonallometric shape onto genetic distances; and A4eB4: shape (including allometric shape) onto ecological distances after

controlling for phylogeny.

62

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Table 4

Percentages of correctly classified specimens using discriminant analyses

based on discriminant functions computed using the first 30 PCs of shape

(which account for 77.1% and 78.2% of variance in females and males, respec-

tively) or using Procrustes shape distances (PRD)

Species Females Males

PCs PRD PCs PRD

Allenopithecus nigroviridis 100.0 100.0 100.0 100.0

Cercopithecus aethiops 94.7 93.5 94.7 93.8

Cercopithecus ascanius 73.0 73.0 87.2 84.6

Cercopithecus campbelli 87.5 90.6 80.6 80.6

Cercopithecus cephus 86.2 79.3 82.8 79.3

Cercopithecus diana 78.1 71.9 78.1 78.1

Cercopithecus erythrogaster* 100.0 100.0 100.0 100.0

Cercopithecus erythrotis* 100.0 100.0 50.0 60.0

Cercopithecus hamlyni 100.0 100.0 93.3 100.0

Cercopithecus lhoesti 100.0 100.0 88.9 94.4

Cercopithecus mitis 91.0 85.1 89.9 84.8

Cercopithecus mona 81.2 75.0 78.9 78.9

Cercopithecus neglectus 100.0 100.0 100.0 96.3

Cercopithecus nictitans 79.2 62.5 47.8 47.8

Cercopithecus petaurista 100.0 100.0 80.0 84.0

Cercopithecus pogonias 76.3 86.8 84.2 78.9

Cercopithecus preussi* 100.0 100.0 80.0 80.0

Cercopithecus sclateri* 100.0 100.0 100.0 100.0

Erythrocebus patas 100.0 100.0 85.7 85.7

Miopithecus ogouensis 100.0 100.0 90.9 90.9

Miopithecus talapoin* 100.0 100.0 100.0 100.0

Cercocebus atys 100.0 100.0 100.0 100.0

Colobus guereza 100.0 100.0 100.0 100.0

Total % 90.6 88.9 88.3 87.3


of species that include misclassified individuals (16 compared tonine in females). Although within species sample shape varianceis similar in the two sexes (female average variance¼ 0.00299,male average variance¼ 0.00303, paired two-tailed t-testt22¼�0.362, p¼ 0.720), within species size variation is signif-icantly larger in males (female average SD¼3.2, male SD¼ 5.5, paired two-tailed t-test t22¼�4.194,p¼ 0.0004). Larger variation in the size of males might be re-lated to an extension of the growth period that contributes to sex-ual dimorphism and has as a by-product a higher frequency ofextreme phenotypes in species, like guenons, with a strong allo-metric model of shape variation. These specimens are morelikely to be misclassified, as suggested by high percentages ofmisclassified individuals of either sex (17.8% for males,10.5% for females) who lay outside the 95% interval of withinspecies size variation. However, whether larger variation inmale size also contributes to increased uncertainties in clustersof male mean shapes is less clear.

Sampling error notwithstanding, the smallest and largest gue-non genera, Miopithecus and Erythrocebus, were consistently dis-tinguished from other guenon species, discriminated along thefirst two PCs of shape as well as being among the most divergentin the partial disparity analysis. Miopithecus is at least as distant asthe colobine outgroup when compared to the grand mean of allspecies for either sex. At the opposite extreme of size variation,the skull of Erythrocebus patas is slightly less distinctive thanthose of the Miopithecus species, but is still further from the grandmean than is the skull of the papionin outgroup, C. atys.

Miopithecus belongs to an ancient guenon lineage (Tosiet al., 2005), but it is also the smallest living African monkey,commonly perceived as a ‘dwarf’ genus. Verheyen (1962) com-mented on the ‘aberrant’ nature of Miopithecus cranial shape,explained by Shea (1992) as a product of rate hypomorphosis,a decrease in growth rate over a given time. The ecological con-ditions under which selection for small body size occurred inMiopithecus are still largely unexplored. Dietary niche parti-tioning might be one explanation, given the observation thatover one third of the talapoin diet is insects (Gautier-Hion,1978). However, as Shea (1992) points out, such supplementa-tion may not have been the prime mover in the evolution ofsmaller body size. What proportion of its distinctive morphol-ogy results from its small (probably derived) size as opposedto its relatively long evolutionary history requires furtherinvestigation. This is particularly true given a very recent phy-logenetic analysis on 11 species of guenons using short inter-spersed elements (Xing et al., 2007) that confirmed all themain clades reported by Tosi et al. (2005) but shed doubts onthe evolutionary age of Miopithecus by suggesting it could beclosely related to the arboreal guenons and thus may havediverged more recently than originally thought.

Patas monkeys have acquired distinct adaptations to terres-trial life and large home range areas (Gebo and Sargis, 1994;Isbell et al., 1998b). Terrestrial primates tend to be larger thanthose that are arboreal, and increased body mass may conferadvantages through protection from predation, increased ther-moregulatory efficiency, and buffering against food shortages.Home range area is often linked to habitat productivity, whichin many cases is a function of rainfall (Isbell et al., 1998b).The large home range areas of patas monkeys are likely tobe a response to relatively unproductive habitats (Isbellet al., 1998b). It has also been noted that E. patas is subjectto greater seasonality and a more unpredictable environmentthan is usually the case for guenons (Cords, 1987). Life historystrategies of E. patas appear to reflect this; it has a younger ageat first birth and shorter interbirth intervals than would be ex-pected for a guenon of its body mass (Nakagawa et al., 2003).If environmental selective pressures were intense enough to in-fluence life history evolution they may well have also affectedbody mass, which in turn appears to have contributed to thedivergent cranial morphology of E. patas.

The strong links between the extremes of shape and size di-vergence suggest that allometry has played a central role in theevolution of guenon skull morphology. Indeed, in the speciesanalysed, shape distances correlated most strongly with sizevariation, although shape was also significantly correlatedwith genetic distances. Correlations between shape and ge-netic distance became larger when size-independent shape var-iation was analysed. This indicates that strongly divergentshapes that make similarity relationships inconsistent withphylogeny are partly a by-product of size divergence. Correla-tions between size and shape were also much larger than thosebetween shape and ecology, reinforcing the importance of al-lometry in determining skull shape in guenons.

Whether, or to what extent, guenon skull shape variationhas been produced by simple extension or truncation of

Table 5

Mahalanobis distances between centroids and Procrustes distances between species means are shown for females of all study species below and above the main diagonal, respectively. Abbreviation for species

names are shown in Table 1

nig aet asc cam cep dia eryg* eryt* ham lhoe mit mon neg nic pet pog pre* scla* pat ogo tal* atys gue

nig e 0.057 0.075 0.060 0.068 0.050 0.072 0.086 0.058 0.055 0.043 0.057 0.050 0.053 0.070 0.072 0.065 0.076 0.067 0.136 0.115 0.068 0.111

aet 7.36 e 0.058 0.049 0.050 0.043 0.058 0.060 0.065 0.042 0.049 0.043 0.050 0.044 0.050 0.056 0.052 0.060 0.064 0.119 0.095 0.075 0.100

asc 8.02 7.31 e 0.042 0.022 0.059 0.042 0.039 0.077 0.056 0.059 0.039 0.068 0.047 0.033 0.024 0.055 0.033 0.087 0.089 0.068 0.087 0.122

cam 7.28 7.36 5.17 e 0.037 0.049 0.049 0.057 0.057 0.050 0.051 0.024 0.051 0.044 0.039 0.040 0.055 0.052 0.075 0.101 0.082 0.070 0.116

cep 7.95 6.62 2.54 4.84 e 0.048 0.044 0.042 0.072 0.049 0.051 0.035 0.059 0.035 0.026 0.026 0.053 0.038 0.084 0.098 0.076 0.080 0.113

dia 7.07 5.97 5.92 5.69 4.89 e 0.062 0.067 0.061 0.042 0.028 0.046 0.037 0.025 0.048 0.059 0.055 0.061 0.066 0.131 0.108 0.076 0.096

eryg* 6.96 6.45 5.04 6.24 5.76 6.47 e 0.051 0.073 0.060 0.064 0.046 0.069 0.058 0.047 0.047 0.065 0.038 0.083 0.097 0.080 0.086 0.126

eryt* 8.76 6.82 4.13 5.51 4.52 6.31 5.40 e 0.092 0.064 0.070 0.053 0.079 0.058 0.044 0.045 0.064 0.042 0.097 0.098 0.074 0.100 0.118

ham 8.10 8.23 8.69 7.83 8.17 6.89 8.19 10.00 e 0.058 0.059 0.061 0.056 0.065 0.075 0.076 0.067 0.078 0.059 0.125 0.107 0.069 0.135

lhoe 7.53 5.82 6.62 7.09 5.88 5.32 7.17 7.09 6.47 e 0.043 0.048 0.051 0.043 0.054 0.057 0.042 0.058 0.068 0.125 0.103 0.071 0.110

mit 5.65 6.35 6.09 6.43 5.70 3.80 6.45 6.53 7.36 5.54 e 0.047 0.039 0.027 0.052 0.058 0.057 0.062 0.068 0.135 0.109 0.070 0.098

mon 6.92 6.34 4.81 3.31 4.73 5.21 5.62 5.39 8.30 6.97 5.84 e 0.052 0.039 0.039 0.033 0.052 0.045 0.072 0.102 0.081 0.073 0.115

neg 7.12 6.50 6.46 5.71 5.94 4.85 6.70 6.90 7.45 6.41 5.57 6.02 e 0.042 0.059 0.067 0.065 0.070 0.066 0.134 0.112 0.075 0.103

nic 6.81 5.88 4.97 5.44 3.83 2.87 6.39 5.55 7.80 5.39 3.18 4.79 4.84 e 0.038 0.047 0.055 0.052 0.074 0.124 0.099 0.074 0.098

pet 7.77 6.54 4.43 4.40 3.61 4.84 5.57 4.56 8.16 6.65 5.45 4.87 5.41 4.20 e 0.037 0.058 0.043 0.085 0.103 0.079 0.082 0.108

pog 7.98 7.45 3.39 4.98 3.71 6.46 6.25 5.29 9.26 7.49 6.66 3.55 6.97 5.32 5.08 e 0.059 0.041 0.087 0.091 0.070 0.086 0.122

pre* 6.96 6.50 6.47 6.74 6.05 5.81 7.33 7.43 6.74 4.46 5.86 6.46 7.21 5.96 7.12 7.24 e 0.063 0.076 0.112 0.090 0.085 0.123

scla* 8.47 7.17 3.75 6.53 4.79 6.22 3.75 4.34 8.89 6.68 6.45 5.74 7.04 5.65 5.33 5.47 7.50 e 0.087 0.099 0.077 0.091 0.123

pat 10.00 8.49 11.17 11.20 11.09 8.97 10.38 12.05 8.45 9.33 9.50 10.25 10.05 9.82 10.94 11.50 9.75 10.97 e 0.133 0.120 0.086 0.134

ogo 13.40 13.48 10.09 10.56 10.50 13.28 11.37 11.21 13.58 14.22 14.13 10.75 13.20 12.96 11.28 9.80 12.47 11.58 15.60 e 0.065 0.141 0.190

tal* 11.05 10.59 7.48 8.13 8.03 10.90 9.01 8.26 10.88 11.48 11.28 8.43 10.78 10.46 8.65 7.48 9.85 9.04 13.75 6.02 e 0.125 0.160

atys 9.53 11.01 12.30 11.20 11.84 11.31 12.40 12.87 11.45 10.57 10.56 11.44 11.20 10.70 11.41 12.28 11.93 12.56 13.08 18.16 15.36 e 0.123

gue 14.70 13.06 14.63 14.03 14.32 13.03 14.88 13.33 16.28 14.34 13.18 14.41 13.50 13.41 12.95 15.22 15.30 14.77 16.79 20.41 17.43 14.66 e

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Table 6

Mahalanobis distances between centroids and Procrustes distances between species means are shown for males of all study species below and above the main diagonal, respectively. Abbreviation for species names

are shown in Table 1

nig aet asc cam cep dia eryg* eryt* ham lhoe mit mon neg nic pet pog pre* scla* pat ogo tal* atys gue

nig e 0.061 0.085 0.062 0.084 0.058 0.089 0.068 0.067 0.051 0.049 0.062 0.050 0.063 0.080 0.078 0.059 0.089 0.076 0.149 0.144 0.074 0.097

aet 7.19 e 0.061 0.044 0.057 0.041 0.063 0.045 0.068 0.049 0.050 0.042 0.048 0.043 0.055 0.056 0.049 0.065 0.077 0.121 0.116 0.075 0.098

asc 8.69 6.81 e 0.043 0.023 0.058 0.036 0.035 0.091 0.072 0.068 0.047 0.072 0.044 0.031 0.028 0.069 0.039 0.116 0.086 0.083 0.096 0.116

cam 7.89 6.46 5.37 e 0.043 0.037 0.052 0.028 0.070 0.050 0.043 0.026 0.045 0.029 0.036 0.038 0.050 0.052 0.091 0.113 0.108 0.079 0.100

cep 8.66 6.51 2.76 5.12 e 0.057 0.033 0.032 0.092 0.072 0.069 0.043 0.070 0.041 0.030 0.029 0.068 0.040 0.116 0.091 0.087 0.091 0.112

dia 7.52 5.51 5.60 3.94 5.30 e 0.062 0.035 0.065 0.042 0.033 0.037 0.040 0.027 0.051 0.056 0.040 0.066 0.075 0.131 0.126 0.077 0.093

eryg* 9.16 7.21 4.81 6.23 4.40 6.07 e 0.041 0.094 0.078 0.073 0.051 0.075 0.050 0.038 0.043 0.072 0.045 0.117 0.093 0.089 0.099 0.119

eryt* 7.91 5.81 4.07 3.55 3.48 3.13 4.56 e 0.074 0.053 0.046 0.030 0.053 0.022 0.032 0.035 0.050 0.047 0.097 0.110 0.103 0.078 0.101

ham 8.41 8.26 9.55 7.41 9.59 7.06 9.68 7.77 e 0.054 0.060 0.080 0.059 0.072 0.090 0.092 0.065 0.102 0.071 0.149 0.142 0.068 0.133

lhoe 7.13 5.93 6.76 6.08 6.98 5.44 8.02 5.53 6.75 e 0.039 0.053 0.044 0.048 0.068 0.069 0.035 0.080 0.070 0.143 0.138 0.072 0.108

mit 6.12 5.38 6.20 5.51 6.46 4.39 6.76 4.71 7.78 5.86 e 0.044 0.036 0.037 0.061 0.065 0.042 0.079 0.069 0.143 0.136 0.070 0.097

mon 7.65 5.81 4.94 3.46 4.34 4.13 4.88 3.14 8.80 6.57 4.91 e 0.047 0.030 0.040 0.037 0.050 0.052 0.091 0.116 0.112 0.083 0.093

neg 6.77 6.33 6.57 4.72 6.32 5.22 7.11 5.59 7.48 6.76 5.15 5.04 e 0.045 0.065 0.067 0.045 0.078 0.068 0.141 0.137 0.075 0.097

nic 7.17 5.56 4.67 3.41 4.06 2.87 5.12 2.40 7.89 5.67 3.90 3.40 4.86 e 0.036 0.043 0.042 0.055 0.089 0.119 0.114 0.076 0.096

pet 8.48 6.68 5.12 3.79 4.80 5.23 5.32 3.98 8.62 7.13 5.93 4.65 5.74 3.87 e 0.032 0.064 0.042 0.111 0.098 0.093 0.092 0.102

pog 8.23 6.74 3.61 4.79 3.86 5.48 5.26 3.99 9.72 7.00 6.24 3.39 6.23 4.76 5.03 e 0.067 0.040 0.113 0.091 0.089 0.094 0.107

pre* 7.21 5.69 6.36 5.54 6.18 4.96 6.62 5.00 7.29 3.70 5.53 5.62 5.89 4.64 6.49 6.56 e 0.076 0.074 0.138 0.135 0.080 0.104

scla* 9.16 7.32 4.41 6.05 4.61 6.27 4.62 4.97 10.21 7.91 7.18 5.29 7.02 5.24 5.63 4.94 7.10 e 0.122 0.094 0.093 0.106 0.112

pat 9.52 7.82 10.78 9.74 11.03 8.36 10.65 9.62 8.56 8.72 8.00 9.40 8.82 9.40 10.19 10.74 9.23 11.32 e 0.178 0.175 0.095 0.126

ogo 13.28 11.83 8.60 10.30 9.43 11.69 9.77 10.58 13.38 12.75 12.81 10.34 11.99 11.30 10.31 8.58 11.94 10.06 15.21 e 0.044 0.155 0.175

tal* 12.04 10.88 8.43 9.16 9.08 10.65 9.71 9.53 11.54 11.66 11.82 9.76 11.12 10.35 9.09 8.44 11.35 10.13 14.11 4.71 e 0.146 0.170

atys 9.38 10.55 12.65 11.37 11.91 10.72 13.01 10.77 11.19 10.72 9.62 11.26 10.99 10.19 11.36 12.17 11.09 13.03 11.88 17.92 16.07 e 0.126

gue 13.05 12.79 14.30 13.20 13.79 12.70 14.86 12.96 15.58 14.84 12.75 13.15 13.07 12.63 12.34 13.73 14.70 14.51 15.94 18.90 17.24 14.15 e

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a common allometric trajectory needs to be investigated usingontogenetic series. The patterns of conserved allometries evi-dent in guenons are strongly reminiscent of those found inneotropical monkeys, although congruence with studies of pa-pionins largely depends on whether static interspecific (Single-ton, 2002) or ontogenetic (Collard and O’Higgins, 2001)allometries are considered. Comparisons of cranial trajectorieswithin papionins (Collard and O’Higgins, 2001; Singleton,2002) and apes (Mitteroecker et al., 2004) demonstrate thepresence of important size-related shape changes within pri-mates but do not support hypotheses of simple extension/trun-cation of a common allometric line in the taxa studied. Inguenons, however, small divergence of shape trajectories (Car-dini and Elton, 2008), correlations between magnitudes of sizeand shape sexual dimorphism, extreme divergence of shape inspecies at extremes of size variation, and phenetic clusters mir-roring size groups suggest that, as in South American monkeys(Marroig and Cheverud, 2005), a large component of shapevariation in guenon skulls has been produced followinga path of least evolutionary resistance (Schluter, 2000) setby a strong covariation among allometric traits. In otherwords, size (probably selected for by dietary and other ecolog-ical factors, such as predation) has helped to determine mor-phological change. This biasing of the direction ofevolutionary shape modification may have resulted in the con-served morphology evident in many guenon taxa. Such biases,however, decay with time, and shape variation is progressivelyless constrained as the structure of trait covariance is modifiedby selective pressures (Renaud et al., 2006). Thus, for in-stance, in partial disparity analysis the large shape divergenceof A. nigroviridis, basal to all guenons (Tosi et al., 2005), hasmore to do with phylogeny than with its size, which is aboutaverage for a guenon. This could indicate that constraints onshape modification have lessened over time in Allenopithecus.On the other hand, the highly distinctive Miopithecus is botha probable basal lineage and the smallest guenon. Its shape di-vergence is likely to be the product of not only a long evolu-tionary history but also of strong selective pressures leading toa reduction in size and consequent allometric shape modifica-tions of the skull.

The contributions of evolutionary distance and ecology

There are no compelling ecological and behavioural rea-sons to expect that guenons would be particularly conservativein their patterns of cranial and mandibular shape variation.Members of the clade exploit a wide variety of ecologicalniches and exhibit considerable behavioural diversity. It isthus surprising that small matrix correlations between shapeand ecology (and also, not shown, between size and ecology)suggest no strong convergences in relation to diet, habitat, andlocomotion in the guenon clade as a whole. This is not to saythat individual species fail to show skull features that havearisen in response to specific ecological and behavioural pres-sures; ecology, for example, is likely have contributed directlyor indirectly (via size) to skull shape in Erythrocebus and Mio-pithecus. Even if correlations between skull form and ecology

are weak, size and ecology are to some extent interrelated andit is difficult to partition their roles completely. They are alsoassociated with genetic distance, in that species that are lessclosely related might be expected to show greater differencesin size, ecology, and behaviour. The possibility of a combinedcontribution of ecology and evolutionary history is discussedbelow with respect to another, albeit moderately divergent,guenon species, C. aethiops.

It is apparent that genetic distance alone accounts for someof the shape differences in guenon skulls. Not only are signifi-cant correlations of shape with genetic distances evident, butdivergence of species mean shapes also increases with evolu-tionary distance. In females, relative distances to the grandmean of all species were 18.2 for the colobine C. guereza,7.4 for the papionin C. atys, 4.0 for the basal A. nigroviridis,and below 3 for most other guenons. A similar observation ofshape divergence being roughly proportional to evolutionarytime can also be made for males. It is possible that the use ofpartial disparity (Zelditch et al., 2004), which measures dis-tances between each mean shape and their grand mean, may in-troduce a bias if a large number of species are ‘clumped’ ina similar body mass range (in this case, small-to-medium), pro-ducing a grand mean closer to the means of species in thatrange. To avoid this, the average of all pairwise distances foreach taxon can be used instead. When compared to partial dis-parity, the contribution of each species to total disparity wasmore ‘evenly’ spread across taxa, ranging from 2.6e2.5% to11.2e10.4% (females-males, respectively). Thus, the emphasison highly divergent species is indeed reduced. However, sincethe metric has a correlation of 1.000 with partial disparity, itsuse does not change the general patterns observed in this study.

Analysis of the whole sample (including all guenon taxaand both outgroups) in the shape space and size-shape spaceindicated a good separation of the outgroup species. Phylog-eny is likely to account for the discrimination of at least oneof the outgroup species, Colobus guereza. An expanded gonialregion of the mandible, short nasal bones, high vaulted cra-nium, and larger interorbital distance are found in C. guerezaand most other colobines (Strasser and Delson, 1987). Thesecharacters are considered ancestral compared to the derivedcondition, associated with lengthening of the face, seen in cer-copithecines (Verheyen, 1962; Strasser and Delson, 1987).Within the cercopithecines, papionins have a more elongatedface than guenons (Szalay and Delson, 1979). This trend of fa-cial elongation is partly related to size and is especially evi-dent in the largest African monkeys, the baboons (Papio)and mandrills (Mandrillus). Cercocebus atys, the papionin out-group in our analysis, is smaller than Papio and Mandrillus,and is more comparable in size to E. patas, but does nothave a particularly long face (which may explain why it isless divergent than might be expected for a papionin). How-ever, a relatively small neurocranium and deep mandible,which are not associated with short nasals as in colobines,seem to be among the characters that discriminate this speciesfrom the others.

Within the guenon clade, C. hamlyni was clearly separatedon the first two PCs of the shape space, as well as to a certain


degree on the second PC of the size-shape space (ssPC2). Thisdistinctiveness was emphasised by its divergent shape as indi-cated by partial disparity and its isolation in the similarityanalysis. Since C. hamlyni, the owl-faced monkey, is an aver-age-sized arboreal guenon, size alone is unlikely to account forthe increased degree of morphological divergence in its skull.C. hamlyni is unusual in that molecular data do not support itsinclusion in either of the two major clades of arboreal guenons(Tosi et al., 2005). It might, therefore, be a representative ofthe early radiation of the arboreal lineage. Such early separa-tion from other arboreal species could help to explain its mor-phological distinctiveness. Modern populations of C. hamlyniare mostly restricted to a relatively small number of mountainforests in eastern Congo, and the species is presently classifiedas near threatened or vulnerable, with one subspecies (C. h. ka-huziensis) listed as endangered (Kingdon, 1997; IEA, 1998;Butynski and Members of the Primate Specialist Group,2000). Whether genetic bottlenecks might have contributed tofixation of autoapomorphic traits cannot be said until more isknown about the genetics and evolutionary history of this spe-cies. Similarly, more information is required on its ecology andbehaviour to assess whether its distinctive skull shape hasarisen through social or ecological pressures.

Another species that appeared distinctive in the size-shapespace (separated on ssPC3 and ssPC4 from the outgroup spe-cies and the other guenons) was Cercopithecus aethiops. How-ever, this species did not appear particularly divergent in anyof the other analyses. C. aethiops is a relatively common spe-cies with a widespread distribution across Africa, so is well-represented in museum collections. Its sample size was largerthan those of the other species, and it was therefore possiblethat it weighted the derivation of the main axes of the size-shape space. As with the discriminant analysis, a randomsubsample of C. aethiops specimens was used in place ofthe entire C. aethiops sample to ascertain whether this wasthe case. The results (not shown) of this analysis showedthat the separation of C. aethiops from other guenons wasless defined than when the larger sample was used, and oc-curred along the fourth ssPC rather than the first. Nonetheless,overall separation remained good, verifying its distinctivenessin the size-shape space.

The C. aethiops face is relatively more elongated and thecranial vault less enlarged than in many other guenons. Suchdivergence in skull shape might be attributable to a relativelylong history of genetic isolation, as indicated by branchlengths in Tosi et al.’s (2005) study. It is also possible thatits morphological divergence from other species is somehowrelated to its distinct ecology. Vervet monkeys are highly eco-logically flexible, with eclectic diets and the ability, uncom-mon in other guenons, to inhabit marginal and disturbedhabitats (Fedigan and Fedigan, 1988). The vervet postcraniumdoes not show the extreme adaptations to terrestriality evidentin the other terrestrial guenons, C. lhoesti and E. patas (Geboand Sargis, 1994). Also unlike the open-habitat adapted patasmonkey, vervets are medium-sized, with only moderate sexualdimorphism (Fedigan and Fedigan, 1988). It is apparent thatthe monophyly of the terrestrial guenons (Tosi et al., 2004,

2005) does not simplistically equate with common ecological,biological, and behavioural responses to terrestriality. Re-search into the morphological variation of vervet skulls indi-cates that spatial and environmental factors, particularlyrainfall, contribute to variation in both size and shape, al-though a significant proportion of variance remains unex-plained (Cardini et al., 2007). It is thus possible that vervetecology has influenced skull shape, but further research intoits ecomorphologydunfortunately beyond the scope of thepresent studydis necessary to explore this hypothesis.

Within the overall pattern of conserved allometric changesin guenon skull shape, it is clear that neither genetic distances(as a proxy for phylogeny) nor ecology provide simple expla-nations for the extreme divergence evident in some species,although their consideration does shed light on some morpho-logical differences, such as those between the basal Allenopi-thecus and the rest of the tribe. Although complexities areintroduced by their interrelationships with each other andwith size, ecology and evolutionary history remain importantcomponents in understanding at least some aspects of morpho-logical differentiation in guenons. The work reported herehighlights instances in which morphological divergence can-not be attributed mostly to size. Crucially, these will help toframe future research projects focusing on if, how, and whyecological or phylogenetic differences contribute to skull mor-phology in specific taxa such as C. aethiops and C. hamlyni.

Species discrimination

The results of the phenetic analyses show that there is ap-preciable shape differentiation in a number of guenon taxa,specifically Allenopithecus and Miopithecus, whose distinctivemorphologies have been noted in previous studies (Verheyen,1962; Martin and MacLarnon, 1988; Shea, 1992), as well as E.patas, C. aethiops, and C. hamlyni. Identifying such extremesof variation, however, does not help to determine whethersmaller but nonetheless informative differences can be foundin the skulls of other guenons, particularly those in the genusCercopithecus. Good discrimination of guenon species basedon skull shape was not an a priori expectation of this study.Other than in size, most species look very similar and diagnos-tic characters are virtually absent. Indeed, previous research(Verheyen, 1962) found only modest differentiation within Cer-copithecus, and in the present study, inspection of first axes ofshape (or size-shape) variation also showed relatively poor sep-aration of most species. Nonetheless, percentages of correctlyclassified specimens according to species were high in themain analyses and the hold-out samples, regardless of whichmethod was used for species discrimination. This indicatesthat small quantitative differences that are large enough to dis-criminate species might well be present. It is highly likely thata large number of morphometric descriptors, such as the 86landmarks measured on the cranium and mandible in this study,are necessary to pick up these slight but significant variations.

All species with the largest errors in species identificationbelong to the arboreal guenon clade. This clade is approxi-mately the same age as the terrestrial clade (4.6 versus 4.8


Ma, according to the molecular clock of Tosi et al., 2005), buthas given rise to many more species, some probably throughrapid differentiation during the forest fragmentation of thePlio-Pleistocene (Hamilton, 1988). Cercopithecus ascanius in-cludes several specimens of either sex which are misclassifiedas C. cephus and some females that are misclassified as C. er-ythrotis. These three species belong to the same terminal cladeof arboreal guenons in Tosi et al.’s (2005) molecular phylog-eny. Thus, both morphological and genetic data suggest veryclose relationships among them. However, misclassificationdid not always fall along phylogenetic lines. Specimens ofC. pogonias and C. mona were misclassified into several spe-cies in a pattern that had no clear relationship with phylogeny.Unexpectedly, C. campbelli and C. mona are not easily con-fused in discriminant analysis, despite strong similarities(see phenograms). This suggests at least a moderate degreeof morphological divergence between parapatric populationsof these closely related species.

Misclassified specimens of C. diana are generally found inC. nictitans, although the two species are not closely related.C. nictitans is the sister species of C. mitis, and although C.mitis is not extensively misclassifed, such specimens are foundin C. nictitans. The molecular phylogeny of Tosi et al. (2005)suggests that C. mitis albogularis is actually more closely re-lated to C. nictitans than to other subspecies of C. mitis. Thismight explain why several specimens of C. mitis are classifiedas C. nictitans (up to five among females and up to threeamong males). However, among eight individuals classifiedas C. mitis albogularis in museum databases, only one is mis-classified as C. nictitans in the discriminant analysis. The lim-ited information on subspecies available in museums and theproblematic taxonomy of the C. mitis-nictitans group (Napier,1981) raise issues that need to be addressed through further re-search on arboreal guenons. This is reinforced by the observa-tion that misclassified specimens of C. nictitans are spreadacross four to six loosely-related species.

Among species in which females and males are misclassifiedmost frequently, less than half of the wrongly-assigned speci-mens seem to be found in the corresponding sister species.This can be ascribed to short time since speciation. Overall, di-versification of guenon skulls is modest, and is especially smallamong arboreal species, but populations identified on the basisof pelage colour and geographic distribution do correspond tomorphologically divergent lineages. In the broader context ofspecies recognition, morphological divergence must not beseen as a necessary property for inferring species boundaries,but as a line of evidence that needs to be compared with resultsfrom studies using other data and methods, that may either sup-port or contradict the hypothesis that a morphologically diver-gent population represents a ‘good species’ (de Queiroz, 2005).

Conclusions

Our analyses suggest that guenon skulls show an allometri-cally conserved pattern of shape differentiation, but it is appar-ent that much remains to be discovered about the more subtlelinks between morphology, phylogeny, ecology, and behaviour

within the clade. One major question that emerges is why gue-non skulls appear more evolutionarily conserved than those oftheir sister taxon, the papionins. An obvious differencebetween the two is the presence or absence of an elongatedmuzzle. It is possible that whereas the largely terrestrial,open-habitat papionins responded to ecological and behaviou-ral pressures through elaborating hard tissue features, leadingto divergent skull morphologies within the clade, the primarilyarboreal guenons benefited more from altering facial coloura-tion, soft tissue traits like whiskers, and vocalisations. Changessuch as these may have been advantageous in relatively low-light forest conditions, where hard tissue features might beless obvious than bright colouration or distinctive calls. None-theless, the majority of guenon specimens included in oursample were correctly classified to species in discriminantanalyses. This suggests that most population boundaries indi-cated by vocalisations and soft tissue characters are alsoreflected in hard tissue morphology, even though a large num-ber of accurate morphometric descriptors may be needed topick up these subtle differences. The significant correlation be-tween genetic distance and shape, although not as strong as thecorrelation between size and shape, indicates that phylogenyinfluences skull shape within the guenons. The evolutionaryhistory of the clade has yet to be elucidated fully, hamperedas it is by the paucity of the guenon fossil record. However,further molecular analyses, particularly phylogeographic stud-ies, could provide important insights into guenon speciationand population genetics, which in turn could be mappedonto observed differences in hard tissue morphology. Thistype of approach might help us to understand whether the dis-tinctive morphology of C. hamlyni, for example, is the productof stochastic events in its evolutionary history, or whether it isdue to ecological and social pressures.

Of all the factors included in our study that would potentiallyinfluence morphological differentiation, ecology was the leastsignificant. Given the inter- and intraspecific ecological varia-tions in the tribe, this was unexpected. It is probable that ecol-ogy does influence skull shape, and hints about this are given bythe divergence of not only E. patas and Miopithecus, that haveobviously distinct ecologies, but also by the modest differenti-ation of the eurytopic and geographically widespread C. ae-thiops. It is possible that the ‘broad brush’ categorisation ofecologies used in this study conceals important yet subtle dis-tinctions between most taxa. Parallels can be drawn here withthe discriminant analysis, in which a large number of detailedmorphological descriptors were required to classify species.Field research has provided a wealth of information about gue-non ecology as well as behaviour, but detailed studies of someof the more cranially distinctive taxa, like Miopithecus and C.hamlyni, are yet to be undertaken, and more data on intraspe-cific variation are also required. Nonetheless, enough informa-tion is currently available on well-studied species such as thevervet to address in more detail the links between small varia-tions in ecology and skull shape. The future integration of de-tailed ecological, behavioural, and morphological data wouldbe highly beneficial to our understanding of the adaptationsand diversification of the guenons.


Acknowledgements

A large number of people have contributed in differentways to this study. We are deeply grateful to all of them,and apologise to those whom we might have forgotten to ac-knowledge. Special thanks are due to P. O’Higgins andM. Bastir, both at the University of York; S. Cobb, Universityof Hull; C.E. Oxnard, University of Western Australia; S. Mar-telli, University College London; E. Delson, City University ofNew York; S.R. Frost, University of Oregon; C.P. Groves,Australian National University; C.J. Jolly and T.R. Disotell,New York University, New York; F.J. Rohlf, State Universityof New York; C.P. Klingenberg, University of Manchester,Manchester; P. Mitteroecker, F. L. Bookstein and K. Schaefer,University of Vienna; R.W. Thorington, Jr., L. Gordon, C.A.Ludwig, J.G. Mead, C. Potter, D.F. Schmidt, A.L. Gardner,C.A. Shaw, and M. Sitnik, all at the National Museum of Nat-ural History, Washington; N. Gilmore, Academy of NaturalSciences, Philadelphia; J. Spence, T. Pacheco, and P.A. Bruna-uer, all at the American Museum of Natural History, NewYork; J.M. Chupasko and M.D. Omura, Museum of Compar-ative Zoology of the Harvard University, Cambridge; M. Schu-lenberg and J. Fooden, Field Museum, Chicago; R. Asher,I. Thomas, and R. Sastrawan, Museum fur Naturkunde, Berlin;O. Roher-Ertl, Staatliche Naturwissenschaftliche SammlugenBayerns, Munich; C. Rovati and S. Maretti, Museo di StoriaNaturale di Pavia, Pavia; C.P.E. Zollikofer, M. Zefferer,M. Bragger, T. Weingrill, M. Gisi, and C. Zebig-Brunner, allthe University of Zurich; W. Van Neer and W. Wendelen,Royal Museum for Central Africa, Tervuren; P. Jenkins, D.Hills and L. Tomsett British Museum of Natural History,London; and J. Harrison and M. Harman, Powell-Cotton Mu-seum, Birchington.

We also very much appreciate the comments of the editorSusan Anton, Becky Ackermann, and several anonymous ref-erees in improving this work, and thank them for their timeand trouble. We are particularly grateful to one reviewer fortheir advice on and suggestions about how to recalculate thepartial disparity analysis so that the ‘clumped’ means didnot overly influence the analysis.

This paper is dedicated to the memory of Walter N. Ver-heyen in recognition of his great contribution to the under-standing of the evolution of form in African monkeys. Weregret that the author of one of the most cited studies on cer-copithecine monkey cranial variation, who was of extraordi-nary help to us with his advice and friendship in occasion ofincidental, but unforgettable, meetings during early stages ofthis work, will not be able to see the outcome of a researchthat he greatly helped to inspire.

This study was funded by a grant from the Leverhulme Trust.

References

Adams, D.C., Slice, D.E., Rohlf, F.J., 2004. Geometric morphometrics: ten

years of progress following the ‘revolution’. Ital. J. Zool. 71, 5e16.

Bookstein, F.L., 1991. Morphometric Tools for Landmark Data. Cambridge

University Press, Cambridge, Massachusetts.

Butynski, T.M., 2002. The guenons: an overview of diversity and taxonomy. In:

Glenn, M.E., Cords, M. (Eds.), The Guenons: Diversity and Adaptation in Af-

rican Monkeys. Kluwer Academic/Plenum Publishers, New York, pp. 3e13.

Butynski, T., Members of the Primate Specialist Group, 2000. Cercopithecus

hamlyni ssp. kahuziensis. In: IUCN 2006 (Ed.), 2006 IUCN Red List of

Threatened Species. Available online at: www.iucnredlist.org. Downloaded

on May 02, 2007.

Cardini, A., Elton, S., 2008. Variation in guenon skulls (II): sexual dimor-

phism. J. Hum. Evol. 54 (5), 638e647.

Cardini, A., Elton, S., Skull functional and developmental modules: mosaic

evolution and phylogenetic signal. Biol. J. Linn. Soc., in press.

Cardini, A., Jansson, A.-U., Elton, S., 2007. Ecomorphology of vervet mon-

keys: a geometric morphometric approach to the study of clinal variation.

J. Biogeogr. 34, 1663e1678.

Chapman, C.A., Chapman, L.J., Cords, M., Mwangi Gathua, J., Gautier-

Hion, A., Lambert, J.E., Rode, K., Tutin, C.E.G., White, L.J.T., 2002. Var-

iation in the diets of Cercopithecus species: differences within forests,

among forests, and across species. In: Glenn, M.E., Cords, M. (Eds.),

The Guenons: Diversity and Adaptation in African Monkeys. Kluwer

Academic/Plenum Publishers, New York, pp. 325e350.

Cheverud, J.M., Richtsmeier, J.T., 1986. Finite element scaling applied to sex-

ual dimorphism in rhesus macaque (Macaca mulatta) facial growth. Syst.

Zool. 35, 381e399.

Collard, M., O’Higgins, P., 2001. Ontogeny and homoplasy in the papionin

monkey face. Evol. Dev. 3, 322e331.

Cords, M., 1987. Forest guenons and patas monkeys: male-male competition

in one-male groups. In: Smuts, B.B., Cheney, D.L., Seyfarth, R.M.,

Wrangham, R.W., Struhsaker, T. (Eds.), Primate Societies. University of

Chicago Press, Chicago, pp. 98e111.

Curtin, S.H., 2002. Diet of the roloway monkey (Cercopithecus diana rolo-way) in Bia National Park, Ghana. In: Glenn, M.E., Cords, M. (Eds.),

The Guenons: Diversity and Adaptation in African Monkeys. Kluwer

Academic/Plenum Publishers, New York, pp. 351e371.

de Queiroz, K., 2005. Different species problems and their resolution. BioEs-

says 27, 1263e1269.

Dryden, I.L., Mardia, K.V., 1998. Statistical Shape Analysis. John Wiley and

Sons, New York.

Elton, S., 2007. Environmental correlates of the cercopithecoid radiations.

Folia Primatol. 78, 344e364.

Fedigan, L., Fedigan, L.M., 1988. Cercopithecus aethiops: a review of field

studies. In: Gautier-Hion, A., Bourliere, F., Gautier, J.-P., Kingdon, J.

(Eds.), A Primate Radiation: Evolutionary Biology of the African

Guenons. Cambridge University Press, Cambridge, pp. 394e411.

Frost, S.R., Marcus, L.F., Bookstein, F.L., Reddy, D.P., Delson, E., 2003. Cra-

nial allometry, phylogeography, and systematics of large-bodied papionins

(primates: cercopithecinae) inferred from geometric morphometric analy-

sis of landmark data. Anat. Rec. 275A, 1048e1072.

Gautier-Hion, A., 1978. Food niches and coexistance in sympatric primates in

Gabon. In: Chivers, D.J., Herbert, J. (Eds.), Recent Advances in Primatol-

ogy, vol. II. Academic Press, New York, pp. 270e286.

Gautier-Hion, A., 1988a. The diet and dietary habits of forest guenons. In:

Gautier-Hion, A., Bourliere, F., Gautier, J.-P., Kingdon, J. (Eds.), A Pri-

mate Radiation: Evolutionary Biology of the African Guenons. Cambridge

University Press, Cambridge, pp. 257e283.

Gautier-Hion, A., 1988b. Polyspecific associations among forest guenons: eco-

logical, behavioural and evolutionary aspects. In: Gautier-Hion, A.,

Bourliere, F., Gautier, J.-P., Kingdon, J. (Eds.), A Primate Radiation: Evo-

lutionary Biology of the African Guenons. Cambridge University Press,

Cambridge, pp. 453e476.

Gebo, D.L., Sargis, E.J., 1994. Terrestrial adaptations in the postcranial skel-

etons of guenons. Am. J. Phys. Anthropol. 93, 341e371.

Grubb, P., Butynski, T.M., Oates, J.F., Bearder, S.K., Disotell, T.R.,

Groves, C.P., Struhsaker, T.T., 2003. Assessment of the diversity of African

primates. Int. J. Primatol. 24, 1301e1357.

Hair, J.H., Anderson, R.E., Tatham, R.L., Black, W.C., 1998. Multivariate Data

Analysis. Prentice Hall, Upper Saddle River, New Jersey.

Hamilton, A.C., 1988. Guenon evolution and forest history. In: Gautier-

Hion, A., Bourliere, F., Gautier, J.P., Kingdon, J. (Eds.), A Primate Radi-

http://www.iucnredlist.org


ation: Evolutionary Biology of the African Guenons. Cambridge Univer-

sity Press, Cambridge, pp. 13e34.

Harmon, L.J., Kolbe, J.J., Cheverud, J.M., Losos, J.B., 2005. Convergence and

the multidimensional niche. Evolution 59, 409e421.

IEA, 1998. African Mammals Databank e a Databank for the Conservation

and Management of the African Mammals, vols. 1e2. Report to the Direc-

torate-General for Development (DGVIII/A/1) of the European Commis-

sion. Project No. B7e6200/94-15/VIII/ENV. Bruxelles.

Isbell, L.A., 1998. Diet for a small primate: insectivory and gummivory in the (large)

patas monkey (Erythrocebus patas pyrrhonotus). Am. J. Primatol. 45, 381e398.

Isbell, L.A., Pruetz, J.D., Lewis, M., Young, T.P., 1998b. Locomotor activity

differences between sympatric patas monkeys (Erythrocebus patas) and

vervet monkeys (Cercopithecus aethiops): implications for the evolution

of long hindlimb length in Homo. Am. J. Phys. Anthropol. 105, 199e207.

Isbell, L.A., Pruetz, J.D., Young, T.P., 1998a. Movements of vervets (Cercopithe-

cus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food

resource size, density and distribution. Behav. Ecol. Sociobiol. 42, 123e133.

Jernvall, J., Wright, P., 1998. Diversity components of impending primate

extinctions. Proc. Natl. Acad. Sci. 95, 11279e11283.

Kendall, D.G., 1984. Shape manifolds, Procrustean metrics and complex pro-

jective spaces. Bull. Lond. Math. Soc. 16, 81e121.

Kingdon, J.S., 1997. The Kingdon Field Guide to African Mammals.

Academic Press, London.

Klingenberg, C.P., 1996. Multivariate allometry. In: Marcus, L.F., Corti, M.,

Loy, A., Naylor, G.J.P., Slice, D.E. (Eds.), Advances in Morphometrics.

Plenum Press, New York, pp. 23e49.

Klingenberg, C.P., 1998. Heterochrony and allometry: the analysis of evolu-

tionary change in ontogeny. Biol. Rev. 73, 79e123.

Klingenberg, C.P., Monteiro, L.R., 2005. Distances and directions in multidi-

mensional shape spaces: implications for morphometric applications. Syst.

Biol. 54, 678e688.

Kozak, K.H., Larson, A., Bonnett, R.M., Hramon, L., 2005. Phylogenetic anal-

ysis of ecomorphological divergence, community structure, and diversifi-

cation rates in dusky salamanders (Plethodontidae: Desmognathus).

Evolution 59, 2000e2016.

Leakey, M., 1988. Fossil evidence for the evolution of the guenons. In: Gaut-

ier-Hion, A., Bourliere, F., Gautier, J.P., Kingdon, J. (Eds.), A Primate

Radiation: Evolutionary Biology of the African Guenons. Cambridge Uni-

versity Press, Cambridge, pp. 7e12.

Legendre, P., Legendre, L., 1998. Numerical Ecology, second ed. Elsevier,

Amsterdam, pp. 552e560.

Leigh, S.R., 2006. Cranial ontogeny of Papio baboons (Papio hamadryas).

Am. J. Phys. Anthropol. 130, 71e84.

Leigh, S.R., Shah, N.F., Buchanan, L.S., 2003. Ontogeny and phylogeny in

papionin primates. J. Hum. Evol. 45, 285e316.

Marcus, L.F., Hingst-Zaher, E., Zaher, H., 2000. Application of landmark morpho-

metrics to skulls representing the orders of living mammals. Hystrix 11, 27e48.

Marroig, G., Cheverud, J.M., 2001. A comparison of phenotypic variation and co-

variation patterns and the role of phylogeny, ecology, and ontogeny during cra-

nial evolution of New World monkeys. Evolution 55 (12), 2576e2600.

Marroig, G., Cheverud, J.M., 2005. Size as a line of least evolutionary resis-

tance: diet and adaptive morphological radiation in New World monkeys.

Evolution 59 (5), 1128e1142.

Martin, R.D., MacLarnon, A.M., 1988. Quantitative comparisons of the

skull and teeth in guenons. In: Gaultier-Hion, A., Bourliere, F.,

Gautier, J.P., Kingdon, J. (Eds.), A Primate Radiation: Evolutionary Bi-

ology of the African Guenons. Cambridge University Press, Cambridge,

pp. 160e183.

Martins, E., 1999. Estimation of ancestral states of continuous characters:

a computer simulation study. Syst. Biol. 48, 642e650.

McNulty, K.P., 2004. A geometric morphometric assessment of hominoid cra-

nia: conservative African apes and their liberal implications. Ann. Anat.

186, 429e433.

McNulty, K.P., Frost, S.R., Strait, D.S., 2006. Examining affinities of the

Taung child by developmental simulation. J. Hum. Evol. 51, 1e23.

Mitteroecker, P., Gunz, P., Bernhard, M., Schaefer, K., Bookstein, F.L., 2004.

Comparison of cranial ontogenetic trajectories among great apes and

humans. J. Hum. Evol. 46, 679e697.

Mitteroecker, P., Gunz, P., Bookstein, F.L., 2005. Heterochrony and geometric

morphometrics: a comparison of cranial growth in Pan paniscus versus

Pan troglodytes. Evol. Dev. 7, 244e258.

Nakagawa, N., 1999. Differential habitat utilization by patas monkeys (Eryth-

rocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus)

living sympatrically in northern Cameroon. Am. J. Primatol. 49,

243e264.

Nakagawa, N., Hideyuki Ohsawa, H., Muroyama, Y., 2003. Life-history pa-

rameters of a wild group of West African patas monkeys (Erythrocebus

patas patas). Primates 44, 281e290.

Napier, P.H., 1981. Catalog of Primates in the British Museum (Natural His-

tory) and Elsewhere in the British Isles, Part II: Family Cercopithecinae,

Subfamily Cercopithecinae. British Museum (Natural History), London.

Nunn, C.L., 2002. A comparative study of leukocyte counts and disease risk in

primates. Evolution 56, 177e190.

Nunn, C.L., Altizer, S.M., Sechrest, W., Jones, K.E., Barton, R.A.,

Gittleman, J.L., 2004. Parasite species richness and the evolutionary diver-

sity of primates. Am. Nat. 162, 597e614.

O’Higgins, P., Collard, M., 2001. Sexual dimorphism and facial growth in

papionin monkeys. J. Zool., Lond. 257, 255e272.

O’Higgins, P., Jones, N., 1999. Morphologika. Tools for Shape Analysis.

University College London, London.

Polly, P.D., 2005. Development and phenotyopic correlations: the evolution of

tooth shape in Sorex araneus. Evol. Dev. 7, 29e41.

Renaud, S., Auffray, J.-C., Michaux, J., 2006. Conserved phenotypic variation

patterns, evolution along lines of least resistance, and departure due to

selection in fossil rodents. Evolution 60, 1701e1717.

Rohlf, F.J., 1998. On applications of geometric morphometrics to study of

ontogeny and phylogeny. Syst. Biol. 47, 147e158.

Rohlf, F.J., 2003. TpsSmall. Department of Ecology and Evolution, State Uni-

versity of New York, Stony Brook, New York. Available online at: http://

life.bio.sunysb.edu/morph/

Rohlf, F.J., 2005. NTSYSpc, Version 2.20f. Exeter Software, Setauket, New York.

Rohlf, F.J., Marcus, L.F., 1993. A revolution in morphometrics. Trends Ecol.

Evol. 8, 129e132.

Rohlf, F.J., Slice, D.E., 1990. Extensions of the Procrustes method for the

optimal superimposition of landmarks. Syst. Zool. 39, 40e59.

Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University

Press, New York.

Shea, B.T., 1992. Ontogenetic scaling of skeletal proportions in the talapoin

monkey. J. Hum. Evol. 23, 283e307.

Singleton, A.M., 2002. Patterns of cranial shape variation in the Papionini

(Primates: Cercopithecinae). J. Hum. Evol. 42, 547e578.

Slice, D.E., 1999. Morpheus (beta version). Department of Ecology and

Evolution, State University of New York, Stony Brook, New York.

SPSS for Windows, 2002. SPSS Inc., Version 11.5.0. SPSS Inc., Chicago, Il-

linois, USA.

Strasser, E., Delson, E., 1987. Cladistic analysis of cercopithecid relationships.

J. Hum. Evol. 16, 81e99.

Szalay, F.S., Delson, E., 1979. Evolutionary History of the Primates. Academic

Press, New York.

Tosi, A.J., Detwiler, K.M., Disotell, T.R., 2005. X-chromosomal window into

the evolutionary history of the guenons (Primates: Cercopithecini). Mol.

Phylogenet. Evol. 36, 58e66.

Tosi, A.J., Melnick, D.J., Disotell, T.R., 2004. Sex chromosome phylogenetics

indicate a single transition to terrestriality in the guenons (tribe Cercopi-

thecini). J. Hum. Evol. 46, 223e237.

Verheyen, W.N., 1962. Contribution a la craniologie comparee des primates.

Les genres Colobus Illiger 1811 et Cercopithecus Linne 1758. Musee

Royal de l’Afrique Centrale, Tervuren, Annales 8 (105), 1e255.

Wood, B.A., Richmond, B., 2000. Human evolution: taxonomy and paleobiol-

ogy. J. Anat. 97, 19e60.

Xing, J., Wang, H., Zhang, Y., Ray, D.A., Tosi, A.J., Disotell, T.R.,

Batzer, M.A., 2007. A mobile element based evolutionary history of

guenons (tribe Cercopithecini). BMC Biol. 5, 5.

Zelditch, M.L., Swiderski, D.L., Sheets, H.D., Fink, W.L., 2004. Geometric

Morphometrics for Biologists: a Primer. Elsevier Academic Press, San

Diego.

http://life.bio.sunysb.edu/morph/

http://life.bio.sunysb.edu/morph/

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