AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 158:227–241 (2015)

Phylogenetic Relationships Within the Cercocebus–Mandrillus Clade as Indicated by Craniodental Morphology: Implications for Evolutionary Biogeography Lieven Devreese1* and Christopher C. Gilbert2,3,4 1

Cognitive Ethology Laboratory, German Primate Center, Leibniz Institute for Primate Research, Goettingen D-37077, Germany 2 Department of Anthropology, Hunter College of the City University of New York, New York, NY 10065 3 PhD Program in Anthropology, Graduate Center of the City University of New York, New York, NY 10016 4 New York Consortium in Evolutionary Primatology, New York, NY KEY WORDS phylogeography

Cercocebus–Mandrillus; African papionins; phylogeny; morphometrics;

ABSTRACT Objective: The African papionin primates commonly known as mangabeys form a diphyletic group with white-eyelid mangabeys (Cercocebus) being most closely related to drills and mandrills (Mandrillus). However, the phylogenetic relationships among members of the Cercocebus–Mandrillus clade have not been investigated in detail, particularly from a morphological perspective. Early studies of white-eyelid mangabeys considered C. agilis to best represent the ancestral lineage and C. torquatus as the most derived species, the result of multiple biogeographic dispersal events. More recently, a sister-clade relationship between Mandrillus and either C. chrysogaster or C. torquatus has been proposed. Materials and Methods: Here we present the results of phylogenetic analyses based on 206 craniodental characters (103 representing males and females separately) of four species of Cercocebus and both species of Mandrillus. Morphological and molecular data strongly support a diphyletic origin of the African group of monkeys commonly referred to as mangabeys (Cronin and Sarich, 1976; Groves, 1978; Disotell et al., 1992; Disotell, 1994, 2000; Harris and Disotell, 1998; Fleagle and McGraw, 1999, 2002; Harris, 2000; Page and Goodman, 2001; Gilbert, 2007; Gilbert and Rossie, 2007; Gilbert et al., 2009). Currently, two genera of mangabeys are recognized. The semi-terrestrial white-eyelid mangabeys are placed in the genus Cercocebus, closely related to mandrills and drills (Mandrillus), whereas the arboreal crested mangabeys constitute the genus Lophocebus and form an as yet unresolved clade with Theropithecus (geladas), Papio (baboons), and the recently described genus Rungwecebus (kipunjis) (Disotell et al., 1992; Disotell, 1994, 2000; Harris and Disotell, 1998; Fleagle and McGraw, 1999, 2002; Harris, 2000; Groves, 2001; Tosi et al., 2003; Jones et al., 2005; Davenport et al., 2006; Gilbert, 2007; Gilbert and Rossie, 2007; Olson et al., 2008; Burrell et al., 2009; Gilbert et al., 2009, 2011; Zinner et al., 2009; Roberts et al., 2010). Up to seven species of Cercocebus are currently recognized (Zinner et al., 2013), which are distributed across the African rainforest belt from West Africa to the Rift Ó 2015 WILEY PERIODICALS, INC.

Results: When all species of the Cercocebus–Mandrillus clade are analyzed without molecular constraints, results suggest that C. torquatus may indeed be more closely related to mandrills and drills than to other Cercocebus taxa. However, this topology lacks strong statistical support and may be attributable to incomplete lineage sorting and/or reticulation. When we employ a molecular backbone to constrain Cercocebus and Mandrillus monophyly, C. torquatus appears most basal, while C. agilis and C. chrysogaster form a derived clade. Discussion: The molecular backbone view is also congruent with recent genetic analyses and assessments based on the fossil record, but awaits confirmation with additional data. This phylogeny suggests that Cercocebus and Cercocebus 1 Mandrillus arose in western equatorial Africa with subsequent dispersals westward, eastward, and possibly southward over the last > 3 million years. Am J Phys Anthropol 158:227–241, 2015. VC 2015 Wiley Periodicals, Inc.

Valley, as well as south of the Congo River and in two isolated forest blocks in East Africa (Fig. 1). The two species of Mandrillus occur only in the coastal forests of Central Africa from Nigeria to the Congo River, and on the island of Bioko. The geographic ranges of Cercocebus and Mandrillus species are mostly delimited by natural barriers such as rivers and unsuitable non-forested habitat, except for C. agilis and C. torquatus which are Additional Supporting Information may be found in the online version of this article. Grant sponsors: The Leakey Foundation, The American Association of Physical Anthropologists, Hunter College, CUNY. *Correspondence to: Lieven Devreese, Kragendijk 45A, 8300 Knokke-Heist, Belgium. E-mail: [email protected] Received 1 February 2015; revised 12 May 2015; accepted 17 May 2015 DOI: 10.1002/ajpa.22780 Published online 29 June 2015 in Wiley Online Library (wileyonlinelibrary.com).

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L. DEVREESE AND C.C. GILBERT

Fig. 1. Dispersal scenario of white-eyelid mangabeys (Cercocebus) as proposed by Grubb (1978, 1982). Map modified from McGraw and Fleagle (2006), courtesy of Luci Betti-Nash.

parapatric without a clear barrier between them, and for Mandrillus which is sympatric with both C. agilis and C. torquatus, respectively. While the precise number of species recognized varies slightly depending on the species concept being used, the general taxonomy of the Cercocebus–Mandrillus clade is relatively stable and well accepted (Grubb et al., 2003). To date, the phylogenetic relationships among the members of the Cercocebus–Mandrillus clade have not been investigated in detail, particularly from a morphological perspective. Based on gross morphological comparisons and a general assessment of character polarity in mangabey evolution, Grubb (1978, 1982) proposed a hypothetical dispersal scenario for the genus Cercocebus. In his scenario, C. agilis is assumed to best represent the ancestral species. Some individuals of this ancestral population became isolated by the Congo River and gave rise to C. chrysogaster. Similarly, C. galeritus originated after isolation in East Africa. Finally, this scenario hypothesizes that a series of dispersal events started with a westerly migration from the ancestral population (Fig. 1). The resulting western population later dispersed back in an easterly direction, giving rise to American Journal of Physical Anthropology

C. atys and C. lunulatus and eventually, in the coastal forests of Central Africa, to C. torquatus which is currently parapatric with C. agilis (Fig. 1). In a preliminary study of craniodental morphology, McGraw and Fleagle (2006) found three remarkable similarities in cranial features shared by C. torquatus and the genus Mandrillus. Both taxa possess only minor maxillary excavation, pronounced paranasal ridging oriented medially toward the incisors, and a distinctive pattern of cranial temporal lines. McGraw and Fleagle (2006) proposed these similarities to be shared derived characters and suggested a possible sister relationship between C. torquatus and Mandrillus. Other authors have posited C. chrysogaster, the genus’ only representative south of the Congo River, to be the most basal and drill-like of the white-eyelid mangabeys (Dobroruka and Badalec, 1966; Kingdon, 1997) in having a naked, violet rump, bright-colored fur and relatively robust build (including the muzzle of adult males). Unlike all other white-eyelid mangabeys, C. chrysogaster habitually carries its tail in a backward arch. Recently, studies based on nuclear DNA sequence data from a small sample of species found Cercocebus to be

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CERCOCEBUS CRANIODENTAL PHYLOGENY monophyletic, with C. torquatus representing the most basal lineage, while C. agilis and C. chrysogaster were more derived (Perelman et al., 2011; Guevara and Steiper, 2014). However, various mitochondrial DNA sequence data have suggested paraphyletic relationships within Cercocebus (Davenport et al., 2006; Zinner et al., 2009, 2011; Guevara and Steiper, 2014). In these studies, C. torquatus clustered with Mandrillus forming a sister group to other Cercocebus taxa, suggesting contemporary and/or ancient introgressive hybridization among these sympatric species. In the most recent study, Liedigk et al. (2014) found a single mitochondrial genome of C. chrysogaster to be closely related to Mandrillus leucophaeus. Thus, while uncertainty exists regarding the relationships within the genus Cercocebus, none of the previous biogeographic hypotheses proposed in the literature are well-supported by recent molecular analyses. Although the phylogeny of African papionins has been studied at the genus level, the relationships within the Cercocebus–Mandrillus clade at the level of individual species are not well-established and a comprehensive analysis has yet to be conducted. In this study, we examine the phylogenetic relationships among four species of Cercocebus (C. agilis, C. atys, C. chrysogaster, and C. torquatus) and both species of Mandrillus (M. leucophaeus and M. sphinx) based on craniodental data. Specifically, we employ “morphology only” as well as “molecular backbone” analyses and compare our results to previous morphological and molecular analyses. Based on our results, we discuss the biogeography of the Cercocebus–Mandrillus clade, including available morphological, molecular, and fossil data, and develop a number of alternative dispersal scenarios for the genus Cercocebus.

MATERIALS AND METHODS We collected data on 103 characters (37 quantitative, 66 qualitative, coded for males and females separately, 206 characters combined), distributed throughout the skull, with 34 from the vault and base, 25 from the face, 16 from the palate and upper dentition, and 27 from the mandible and lower dentition (Table 1). Body size was coded and included as a qualitative character (Table 1). Data were collected on wild-shot, adult museum specimens from the following collections: American Museum of Natural History, New York (AMNH); Field Museum of Natural History, Chicago (FMNH); National Museum of Natural History, Washington, DC (NMNH); Museum of Comparative Zoology, Cambridge (MCZ); Natural History Museum, London (BMNH); Powell-Cotton Museum, Birchington (PCM); Royal Museum for Central Africa, Tervuren (RMCA); the Randall L. Susman personal collection, Stony Brook (RLS); Iziko South African Museum, Cape Town (SAM); the Frederick Grine personal collection (FEG); and the Transvaal Museum, Pretoria (TM). In a small number of cases, non-pathological captive specimens were also included to increase sample sizes (four female M. sylvanus, one male M. sylvanus, one male P. hamadryas, three female T. gelada, three male T. gelada). Quantitative measurements were made by both authors using digital calipers and recorded to the nearest one-tenth of a millimeter. Qualitative characters were scored according to the character state criteria listed in Table 1. We supplemented measurements and character state assignments with data from Gilbert (2013).

Samples In the initial “morphology only” analysis, focused on the larger question of Cercocebus–Mandrilus phylogeny and Cercocebus monophyly, we assigned four Cercocebus species (C. agilis, C. atys, C. chrysogaster, and C. torquatus) and both Mandrillus species (M. leucophaeus and M. sphinx) to the ingroup and allowed them to group freely. Unfortunately, we were not able to include C. galeritus, C. sanjei, and C. lunulatus due to an insufficient number of verifiable specimens found in the museum collections we examined. In the second analysis, focusing on Cercocebus species-level phylogeny, we enforced a genus-level “molecular backbone” (based on nuclear DNA studies) and assumed Cercocebus monophyly and Mandrillus monophyly within the ingroup. We verified the origin of each specimen based on its provenance as to ensure the exclusion of questionable C. galeritus (formerly included in C. agilis) and C. lunulatus (formerly included in C. atys) specimens in the data set. Sample sizes of most taxa and characters correspond to the minimum of five to ten individuals suggested by Gilbert and Grine (2010), but are low for quantitative data of female M. sphinx (n 5 2 specimens) and for qualitative data of C. atys (n 5 2 males and 2 females). Sample sizes, split up per taxon and per character, can be found in the Supporting Information Tables 1 and 2. Lophocebus and Papio represent two of the closest relatives of the Cercocebus–Mandrillus clade. However, it may be argued that these taxa are derived in their own ways and cannot be considered good models for the primitive condition of Cercocebus and Mandrillus. Since multiple outgroups improve phylogenetic results (e.g., Maddison et al., 1993; Strait and Grine, 2004), we additionally assigned Macaca as an outgroup. Macaca was chosen because it is universally recognized as the sister taxon to the other extant papionins (Cronin and Sarich, 1976; Szalay and Delson, 1979; Strasser and Delson, 1987; Disotell et al., 1992; Disotell, 1994, 2000; Harris and Disotell, 1998; Fleagle, 1999; Tosi et al., 1999, 2003; Harris, 2000; Xing et al., 2005; but see Liedigk et al., 2014). Rungwecebus was excluded as an outgroup due to the lack of any adult specimens (see Davenport et al., 2006; Gilbert et al., 2011). Theropithecus was excluded as an outgroup due to its many derived and autapomorphic features that make it a poor representative of the hypothetical African papionin ancestor, as previously noted by multiple researchers (e.g., Jolly, 1966, 1972; Szalay and Delson, 1979; Strasser and Delson, 1987; Fleagle and McGraw, 1999, 2002; Gilbert, 2007). As in Gilbert et al. (2009) and Gilbert (2013), outgroups contained multiple species, but were lumped into their respective genera in an attempt to include a range of possible morphologies. For Macaca, this included M. fascicularis, M. mulatta, M. nemestrina, and M. sylvanus as these taxa are often considered to be relatively generalized and/or “primitive” macaques by molecular and morphological studies (Fooden, 1975, 1976; Szalay and Delson, 1979; Delson, 1980; Morales and Melnick, 1998; Groves, 2001). For Papio and Lophocebus, specimens from all major taxonomic groups within each genus were included (Supporting Information Table 1 and 2).

Quantitative characters We applied an isometric size correction to the quantitative characters as described in Gilbert et al. (2009). American Journal of Physical Anthropology

230

L. DEVREESE AND C.C. GILBERT TABLE 1. Characters used in this study

Character

Definition

a

Glabella-inion Bregma-basion Biporionic breadth Glabella-bregma Parietal-sagittal chord (bregma-lambda) Lambda-inion Occipital-sagittal length (lambda-opisthion) Foramen magnum maximum width Occipital condyle maximum length Breadth between carotid canals Length of tympanic plate (distance from the most lateral point on the inferior surface of the tympanic plate to the carotid canal) Adult male sagittal crest position States: 0 5 absent, 1 5 intermediate, 2 5 present only posteriorly, 3 5 intermediate, 4 5 extends anteriorly. The distinction between states 2 and 4 is determined by whether the anteriormost point of the crest is well anterior to bregma or begins approximately at or posterior to bregma. Crest is defined here as the meeting or contact of the temporal lines. Postorbital sulcus States: 0 5 absent, 1 5 intermediate, 2 5 post-glabellar depression present, 3 5 intermediate, 4 5 post-orbital sulcus present, 5 5 polymorphic Auditory meatus position Small Taxa States: 0 5 medial (inferior margin of the meatus is medial to porion and thus overhung by a supermeatal roof), 1 5 intermediate, 2 5 Extended laterally relative to the medial state, but still medial to the lateral border of the neurocranium Large Taxa States: 0 5 Extended laterally relative to the medial state, but still medial to the lateral border of the neurocranium, 1 5 intermediate, 2 5 lateral (inferior margin of the meatus is lateral to porion) Anterior temporal line divergence States: 0 5 not widely divergent (pinched or slightly divergent), 1 5 intermediate, 2 5 widely divergent

C1 C2 C4 a C5 a C7 C9 a C10 a C11 a C12 a C14 a C16 a a

C17

C18 a

C19

C20

C21 a

C22 C23 a C25

C26 a

C27

C28 C29 C31

C32 C40 a

C41

a

C42

C43

Nuchal lines in the midline where discernable States: 0 5 not upturned (downturned or straight), 1 5 intermediate, 2 5 upturned Calvarial shape (biporionic length/glabella-inion) Cranial vault index (basion-bregma/glabella-inion) Compound temporonuchal crest Small Taxa States: 0 5 absent, 1 5 intermediate, 2 5 partial crest confined to the lateral third of biasterionic breadth Large Taxa States: 0 5 partial crest confined to the lateral third of bi-asterionic breadth, 1 5 intermediate, 2 5 extensive crest extending almost the entire distance between inion and the lateral margin of the supramastoid crest Definitive parietal notch States: 0 5 parietal/asterionic notch present, 1 5 intermediate, 2 5 parietal/asterionic notch absent Position of the tympanic relative to the postglenoid process Small Taxa States: 0 5 tympanic fused with postglenoid, 1 5 intermediate, 2 5 tympanic unfused and separated from the postglenoid process Large Taxa States: 0 5 tympanic unfused and separated from the postglenoid process, 1 5 intermediate, 2 5 tympanic unfused and widely separated from the tympanic Postglenoid process height States: 0 5 very tall, 1 5 intermediate, 2 5 normal, 3 =intermediate, 4 5 shortened EAM tympanic crest States: 0 5 absent, 1 5 intermediate, 2 5 present Position of the foramen magnum relative to the biporionic line States: 0 5 basion is well posterior to the line, 1 5 intermediate, 2 5 basion approximates the line, 3 5 intermediate, 4 5 basion is well anterior to the line EAM size States: 0 5 small, 1 5 intermediate, 2 5 large Petrous apex ossified beyond spheno-occipital synchondrosis States: 0 5 absent, 1 5 intermediate, 2 5 present Shape of the choanal sides Small Taxa States: 0 5 divergent anteriorly, 1 5 intermediate Large Taxa States: 0 5 intermediate, 1 5 parallel Shape at the posterior end of the medial pterygoid plates Small Taxa States: 0 5 moderately divergent, 1 5 intermediate, 2 5 strongly divergent Large Taxa States: 0 5 intermediate, 1 5 moderately divergent, 2 5 intermediate Shape at the posterior edge of vomer States: 0 5 not incised, 1 5 intermediate, 2 5 incised

American Journal of Physical Anthropology

Character type

Reference

QN, QN, QN, QN, QN, QN, QN, QN, QN, QN, QN,

Wood, 1991 Wood, 1991 Wood, 1991 Wood, 1991 Wood, 1991 Wood, 1991 Wood, 1991 Wood, 1991 Wood, 1991 Chamberlain, 1987 Chamberlain, 1987

O O O O O O O O O O O

QL, O

Eck and Jablonski, 1984, 1987

QL, U

Szalay and Delson, 1979

QL, O

Groves, 1978, 2000

QL, O

QL, O

Groves, 2000; McGraw and Fleagle, 2006; Gilbert, 2007 Gilbert, 2007

QN, O QN, O QL, O

General General Strait et al., 1997

QL, O

Groves, 2000

QL, O

Groves, 2000

QL, O

Groves, 2000

QL, O QL, O

Groves, 2000 Dean and Wood, 1981, 1982; Strait et al., 1997

QL, O

QL, O

Strait and Grine, 2004 Collard and Wood, 2000 Groves, 2000

QL, O

Groves, 2000

QL, O

Groves, 2000

QL, O

231

CERCOCEBUS CRANIODENTAL PHYLOGENY TABLE 1. Continued

Character

Definition

C44

Vomer-presphenoid junction States: 0 5 vomer uninflated, 1 5 intermediate, 2 5 vomer inflated Vomer/Sphenoid/Palatine contact States: 0 5 meet at one point, 1 5 intermediate, 2 5 separated by another bone, 3 5 intermediate, 4 5 palatine doesn’t reach vomer Vomer/sphenoid contact in the midline Small Taxa States: 0 5 intermediate, 1 5 another bone between Large Taxa States: 0 5 clean contact, 1 5 intermediate Petrous process position States: 0 5 medially positioned, 1 5 intermediate, 2 5 laterally positioned Appearance of fossae anterior to the foramen magnum States: 0 5 absent or poorly defined, 1 5 intermediate, 2 5 present and clearly visible, 3 5 intermediate, 4 5 deeply excavated and sharply defined Superior facial height (nasion-prosthion) Superior facial breadth (frontomalaretemporale-frontomalaretemporale) Bizygomatic breadth (zygion-zygion) Bimaxillary breadth (zygomaxillare-zygomaxillare) Maximum nasal aperture width (maximum width at whatever height it occurs) Zygomaxillare-porion Upper facial prognathism (porion-glabella) Lower facial prognathism (porion-prosthion) Lacrimal bone position States: 0 5 extends outside the orbit, 1 5 intermediate, 2 5 within orbit Medial orbital wall composition States: 0 5 vomer contribution (frontal covers ethmoid), 1 5 ethmoid contribution Presence/Absence of maxillary fossae States: 0 5 absent, 1 5 intermediate, 2 5 present Development of maxillary fossae Given present in F19, Small Taxa States: 0 5 extend up to the infraorbital plate, 1 5 intermediate, 2 5 invades infraorbital plate, 3 5 intermediate, 4 5 deeply invades the infraorbital plate Given present in F19, Large Taxa States: 0 5 superior to alveolus only, 1 5 intermediate, 2 5 extend up to the infraorbital plate, 3 5 intermediate, 4 5 invades infraorbital plate Maxillary ridge in males States: 0 5 absent, 1 5 intermediate, 2 5 present Male maxillary ridge orientation States: 0 5 medial towards incisors, 1 5 intermediate, 2 5 lateral towards canines Muzzle dorsum outline States: 0 5 rounded, 1 5 intermediate, 2 5 peaked, 3 5 intermediate, 4 5 flat, 5 5 polymorphic between states 0 and 4, 6 5 polymorphic between states 0, 2, and 4 Contact of maxillary frontal processes States: 0 5 frontal processes of maxillae do not meet in the midline, 1 5 intermediate, 2 5 frontal processes of maxillae meet in the midline Frontal/premaxilla contact States: 0 5 absent, 1 5 intermediate, 2 5 present Positioning of the zygomatic foramina States: 0 5 no foramina observable, 1 5 intermediate, 2 5 at or below plane of orbital rim, 3 5 intermediate, 4 5 foramina above and below the plane of the orbital rim, 5 5 intermediate, 6 5 above plane of orbital rim, 7 5 polymorphic Projection of nasal bones States: 0 5 nasal bones do not project above the frontal/maxillary suture, 1 5 intermediate, 2 5 nasal bones project above the frontal/maxillary suture Glabella prominence States: 0 5 glabella not prominent, 1 5 intermediate, 2 5 glabella prominent General facial profile in lateral view States: 0 5 straight, 1 5 intermediate, 2 5 concave Nasal bone orientation in lateral view States: 0 5 straight (after anteorbital drop, if present), 1 5 intermediate, 2 5 slightly upturned, 3 5 intermediate, 4 5 upturned Nasal bone extension over nasal aperture States: 0 5 no extension, 1 5 intermediate, 2 5 slight extension, 3 5 intermediate, 4 5 significant extension Anteorbital drop States: 0 5 absent, 1 5 intermediate, 2 5 present Piriform profile States: 0 5 no anteorbital drop, distinct point at rhinion, 1 5 intermediate, 2 5 anteorbital drop, distinct point at rhinion, 3 5 intermediate, 4 5 anteorbital drop, no distinct point at rhinion Maxillo-alveolar length (Prosthion to a point where the line joining the posterior borders of the maxillary tuberosities crosses the median plane)

C45 a

C46

C47 C48 a

F1 F3 F4 a F5 F9 a

F14 F15 F16 F17

a a

F18 F19 a

F20

F21 F22 F23 F24 F25 F27

F28 F29 F30 F31 F32 F33 F34 a

P1

Character type

Reference

QL, O

Groves, 2000

QL, U

General

QL, O

General

QL, O

Gilbert, 2007

QL, O

General

QN, QN, QN, QN, QN,

Wood, Wood, Wood, Wood, Wood,

O O O O O

QN, O QN, O QN, O QL, O QL, O QL, O QL, O

QL, O QL, O

1991 1991 1991 1991 1991

Wood, 1991 Chamberlain, 1987 Chamberlain, 1987 Szalay and Delson, 1979 Trevor-Jones, 1972 Szalay and Delson, 1979 Gilbert, 2007

QL, U

General McGraw and Fleagle, 2006 General

QL, O

General

QL, O

General

QL, U

General

QL, O

General

QL, O

General

QL, O

General

QL, O

Gilbert, 2007

QL, O

Gilbert, 2007

QL, O QL, O

General General

QN, O

Wood, 1991

American Journal of Physical Anthropology

232

L. DEVREESE AND C.C. GILBERT TABLE 1. Continued

Character type

Reference

Maxillo-alveolar breadth (ectomolare-ectomolare) Incisive canal-palatomaxillary suture (distance between the posterior edge of the incisive canal and the palatomaxillary suture) Upper incisor alveolar length (distance between prosthion and the midpoint of the interalveolar septum between I2 and C) Upper premolar alveolare length (minimum distance between the midpoints of the interalveolar septa between C/P3 and P4/M1) Upper molar length (minimum distance between the midpoint of the P4/ M1 interalveolar septum and the most posterior of the walls of the M3 alveoli) Canine interalveolar distance (minimum distance between the upper canine alveoli) M3 interalveolar distance (minimum distance between the inner aspect of the alveolar process at the midpoint of M3) Upper premolar ratio (P4 crown area/M1 crown area)

QN, O QN, O

Wood, 1991 Wood, 1991

QN, O

Wood, 1991

QN, O

Wood, 1991

QN, O

Wood, 1991

QN, O

Wood, 1991

QN, O

Wood, 1991

QN, O

P18

Mesial compressed sulcus on upper male canine States: 0 5 present on the crown only, 1 5 present and extends onto root

QL, O

P20

Bilophodont molars States: 0 5 incomplete bilophodonty, 1 5 intermediate, 2 5 complete bilophodonty P3 protocone relative to paracone States: 0 5 protocone strongly reduced or absent, 1 5 protocone present Upper I1 shape States: 0 5 rhomboidal, 1 5 spatulate (defined as lingually cupped with flare, not flare by itself)

QL, O

Fleagle and McGraw, 1999, 2002 Szalay and Delson, 1979; Strasser and Delson, 1987 General

P24

Upper I2 shape States: 0 5 caniniform, 1 5 apically and mesially inclined

QL, O

P25

Female C1 shape States 5 0 5 “masculine”, 1 5 intermediate, 2 5 conical, 3 5 intermediate, 4 5 incisiform

QL, O

P26 a M1

QL, O QN, O QN, O QN, O

Wood, 1991 Wood, 1991

QN, O QN, O

Wood, 1991 Wood, 1991

QN, O

Wood, 1991

M15

Size of I1 relative to I2 States: 0 5 I1  I2, 1 5 intermediate, 2 5 I1 > I2 Symphyseal height (minimum distance between the base of the symphysis and infradentale) Corpus height at M1 Corpus width at M1 (maximum width at right angles to corpus height at M1, taken at the midpoint of M1) Corpus height at M3 Lower premolar alveolar length (minimum distance between the midpoints of the interalvolar septa between C/P3 and P4/M1) Lower molar alveolar length (minimum distance between the midpoints of the interalvolar septa between P4/M1 and the most posterior of the walls of the M3 alveolus) Lower premolar ratio (P4 crown area/M1 crown area)

Szalay and Delson, 1979 Szalay and Delson, 1979; Strasser and Delson, 1987 Szalay and Delson, 1979; Strasser and Delson, 1987 Szalay and Delson, 1979; Napier 1981, 1985 General Wood, 1991

QN, O

M16

P3 distal cingulum States: 0 5 absent, 1 5 present

QL, O

M17

Buccal face of P4 crown States: 0 =straight as seen in occlusal view, 1 5 intermediate, 2 5 inflated as seen in occlusal view P4 mesiobuccal flange, an extension of the enamel cap down onto the root States: 0 5 absent, 1 5 present Lower molar hypoconulid States: 0 5 Hypoconulid present in all lower molariform teeth, 1 5 intermediate, 2 5 Hypoconulid absent in all lower molariform teeth except M3, 3 5 intermediate, 4 5 Hypoconulid absent in all lower molariform teeth M3 tuberculum sextum States: 0 5 absent, 1 5 intermediate, 2 5 present Enamel folding States: 0 5 non-elevated, 1 5 intermediate, 2 5 elevated Lophid orientation relative to the mandibular corpus States: 0 5 transverse, 1 5 intermediate, 2 5 oblique Accessory cuspules in lower molar notches States: 0 5 absent, 1 5 intermediate, 2 5 present Lower incisor lingual enamel States: 0 5 absent, 1 5 present Shape of lower I2 distal surface States: 0 5 straight, 1 5 intermediate, 2 5 bulge, 3 5 intermediate, 4 5 distinct prong

QL, O

Fleagle and McGraw, 1999, 2002 Szalay and Delson, 1979 Szalay and Delson, 1979 Szalay and Delson, 1979 Szalay and Delson, 1979

Character

Definition

a

P2 P3 P4

a

P6

P7 P8 a

P15

P17

P21 P23

a

M3 M4

M5 M7

a

M8

M19 M20

M21 M22 M23 M24 M25 M26

American Journal of Physical Anthropology

QL, O QL, O

QL, O QL, O

QL, O QL, O QL, O

General Szalay and Delson, 1979 Szalay and Delson, 1979

QL, O

Szalay and Delson, 1979

QL, O QL, O

Szalay and Delson, 1979 Szalay and Delson, 1979

233

CERCOCEBUS CRANIODENTAL PHYLOGENY TABLE 1. Continued

Character type

Character

Definition

M27

M41

Mandibular ramus angle States: 0 5 inclined, 1 5 intermediate, 2 5 vertical Gonial region expansion on mandibular ramus States: 0 5 absent, 1 5 intermediate, 2 5 present Inferior portion mandibular symphysis length as scored to a specific tooth in occlusal view States: 0 5 P3, 1 5 intermediate, 2 5 P3-P4, 3 5 intermediate, 4 5 P4, 5 5 intermediate, 6 5 P4-M1, 7 5 intermediate, 8 5 M1, 9 5 polymorphic Median mental foramen States: 0 5 absent, 1 5 present Mental ridges on the symphysis in males States: 0 5 absent, 1 5 intermediate, 2 5 present Development of mandibular corpus fossae States: 0 5 absent, 1 5 intermediate, 2 5 present Width of the extramolar sulcus States: 0 5 narrow, 1 5 intermediate, 2 5 moderate, 3 5 intermediate, 4 5 wide, 5 5 polymorphic Lingual mental foramina positioning States: 0 5 present- single, 1 5 intermediate, 2 5 present- horizontally positioned, 3 5 intermediate, 4 5 present- vertically positioned, 5 5 intermediate, 6 5 present- variably positioned, 7 5 polymorphic P3 lingual "bulge", i.e., P3 crown obliquity States: 0 5 lingual bulge absent (not oblique), 1 5 intermediate, 2 5 lingual bulge is present (oblique) Curve of Spee shape States: 0 5 normal, 1 5 intermediate, 2 5 reversed

BS1

Body size (Cranial size) 0 5 small, 1 5 large

M28 M29

M30 M31 M32 M33 M34

M38

QL, O

Reference

QL, O

Jolly, 1972; Szalay and Delson, 1979 General

QL, U

General

QL, O QL, O

Szalay and Delson, 1979 Szalay and Delson, 1979

QL, O

Gilbert, 2007

QL, U

General

QL, U

Gilbert, 2007

QL, O

General

QL, O

Eck and Jablonski, 1984; Delson and Dean, 1993 Smith and Jungers, 1997; Delson et al., 2000; Fleagle, 1999

QL, O

Following Collard and Wood (2000; 2001), characters are classified by cranial region as follows: C 5 Cranial vault and base; F 5 Face; P 5 Palate and Upper Dentition, M 5 Mandible and lower dentiton. QN 5 Quantitative character, QL 5 Qualitative character, O 5 Ordered, U 5 Unordered. a Character determined to be influenced by allometry. For consistency, character numbering follows Gilbert et al., 2009; Gilbert, 2013.

Allometry has been demonstrated to have a strong influence on papionin craniodental morphology (Gilbert and Rossie, 2007; Gilbert et al., 2009). To control for the effects of allometry, we used the general allometric coding method developed by Gilbert et al. (2009). In this method, a regression is calculated between the geometric mean of all measurements of a specimen and the sizeadjusted character value. Coding of allometrically influenced characters is based on the positive or negative residual value relative to the calculated regression line. For non-allometrically influenced characters we used gap-weighted coding (Thiele, 1993), dividing the variation into three ordered character states.

Qualitative characters For qualitative characters we used the following coding method of Gilbert et al. (2009). Characters were generally considered ordered, except as described below (see also Table 1 and Gilbert et al., 2009). Polymorphic characters were assigned intermediate states when two states had frequencies greater than 20%. For characters with more than two discrete states, we assigned an intermediate (polymorphic) state if the combined frequency 80%. If no two adjacent character states had a combined frequency 80%, we added an additional polymorphic state and the character was considered unordered. In the case of multistate characters, where more than two adjacent states both totaled 80%, we used the average of the two possible intermediate states. Qualitative characters were determined to be influenced by allometry if consistent differences existed between the

morphologies of small and large taxa (Gilbert, 2007). In order to restore perceived homology of allometrically influenced characters, we assigned character states separately in small and large taxa as in the work by Gilbert et al. (2009).

Parsimony analysis To control for the effect of the large degree of sexual dimorphism in papionins, we coded male and female specimens separately and concatenated them together into a “combined-sex” 206 character matrix, as described by Gilbert et al. (2009). Where data were unavailable, or inapplicable for certain sex-specific characters, we used the missing data code (“?”). We performed two separate phylogenetic analyses. In the first analysis we constrained only Macaca and Lophocebus-Papio as successive outgroups to test the monophyly of Cercocebus in relation to Mandrillus. In the second analysis, in addition to constraining the outgroup, Cercocebus and Mandrillus were constrained as monophyletic genera within the ingroup in order to further investigate phylogenetic relationships within the genus Cercocebus (i.e., a nuclear DNA genus-level “molecular backbone”). In this analysis, within Cercocebus and Mandrillus, taxa were allowed to group freely. We subjected the character matrices to parsimony analyses using exhaustive searches in PAUP 4.0b10 (Swofford, 2001). We employed three measures to assess the stability of reconstructed clades. First, we calculated decay indices for the most parsimonious trees. Second, we performed a 10,000 replication branch and bound American Journal of Physical Anthropology

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Fig. 2. Most parsimonious trees resulting from exhaustive analyses with 10,000 replication branch and bound bootstrap procedure with replacement for clade support. Numbers above branches indicate bootstrap support values and italic numbers in parentheses below branches indicate decay indices (i.e., Bremer support values). (a) Single most parsimonious tree resulting from an analysis considering all Cercocebus and Mandrillus taxa simultaneously. Tree Length 5 487, CI 5 0.5092, HI 5 0.4908, RI 5 0.3808, RC 5 0.1939. (b) Single most parsimonious tree resulting from an analysis constraining all Cercocebus taxa as monophyletic (i.e., molecular backbone for Cercocebus monophyly). Tree Length 5 488, CI 5 0.5082, HI 5 0.4918, RI 5 0.3782, RC 5 0.1922.

bootstrap procedure with replacement, and finally, we constructed consensus trees of all trees within 1% of the length of the most parsimonious trees (Strait et al., 1997; Strait and Grine, 2004). We identified craniodental characters that unite clades by mapping character transformations in Mesquite 2.74 (Maddison and Maddison, 2014). The character matrix used in both analyses is provided in the Supporting Information Table 3.

RESULTS Thirty (23 quantitative and 7 qualitative) out of 103 characters for both sexes were determined to be affected by allometry (Table 1), a finding similar to previous analyses of African papionins (Gilbert and Rossie, 2007; Gilbert et al., 2009). A single most parsimonious tree was recovered in the first “morphology only” phylogenetic analysis (Fig. 2a). In the recovered cladogram Cercocebus is paraphyletic, with C. torquatus reconstructed as more closely related to Mandrillus than it is to other species of Cercocebus. However, the decay index, bootstrap support value, and the consensus trees within 1% of the length of the shortest tree (Figs. 3a,c) all indicate relatively low support for the evolutionary reality of this node, suggesting alternate topologies are also possible. The second phylogenetic analysis constrained Cercocebus and Mandrillus to be monophyletic, as suggested by recent phylogenetic analyses based on nuclear DNA (e.g., Perelman et al., 2011; Guevara and Steiper, 2014). Again, a single most parsimonious tree was obtained, in which C. torquatus is regarded as the most basal lineage within Cercocebus, while C. agilis and C. chrysogaster are considered more derived. This tree is well-supported by relatively high bootstrap values and decay indices, and is only one step longer than the tree obtained in the first analysis (Fig. 2b). In this analysis, the consensus trees of all trees within 1% of the most parsimonious American Journal of Physical Anthropology

tree also support C. torquatus as the most basal Cercocebus lineage (Figs. 3b,d). We identified a list of synapomorphies uniting the various Cercocebus–Mandrillus clades as found by the character transformation analyses (Table 2). As noted previously by McGraw and Fleagle (2006), C. torquatus and Mandrillus are united by a number of characters, the most obvious of which include shallow maxillary fossae in males and females, a relatively low neurocranium in males, a relatively tall mandibular corpus in males, widely divergent temporal lines in females, a relatively long tympanic process in females, and a relatively wide neurocranium in females. A monophyletic Cercocebus is supported by distinctive features such as a mesiodistally short lower molar row in males and females, increased upper prognathism in males, less developed to absent mandibular corpus fossae in males, and better developed maxillary fossae that often invade the infraorbital plate in females.

DISCUSSION White-eyelid mangabeys (genus Cercocebus) represent a group of African primates whose evolutionary history is largely unexplored. Unlike other groups of African primates, no thorough investigations of their morphology or vocalizations have been conducted to infer hypotheses concerning their phylogeny and phylogeography, and molecular studies have only started to reveal some of the relationships among members of the extant Cercocebus–Mandrillus clade. The first analysis, which tested the monophyly of Cercocebus with an unconstrained Cercocebus 1 Mandrillus ingroup, reconstructed C. torquatus as more closely related to Mandrillus than to the other mangabeys, but with relatively low statistical support. This sister-clade relationship has been proposed by McGraw and Fleagle (2006) based on a preliminary number of qualitative

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Fig. 3. Consensus trees within 1% of the most parsimonious trees found in each analysis. (a) Strict consensus of all eight trees within 1% of the most parsimonious tree considering all Cercocebus and Mandrillus taxa simultaneously. (b) Strict consensus of both two trees within 1% of the most parsimonious tree enforcing a molecular backbone for Cercocebus monophyly. (c) Majorityrule consensus of all eight trees within 1% of the most parsimonious tree considering all Cercocebus and Mandrillus taxa simultaneously. (d) Majority-rule consensus of two trees within 1% of the most parsimonious tree enforcing a molecular backbone for Cercocebus monophyly. Numbers above branches in (c) and (d) indicate percentage of trees within 1% of the most parsimonious tree supporting a given clade.

characters, most of which are confirmed in the character transformation analysis conducted here. Paraphyletic relationships within Cercocebus have also been found in studies based on mitochondrial DNA (Davenport et al., 2006; Zinner et al., 2009; Guevara and Steiper, 2014; Liedigk et al., 2014). The grouping of C. torquatus with Mandrillus is often interpreted as an indication of contemporary and/or ancient introgressive hybridization among these sympatric species (Zinner et al., 2011; Guevara and Steiper, 2014). Therefore, the finding of

paraphyletic relationships within Cercocebus in this study may be analogous to the results based on certain subsets of molecular data in two ways: first, it may be a reflection of introgressive hybridization events between C. torquatus and Mandrillus, past or present; and second, it may be partially due to the reduced number of characters, both craniodental and postcranial, representing only a subset of the total phenotype relative to previous morphological studies (Fleagle and McGraw, 1999, 2002; Gilbert et al., 2009; Gilbert, 2013). In any case, as American Journal of Physical Anthropology

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L. DEVREESE AND C.C. GILBERT TABLE 2. Potential synapomorphies suggested by character transformation analyses Analysis 1: Cercocebus and Mandrillus Clade 1 Cercocebus/Mandrillus

Clade 3 M. leucophaeus/M. sphinx

Clade 4 C. atys/C. chrysogaster/C. agilis

Clade 5 C. chrysogaster/C. agilis

C7 Short Parietal-Sagittal Chord (Bregma-Lambda) in Males, C21 Upturned Nuchal Crest/Lines Across the Midline in Males, C42 Moderately Divergent to Straight Posterior Ends of the Medial Pterygoid Plates in Males, F22 Medially Oriented Maxillary Ridges in Males, F31 Straight to Slightly Upturned Nasals in Males, P6 Long Upper Premolar Row in Malesa, P7 Short Upper Molar Row in Males, P17 Large Upper Premolars in Males and Females, C1 Short Neurocranium (Glabella-Inion) in Femalesa, C9 Long Lambda-Inion Chord in Femalesa, C10 Long Occipital-Sagittal Length (Lambda-Opisthion) in Femalesa, F16 Low Degree of Lower Facial Prognathism in Femalesa, F20 Shallower Maxillary Fossae in Females, M7 Long Lower Premolar Row in Femalesa, M15 Large Lower Premolars in Females C4 Narrow Biporionic Breadth in Malesa, C5 Short Distance from Glabella to Bregma in Males and Femalesa, C18 Postorbital Sulcus Present in Males and Females, C20 Widely Divergent Temporal Lines in Males, F4 Narrow Bizygomatic Breadth in Males and Femalesa, F5 Narrow Bimaxillary Breadth in Males and Femalesa, F15 Reduced Upper Prognathism in Males, F17 Lacrimal Bone Occasionally Outside of Orbit in Males, F20 Maxillary Fossae Superior to the Alveolus Only in Males and Females, F24 Frontal Processes of Maxilla Do Not Meetin in the Midline in Males and Femalesa, F29 Prominent Glabella in Males and Females, F33 Anteorbital Drop Present in Males and Females, F34 Piriform Profile with Anteorbital Drop and Distinct Point at Rhinion in Males and Females, M1 Tall Mandibular Symphysis in Males and Femalesa, M27 Posteriorly Inclined Mandibular Ramus in Males, M32 Mandibular Corpus Fossae Present in Males, GM1 Large Size in Males and Females, C28 Normal Postglenoid Process Height in Femalesa, F31 Relatively Straight Nasals in Femalesa, P7 Long Upper Molar Row in Females C2 High Neurocranium (Basion-Bregma) in Males, C17 Sagittal Crest Absent in Males, C26 Parietal Notch Present in Malesa, F20 Greater Development of Maxillary Fossae in Males and Females, P3 Long Distance Between Incisive Canal and Palatomaxillary Suture in Males and Femalesa, P15 Broad M3 Interalveolar Distance in Males, M5 Short Mandibular Corpus Height at the Level of m3 in Males, C4 Narrow Biporionic Breadth in Femalesa, C16 Short Tympanic in Females, C22 Relatively Narrow Calvarium, F14 Short ZygomaxillarePorion Chord in Females, P1 Short Maxillo-Alveolar Length in Femalesa C1 Short Neurocranium in Malesa, C10 Long Occipital-Sagittal Length (LambdaOpisthion) in Malesa, C12 Long Occipital Condyles in Malesa, C20 Pinched or Slightly Divergent Temporal Lines in Males, C21 Polymorphic Nuchal Lines in Males, C29 EAM Crest Absent in Males and Females, C31 Basion Anterior or Approximates the Biporionic Line in Malesa, C41 Choanae Oriented Parallel in Malesa, F21 Maxillary Ridges Polymorphic in Males, F24 Frontal Processes of Maxilla Do Not Meetin in the Midline in Malesa, P7 Short Upper Molar Row in Males and Femalesa, P8 Wide Canine Interalveolar Distance in Males and Femalesa, M8 Short Lower Molar Row in Males and Femalesa, M34 Horizontal Lingual Mental Foramina in Malesa, C14 Narrow Bi-Carotid Breadth in Femalesa, P15 Wide M3 Interalveolar Distance in Females Analysis 2: Cercocebus constrained

Clade 1 Cercocebus

Clade 2 M. leucophaeus/M. sphinx

C26 Parietal Notch Present in Males, F15 Increased Upper Prognathism in Males, M8 Short Lower Molar Row in Males and Femalesa, M26 straight i2 distal surface in Malesa, M27 Polymorphic Mandibular Ramus in Males, M32 Polymorphic to Absent Mandibular Corpus Fossae in Males, C7 Short Parietal-Sagittal Chord (Bregma-Lambda) in Femalesa, F1 Short Superior Facial Height (nasionprosthion) in Femalesa, F16 Reduced Lower Facial Prognathism in Femalesa, F20 Maxillary Fossae Polymorphic to Invade the Infraorbital Plate in Females C4 Narrow Biporionic Breadth in Malesa, C5 Short Distance from Glabella to Bregma in Males and Femalesa, C18 Postorbital Sulcus Present in Males and Females, C20 Widely Divergent Temporal Lines in Males, F4 Narrow Bizygomatic Breadth in Males and Femalesa, F5 Narrow Bimaxillary Breadth in Males and Femalesa, F17 Lacrimal Bone Occasionally Outside of Orbit in Males, F20 Maxillary Fossae Superior to the Alveolus Only in Males and Females, F24 Frontal Processes of Maxilla Do Not Meetin in the Midline in Males and Femalesa, F29 Prominent Glabella in Males and Females, F33 Anteorbital Drop Present in Males and Females, F34 Piriform Profile with Anteorbital Drop and Distinct Point at Rhinion in Males and Females, M1 Tall Mandibular Symphysis in Males and Femalesa, M32 Mandibular Corpus Fossae Present in Males, GM1 Large Size in Males and Females, C2 Short Neurocranium (Basion-Bregma) in Femalesa,

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TABLE 2. Continued

Analysis 2: Cercocebus constrained

Clade 3 C. atys/C. chrysogaster/C. agilis

Clade 4 C. chrysogaster/C. agilis

C14 Narrow Bi-Carotid Breadth in Femalesa, C28 Normal Postglenoid Process Height in Femalesa, F31 Relatively Straight Nasals in Femalesa, P7 Long Upper Molar Row in Females C2 High Neurocranium (Basion-Bregma) in Males, C17 Sagittal Crest Absent in Males, F20 Greater Development of Maxillary Fossae in Males and Females, P3 Long Distance Between Incisive Canal and Palatomaxillary Suture in Males and Femalesa, P15 Broad M3 Interalveolar Distance in Males, M3 Short Mandibular Corpus Height at the Level of m1 in Males, M5 Short Mandibular Corpus Height at the Level of m3 in Males, C4 Narrow Biporionic Breadth in Femalesa, C16 Short Tympanic in Females, C20 Pinched or Slightly Divergent Temporal Lines in Females, C22 Relatively Narrow Calvarium, F14 Short Zygomaxillare-Porion Chord in Females, P1 Short MaxilloAlveolar Length in Femalesa C1 Short Neurocranium in Malesa, C12 Long Occipital Condyles in Malesa, C20 Pinched or Slightly Divergent Temporal Lines in Males, C21 Polymorphic Nuchal Lines in Males, C29 EAM Crest Absent in Males and Females, C31 Basion Anterior or Approximates the Biporionic Line in Malesa, C41 Choanae Oriented Parallel in Malesa, F21 Maxillary Ridges Polymorphic in Males, F24 Frontal Processes of Maxilla Do Not Meetin in the Midline in Malesa, P7 Short Upper Molar Row in Males and Femalesa, P8 Wide Canine Interalveolar Distance in Males and Femalesa, M8 Short Lower Molar Row in Males and Femalesa, M34 Horizontal Lingual Mental Foramina in Malesa, C14 Narrow BiCarotid Breadth in Femalesa, P15 Wide M3 Interalveolar Distance in Females

Character states in bold are recognized as synapomorphies in both males and females. Indicates character states that also appear in parallel in other Cercocebus/Mandrillus taxa. See Table 1 for additional details regarding character and character state definitions/values.

a

judged by the results of the morphology-only analysis presented here, it is possible that C. torquatus is sister to Mandrillus and that Cercocebus is paraphyletic. The hypothesis that C. chrysogaster is more closely related to Mandrillus than it is to other mangabeys (Dobroruka and Badalec, 1966; Kingdon, 1997), however, is not supported by the vast majority of morphological and molecular data available at this time. When we employed a molecular backbone and assumed Cercocebus to be monophyletic, C. torquatus represented the initial branching event in our cladogram, while C. agilis and C. chrysogaster are the result of more recent splits, with relatively high statistical support (see Figs. 2 and 3). These relationships within Cercocebus are in agreement with recent molecular findings based on certain mitochondrial and nuclear DNA sequences (Guevara and Steiper, 2014; Perelman et al., 2011), and we hypothesize this to be the true species tree. However, this phylogenetic pattern is not congruent with the dispersal scenario hypothesis proposed by Grubb (1978, 1982) (and neither is the phylogeny in our first analysis). Grubb considered C. agilis as basal and C. atys and C. torquatus as a successive cline of more derived lineages. Our analysis, as well as recent molecular analyses, suggest a contrasting view of polarity to this scenario and compel alternative hypotheses regarding the evolution and biogeography of the genus Cercocebus. Contrary to previous analyses, it may now be hypothesized that Cercocebus originated in western equatorial Africa (the coastal forests today inhabited by C. torquatus). One possibility is that some individuals of this ancestral population migrated in a western direction, giving rise to the precursor of C. atys. Subsequently, an easterly migration from West Africa originated a central African population, from which C. agilis and C. chrysogaster arose after they became separated along both sides of the Congo River (Fig. 4a). An alternative scenario involves two separate easterly migrations starting

in West Africa, from which first C. torquatus and subsequently a central population (C. agilis and C. chrysogaster) originated (Fig. 4b). Yet another hypothesis posits a scenario in which the ancestral C. torquatus population is basal and genetically substructured, and from which a westerly dispersal event from an ancestral C. torquatus subpopulation gave rise to C. atys. Then, a second easterly dispersal event occurred from the same or closely related ancestral C. torquatus subpopulation, eventually giving rise to C. agilis and C. chrysogaster (Fig. 4c). Finally, the dispersing ancestral C. torquatus subpopulation(s) was/were genetically swamped by other surrounding ancestral C. torquatus populations, resulting in the extant C. torquatus population being basal to the atys and agilis/chrysogaster lineages, which actually share a more recent common ancestor with each other (the now extinct ancestral C. torquatus subpopulation). In any case, similar west-to-east dispersal scenarios have been put forth for other African primates sympatric with white-eyelid mangabeys, including chimpanzees (Caswell et al., 2008) and some guenon clades (Tosi, 2008; Kamilar et al., 2009, Guschanski et al., 2013). To date, it is unknown how the two species isolated in East Africa (C. galeritus and C. sanjei) would fit in this scenario, but it seems most likely they originated from a Central African population and became relicts fairly recently. Alternatively, it could be hypothesized that both species reached their current geographic distribution during two separate dispersal events, as is suggested for Piliocolobus (Ting, 2008). To determine which of our dispersal scenarios is most likely, future phylogenetic studies (both molecular and morphological) including all seven Cercocebus taxa will be crucial. While some Cercocebus species are underrepresented in terms of both molecular and morphological samples, they remain important in any attempt to more fully understand the phylogeny and biogeography of Cercocebus. For example, to test the alternate biogeographic American Journal of Physical Anthropology

Fig. 4. Alternative dispersal scenarios of white-eyelid mangabeys (Cercocebus) incorporating results based on the craniodental data of this study, as well as molecular data from other studies and assessments based on the fossil record. Map modified from McGraw and Fleagle (2006), courtesy of Luci Betti-Nash. See text for details.

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CERCOCEBUS CRANIODENTAL PHYLOGENY scenarios in Figure 4, it will be necessary to place C. lunulatus, in particular, in a firmer phylogenetic context. If C. lunulatus is the sister to C. atys (C. torquatus (C. lunulatus, C. atys)), as is often assumed (Groves, 1978; Grubb et al., 2003), then Figure 4c may be the more likely scenario. However, if C. lunulatus represents the second most basal Cercocebus taxon, creating a step-like branching pattern (C. torquatus (C.lunulatus (C. atys))), the dispersal pattern depicted in Figure 4a may be most likely. Given all of the hypothesized hybridization and incomplete lineage sorting within the Cercocebus–Mandrillus clade (Zinner et al., 2011; Guevara and Steiper, 2014), the true Cercocebus dispersal scenario is likely to be more complex than that suggested by a strict reading of any individual cladogram. Based on our phylogenetic analysis, the ancestor of all members of the Cercocebus–Mandrillus clade is hypothesized to be a relatively long-snouted individual, while the extant short-snouted species (e.g., C. agilis) should be considered to possess the derived condition. Fossil remains that can be confidently attributed to the Cercocebus lineage are rare. However, fossils found at Taung in South Africa, long thought to be representatives of the genus Parapapio, have recently been recognized as belonging to a new genus, Procercocebus, the probable sister genus of Cercocebus (Gilbert, 2007, 2013). Procercocebus dates back to 2.0–3.0 million years ago depending on the estimate (e.g., Delson, 1984, 1988; McKee, 1993; Herries et al., 2013; Hopley et al., 2013), and bears a striking resemblance to C. torquatus in its cranial morphology (Gilbert, 2007). This fossil indicates that the ancestral Cercocebus lineage was once distributed much more to the south, possibly linked with the extension of forested environments, and its close resemblance to C. torquatus supports the idea that C. torquatus should be considered as a primitive lineage within Cercocebus or Cercocebus–Mandrillus. Interestingly, one recent molecular analysis suggests that C. torquatus branched off from the rest of the Cercocebus group 3.3 Ma (range from 2.3 to 4.6 Ma; Perelman et al., 2011), in line with the appearance of Procercocebus in the fossil record and further corroborating a retained primitive morphology for C. torquatus over the past three million years. The question remains whether Procercocebus represents an early southern migration from an ancestral western equatorial population, or whether the genus possibly originated in the south, migrated north, and subsequently diversified into the Cercocebus species we observe today (Fig. 4). Since Mandrillus is also found in western equatorial Africa, it might be suggested that a western equatorial origin scenario is most likely not only for Cercocebus, but for the Cercocebus–Mandrillus clade as a whole. Soromandrillus, a fossil genus closely related to Mandrillus, specifically, or the sister taxon to the broader Cercocebus/Procercocebus 1 Mandrillus grouping, is found in the Usno and Omo Shungura Formations of Ethiopia as well as 2.0–3.0 Ma karst deposits in Angola (Gilbert, 2013). Similar to the situation with Procercocebus, the implied distribution of Soromandrillus from Ethiopia to Angola suggests a larger range for the ancestor of mandrills and drills in the past, both to the South and to the East. A direct reading of the fossil record may implicate East Africa as the geographic area of origin for the Mandrillus lineage since the earliest specimens of Soromandrillus are found there at 3.4 Ma (Delson and Dean, 1993; Gilbert, 2013). However, because the exact place-

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ment of Soromandrillus within the lineage is unresolved, the most parsimonious interpretation of the Cercocebus–Mandrillus group’s biogeographic origins is currently equivocal with either western equatorial Africa or East Africa being the most likely options (Gilbert, 2008, 2013). If Soromandrillus is regarded as the most primitive member of the broader Cercocebus/Procercocebus 1 Mandrillus clade, then its presence in East Africa may suggest an origin there. If, however, Soromandrillus is the sister to extant Mandrillus, then western equatorial Africa is the most likely area of geographic origin. Since the Cercocebus–Mandrillus clade is estimated to have split from Theropithecus/Lophocebus/ Rungwecebus/Papio by 6–10 Ma, and Mandrillus is estimated to have split from Cercocebus by 3.6–4.9 Ma (Disotell and Raaum, 2002; Tosi et al., 2003; Perelman et al., 2011), it is perhaps more likely on chronological grounds that Soromandrillus is indeed the sister taxon to Mandrillus. However, these molecular divergence dates also suggest that more primitive members of the Cercocebus–Mandrillus clade should be present in the fossil record prior to the appearance of Soromandrillus, and these earlier taxa will be critical in elucidating the ultimate geographic origins of the broader clade. Future phylogenetic analyses including additional molecular and morphological data (both craniodental and postcranial) as well as all species of Cercocebus, Mandrillus, and their fossil relatives will be needed to choose between any competing alternatives. In any case, the crown Cercocebus/Procercocebus 1 Mandrillus group is reconstructed here and elsewhere as originating in western equatorial Africa (Gilbert, 2008) and it seems likely that the clade has had a presence in this area since at least 3.0 Ma (see above). It has been previously suggested that the extant Cercocebus–Mandrillus vs. Theropithecus/Lophocebus/ Rungwecebus/Papio clades may have been geographically separated near their origin, with the former more closely associated with western equatorial Africa and the latter in East Africa (Gilbert, 2007, 2008). Our analysis reinforces the view that the crown Cercocebus–Mandrillus clade, at least, probably originated in western equatorial Africa.

ACKNOWLEDGMENTS Authors thank the following institutions and individuals for all of their help and assistance in securing access to the specimens examined during the course of this study: AMNH (Eileen Westwig, Eric Delson), NMNH (Linda Gordon, Darrin Lunde, Nicole Edmison), FMNH (Bill Stanley, Michi Schulenberg, Rebecca Banasiak), MCZ (Judith Chupasko, Mark Omura), BMNH (Paula Jenkins, Daphne Hills), PCM (Malcolm Harman), RMCA (Wim Wendelen, Emmanuel Gilissen), SAM (Graham Avery, Kerwin von Willingh), and TM (Francis Thackeray, Steph Potze, Theresa Kearney, Tersia Perregil). In addition, authors thank Randy Susman and Frederick Grine, respectively, for access to extant primate specimens in their care. Luci Betti-Nash kindly provided the base maps which make up Figures 1 and 4 and Andrea Baden assisted with the modification of Figure 4. LD thanks Arnaud Berkein for his warm and generous hospitality in Brussels. CCG thanks Sam Turvey for his wonderful hospitality while conducting research in the UK, the McKenzie and Band families for all their kindness and generosity while in South Africa, and Brian Gilbert, Arnaud and Rebecca Karsenti, Brian and American Journal of Physical Anthropology

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Nicole Jones, Brent Johnson, Audra Hollifield, Michael Rosenthal, and Jia Liu for hospitality provided in various U.S. cities. Finally, authors thank Mike Steiper, Dietmar Zinner, Eske De Crop, and two anonymous reviewers for helpful thoughts and comments that greatly improved the manuscript. CCG was supported at various times by the L.S.B. Leakey Foundation, a Graduate Council Fellowship from Stony Brook University, a Gaylord Donnelley Postdoctoral Fellowship from the Yale Institute for Biospheric Studies, Hunter College, and a professional development grant from the American Association of Physical Anthropologists.

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