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Home , Aegyptopithecus, Afropithecus, Catarrhini, Cercopithecinae, Colobinae, Micropithecus

Proc. Natl. Acad. Sci. USA Vol. 88, pp. 5267-5271, June 1991

Ancestral facial morphology of Old World higher (Anthropoidea///cranium/anatomy) BRENDA R. BENEFIT* AND MONTE L. MCCROSSINt *Department of , Southern Illinois University, Carbondale, IL 62901; and tDepartment of Anthropology, University of California, Berkeley, CA 94720 Communicated by F. Clark Howell, March 11, 1991

ABSTRACT remains of the cercopithecoid Victoia- (1, 5, 6). Contrasting craniofacial configurations of cercopithe- pithecus recently recovered from middle Miocene deposits of cines and great are, in consequence, held to be indepen- () provide evidence ofthe cranial anatomy dently derived with regard to the ancestral catarrhine condition of Old World monkeys prior to the evolutionary divergence of (1, 5, 6). This reconstruction has formed the basis of influential the extant subfamilies and . Victoria- cladistic assessments ofthe phylogenetic relationships between pithecus shares a suite ofcraniofacial features with the extant and extinct catarrhines (1, 2). catarrhine and early Miocene hominoid Afro- Reconstructions of the ancestral catarrhine morphotype pithecus. AU three genera manifest supraorbital costae, anteri- are based on commonalities of subordinate morphotypes for orly convergent temporal lines, the absence of a postglabellar Cercopithecoidea and Hominoidea (1, 5, 6). Broadly distrib- , a moderate to long snout, great facial height below the uted character states are interpreted as primitive and estab- orbits, a deep cheek region, and anteriorly tapering premaxilla. lish the polarity of morphoclines, with derived character The shared presence of these features in a catarrhine generally states having more restricted taxonomic distributions. Based ancestral to apes and Old World monkeys, an early , and an exclusively on living taxa, however, determination of mor- early Old World indicates that they are primitive phocline polarities for cercopithecoid craniofacial attributes characteristics that typified the last common ancestor of Hom- is essentially arbitrary. Extant Old World monkeys are inoidea and Cercopithecoidea. These results contradict prevail- phylogenetically dichotomous, the Colobinae and Cercopith- ing cranial morphotype reconstructions for ancestral catar- ecinae being mutual sister groups characterized by contrast- rhines as Colobus- orHylobates-like, characterized by a globular ing facial configurations. Cercopithecine facial structure is anterior braincase and orthognathy. By resolving several equiv- distinguished from that ofthe relatively short-faced colobines ocal craniofacial morphocline polarities, these discoveries lay the by: a cranial vault of low height, narrow interorbital septum, foundation for a revised interpretation of the ancestral cranial long and narrow nasal bones, moderately long prognathic morphology of Catarrhini more consistent with neontological snout, deep zygoma, moderately tall infraorbital facial and existing paleontological evidence. height, and long anteriorly tapering premaxilla with relatively broad procumbent central set anterior to lateral ones (7). Intrinsic evidence alone cannot reveal whether Colobinae The prevailing cranial morphotype reconstruction of the or Cercopithecinae is more likely to have retained the prim- common ancestor of Old World higher primates has had itive cercopithecoid condition. Craniofacial morphocline po- profound influences on interpretations of the phylogenetic larities within Hominoidea are generally equivocal due to relationships ofearly catarrhines (1, 2). Recent discoveries in their heterogeneity, the long-faced great apes contrasting northern and eastern provide documentation of the with Hylobatidae in a manner similar to the cercopithecine/ craniofacial anatomy of Oligocene catarrhines generally an- colobine comparison.t Therefore, selection ofColobinae and cestral to apes and Old World monkeys and ofearly Miocene Hylobatidae as representative of primitive facial configura- apes (3, 4). Until this time, however, there has been an tions ofthe Cercopithecoidea and Hominoidea, respectively, absence of knowledge concerning the craniofacial configura- rests primarily upon the principle that similarities between tion of Old World monkeys from the earliest portion of their nonsister group taxa are likely to be conservative (1, 5, 6). evolutionary history. Recently discovered facial remains of The alternative explanation, that the orthognathy of Colobi- the earliest are described. Together with nae and Hylobatidae is homoplastic, has been dismissed due recently acquired knowledge of the anatomy of Oligocene to the perceived "remarkable similarity in cranial form catarrhines and early Miocene hominoids, these en- among short-faced anthropoids" (2). able testing ofpreviously formulated craniofacial reconstruc- Cercopithecoid craniofacial morphocline polarities may be tions of the last common ancestor of Hominoidea and Cer- resolved, however, by reference to the fossil record. Unlike copithecoidea. Colobinae and Cercopithecinae, early-to-middle Miocene Current widely accepted reconstructions of ancestral catar- cercopithecoids from Africa constituting the archaic subfam- rhine craniofacial morphology are based on the premise that ily Victoriapithecinae (12) retain a crista obliqua on upper similarities shared by extant colobines and are conser- molars, a hypoconulid on first and second lower molars, and vative retentions from the ancestral Old World higher buccally rotated lower from the ancestral catar- (1, 5, 6). The colobine/ (and, by inference, ancestral rhine condition. Victoriapithecinae accordingly represent the catarrhine) craniofacial morphology is typified by: a cranial sister group to extant Old World monkeys (2, 13, 14). vault of moderate to great height with globular frontal squama, Resemblances between Victoriapithecinae and either extant broad interorbital septum, short and wide nasal bones, short Old World monkey subfamily are, therefore, most parsimo- orthognathous snout, shallow zygoma, short/moderate infraor- niously viewed as typifying the common ancestor of known bital facial height, and abbreviated premaxilla with relatively fossil and modern cercopithecoids. narrow vertically implanted upper incisors set equally forward tExceptions may be a primitively broad interorbital septum (5, 6) and The publication costs of this article were defrayed in part by page charge the conformation of the nasoalveolar clivus and incisive canal (8, 9) payment. This article must therefore be hereby marked "advertisement" although details of polarity for subnasal morphology in great apes in accordance with 18 U.S.C. §1734 solely to indicate this fact. and are disputed (10, 11). 5267 Downloaded by guest on September 25, 2021 5268 Evolution: Benefit and McCrossin Proc. Natl. Acad ScL USA 88 (1991)

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FIG. 1. Facial remains of Victoria- pithecus. (A) Anterior facial reconstruc- tion based on specimens KNM-MB 19001 (frontal), 19689 (right zygomatic), and 18994 (left and right maxillae with P3-M3J (drawn by L. Tindimubona). (B) Lateral view of composite including specimens KNM-MB 19001, 19689, 18994, and 18993 ( with left and right I2-M3). (C) Anterior view offrontal (KNM-MB 19001). (D) Anterior view of right with P3-Ml (KNM-MB 18995). (E) Anterior view of left maxilla with P3-M3. l(Knm-MB 18994). (F) Lat- G eral view of left maxilla with PI-MI (KNM-MB 18994). (G) Palatal view of l I left and right maxillae with P3-M3. (KNM-MB 18994). DESCRIPTION AND COMPARISONS premaxilla, upper central alveolae positioned anterior to those of the lateral incisors, broad upper central incisors Until recently, the craniofacial morphology of Victoriapith- with long roots relative to the lateral incisors, a narrow ecinae was ill known. Excavation ofmiddle Miocene deposits inferiorly V-shaped nasal aperture of moderate height, and a on Maboko Island in western Kenya from 1987 to 1989 led to deep cheek region relative to facial height (Table 1). the discovery of a frontal, zygomatic, mandible, maxillae, The of (Fig. 1C) differs from and premaxillae of Victoriapithecus macinnesi (15). These the predicted ancestral Old World monkey morphotype in fossils provide the opportunity for an independent assess- having a narrow interorbital septum, with interorbital breadth ment, by outgroup comparison, of the morphocline polarity being only 13.3% of anterior biorbital breadth, like that of of colobine and cercopithecine craniofacial features. Recon- cercopithecine monkeys.$ The frontal is dominated by the struction of the ancestral cercopithecoid craniofacial mor- presence of distinct supraorbital costae (18) formed by coa- photype based on these discoveries can, in turn, be used to lescence of the anterolateral extents of the temporal lines address craniofacial morphotype reconstruction of the an- with the superciliary arches at the approximate midline of cestral eucatarrhine.§ each orbit, m. temporalis markings that converge relatively The facial morphology of Victoriapithecus (Fig. 1) differs anteriorly on the squamous portion, and absence of a pos- markedly in almost every respect from the Colobus-like face torbital depression behind glabella. These three features predicted for ancestral cercopithecoids. Like extant cercop- to the formation of a frontal ithecine monkeys, particularly Macaca (7) and Cercopithecus contribute trigon (19). (16), the Victoriapithecus face possesses: a moderately long muzzle and midfacial region, a long and anteriorly tapering 1Data for the index of anterior interorbital breadth x 100/internal biorbital breadth for 228 Colobus crania representing six yield a mean value of 19.1, with species means ranging from a §Extant Old World higher primates and their fossil relatives belong- minimum of 16.7 for Colobus () verus to a maximum of ing to the Cercopithecoidea and Hominoidea are referred to by the 20.1 for Colobus (Colobus) satanus (16). Data for 219 cercopithecin vernacular term eucatarrhine. The ancestral eucatarrhine is the crania yield a mean value of 11.6, with species means ranging from hypothetical last common ancestor of Cercopithecoidea and Hom- a minimum of9.7 for Miopithecus to a maximum of14.2 for inoidea. Cercopithecus hamlyni (16). Downloaded by guest on September 25, 2021 Evolution: Benefit and McCrossin Proc. Natl. Acad. Sci. USA 88 (1991) 5269

Table 1. Indexes of facial proportion for Victoriapithecus Index, x Facial characteristic Victoriapithecus* Cercopithecinae Colobinae Snout length (orbitale-prosthion/Ml tuberosities-prosthion) 0.65 (0.61-0.68) 0.62 (0.55-0.69)t 0.48 (0.45-0.51)t 0.39 (0.35-0.43)§ Malar height (orbitale-zygomaxillare inferior/P2-M2 length) 0.49 (0.39-0.60) 0.59 (0.49-0.71)1 0.27 (0.20-0.33)11 0.38 (0.36-0.39)** Numbers in parentheses are minimum and maximum for *, 1, 11, and ** and x ± 1 standard deviation for t, *, and §. *KNM-MB 18994, left maxilla with P2-M2 and KNM-MB 18995, right maxilla with PI-Ml. tTwelve Macaca (17). SNine Colobus (17). §Sixteen Hylobates (17). IFour Macaca. IIFour Colobus. **Two Hylobates.

RESULTS all colobine genera are viewed as derived (secondarily so for We interpret the facial similarities between Victoriapithecus the interorbital septum). and Cercopithecinae as indicating that the ancestral Old World monkey was characterized by a moderately long DISCUSSION anteriorly tapering snout with a long premaxilla, narrow interorbital septum, moderately deep cheek region relative to Insofar as the popularly reconstructed catarrhine ancestral morphotype was based in part upon the premise that facial height, and broad procumbent upper central incisors II colobines retain a craniofacial conformation similar to the (Table 2). Support for this interpretation comes from the fact common ancestor ofcercopithecoids and hominoids (1, 5, 6), that certain of these traits, often regarded as autapomorphic the revised cercopithecoid ancestral morphotype presented for Cercopithecinae, also occur in some extant and fossil here has important implications for reconstructing the cran- Colobinae (20). The fossil colobines , Rhi- iofacial morphotype ofthe ancestral eucatarrhine. In general, nocolobus, and Dolichopithecus, as well as the extant the relationships of noncercopithecoid fossil catarrhines to colobine Nasalis possess moderately long muzzles, deep extant Old World higher primate groupings are more ambig- malar regions, and narrow interorbital septae (21-24). A uous than are those of fossil cercopithecoids (2). Tradition- moderately long snout is also found in the fossil colobine ally, noncercopithecoid catarrhines have been regarded as (25) and in some populations of Colobus hominoids but, with the exception of a -Pongo guereza. Less convergence in the evolution of cercopithecid phyletic linkage (26-29), little consensus exists as to which craniofacial structure need be posited if these features are Oligo-Miocene catarrhines (if any) represent ancestors of the generally ancestral for Old World monkeys whereas the short hylobatids and great apes. Given the diversity of extant face and broad interorbital septum pertaining to most but not hominoid morphologies and the absence of unambiguous sister taxa, craniofacial morphoclines within Hominoidea remain equivocal. "Although the hypodigm of Victoriapithecus was at one time sug- The relatively orthognathous faces of the Miocene Euro- gested to include representatives of both Colobinae and Cercop- pean catarrhines (30, 31) and (32, ithecinae (7), this hypothesis has now been "abandoned" by its 33) have been held to corroborate a gibbon-like configuration original proponent (20). Clearly, if Victoriapithecus is viewed as an early representative of, for example, Cercopithecinae, then Colo- for ancestral hominoids (1, 6). Detailed study and phyloge- binae must have independently lost all vestiges of the upper netic analysis, however, indicate that the relationships of crista obliqua and lower first and second molar hypoconulid as well Pliopithecus lie outside the eucatarrhine radiation (2, 34-36) as undergoing a separate trend toward orthal alignment ofthe lower while the superfamily affinities of Oreopithecus continue to premolars. That this eventuality is appreciably less parsimonious be obscure (37-41). The craniofacial (and hence less likely) than that Victoriapithecus preceded the last conformations of plio- common ancestor of Colobinae and Cercopithecinae has been pithecids and oreopithecids may, therefore, be relevant only affirmed by several authorities (2, 12-14). as outgroups to the eucatarrhines. Table 2. Comparison of ancestral cercopithecoid craniofacial morphotypes Prevailing ancestral cercopithecoid Revised ancestral cercopithecoid Attribute craniofacial morphotype* craniofacial morphotype Temporal lines Weakly marked, well separated, and running Strongly marked and converging parallel throughout their course or anteriorly converging posteriorly Brow structure Simple superciliary arches Supraorbital costae Interorbital septum Broad Narrow Nasal bones Short and broad Long and narrow Snout length Short Moderately long Infraorbital facial height Shallow Deep Malar height Shallow Moderately deep Premaxilla Short and broad anteriorly Long and tapering anteriorly Upper central incisors Narrow, vertically implanted, and set as far Broad, procumbent, and set forward as upper lateral incisors anterior to upper lateral incisors *See refs. 1, 5, and 6. Downloaded by guest on September 25, 2021 5270 Evolution: Benefit and McCrossin Proc. Natl. Acad. Sci. USA 88 (1991) Consideration of the morphology of archaic representa- anteriorly convergent temporal lines, and the absence of a tives of the Hominoidea of demonstrable phylogenetic posi- postglabellar depression, interpreted here to be part of a tion should clarify the morphocline polarities of craniofacial complex related to small size. The coincidence ofthese attributes. The preponderance of evidence supports phylo- features in Aegyptopithecus and and similari- genetic placement of the early Miocene as ties in prognathism, depth of the zygoma, and infraorbital a hominoid predating the divergence of hylobatids and great facial height have been suggested to reflect a phyletic linkage apes** (46, 47). Known cranial remains of Proconsul mani- between the two genera (3, 61) or possibly "to prove to be fest maxillary, premaxillary, and zygomatic proportions of primitive catarrhine characters and thus not indicative of a moderate length and depth, intermediate between Hylobates close phylogenetic relationship" (54). Pervasive similarities and (48-50), and upper central incisors ofgreater breadth of the frontal, maxilla, premaxilla, and zygomatic morphol- (relative to upper second molar length) than those of extant ogy of Victoriapithecus, Afropithecus, and Aegyptopithecus colobines, gibbons with tendencies toward folivory (Hylo- lead us to strongly favor the latter interpretation. bates moloch and H. agilis), , Pliopithecus vindobon- We conclude that the facial morphology of cerco- ensis, and Oreopithecus.tt Afropithecus, known from the pithecoids, hominoids, and the common ancestor of eucata- early Miocene of Kenya (4), exhibits features such as elon- rrhines was not gibbon- or Colobus-like. Instead, the facial gation of upper premolars, reduced molar cingula, thick morphology of the ancestral Old World higher primate was molar enamel, and development of a mandibular inferior characterized by the presence of a frontal trigon, a moder- transverse torus suggestive ofa linkage with the great ape and ately long snout, moderate facial height below the orbits, a (53). The well-preserved cranium of Afropith- deep cheek region, anteriorly tapering premaxilla, and pro- ecus possesses a markedly long snout, anteriorly tapering cumbent upper incisors. premaxilla with broad and procumbent central incisors, a very deep cheek region, and tall facial height below the orbits We are grateful to the Office of the President of the Republic of Kenya and to the National Museums of Kenya for permission to (4, 54). Evidence from the stem hominoid Proconsul and a conduct research on Maboko Island and at the National Museums of candidate early member of the great ape and human clade Kenya. Special thanks are owed to Richard Leakey and Meave (Afropithecus), therefore, raises the possibility that moderate Leakey for their assistance in both administrative and scientific to long snouts, long premaxillae, moderate to deep infraor- aspects of this study. We also thank F. Clark Howell, John Fleagle, bital facial height, and broad and procumbent upper central Alan Walker, Steve Ward, and Eric Delson for comments on earlier incisors may typify both the basal hominoid and ancestral versions of this manuscript. Financial support for the project was great ape/human morphotypes. Among Miocene African provided by the National Geographic , Wenner-Gren Foun- dation for Anthropological Research, L. S. B. Leakey Foundation, hominoids, only , a possible representative of Fulbright Collaborative Research Program, Rotary International Hylobatidae, manifests a short muzzle and shallow infraor- Foundation, and the Boise Fund of Oxford University. bital facial height reminiscent of the gibbon and Colobus facial (17, 55). 1. Delson, E. & Andrews, P. (1975) in Phylogeny ofthe Primates: The well known Oligocene protocatarrhine** Aegyptopith- A Multidisciplinary Approach, eds. Luckett, W. P. & Szalay, ecus possesses a very small cranial vault, moderately long F. S. (Plenum, New York), pp. 405-446. muzzle, deep zygoma, moderate infraorbital facial height, 2. Harrison, T. (1987) J. Hum. Evol. 16, 41-80. and long premaxilla (3, 59, 60). Because this configuration 3. Simons, E. L. (1987) J. Hum. Evol. 16, 273-289. the catarrhine 4. Leakey, R. E. & Leakey, M. G. (1986) (London) 324, conflicts with reconstructed morphotype 143-146. based on Colobus and Hylobates (1, 6), the long face of 5. Vogel, C. (1966) Bibl. Primatol. 4, 1-226. Aegyptopithecus has been viewed as an "autapomorphy 6. Vogel, C. (1968) in and Phylogeny of Old World which would exclude it from the direct ancestry to all later Primates, ed. Chiarelli, A. B. (Rosenberg & Sellier, Turin, catarrhines" (2). By taking into consideration general simi- Italy), pp. 21-55. larities of craniofacial proportions between the revised an- 7. Delson, E. (1975) Contrib. Primatol. 5, 167-217. cestral cercopithecoid and hominoid morphotypes proposed 8. Ward, S. C. & Pilbeam, D. R. (1983) in New Interpretations of here, we regard the known facial morphology of Aegyptop- Ape and Human Ancestry, eds. Ciochon, R. L. & Corruccini, ithecus to accord reasonably well to a hypothetical catarrhine R. S. (Plenum, New York), pp. 211-238. ancestor. when musculoskeletal con- 9. Ward, S. C. & Kimbel, W. H. (1983) Am. J. Phys. Anthropol. Indeed, considering 61, 157-171. straints imposed by the possession of a small braincase in a 10. Martin, L. (1986) in Major Topics in Primate and Human fruit- and leaf-eating primate the size of Aegyptopithecus, it Evolution, eds. Wood, B., Martin, L. & Andrews, P. (Cam- is difficult to conceive of the gibbon- or Colobus-like face as bridge Univ. Press, Cambridge, England), pp. 161-187. possibly pertaining to an archaic catarrhine generally ances- 11. Shea, B. T. (1988) in , ed. Schwartz, J. H. tral to both Cercopithecoidea and Hominoidea. (Oxford Univ. Press, Oxford), pp. 233-257. One of the strongest points of similarity of Victoriapithe- 12. von Koenigswald, G. H. R. (1969) Fossil Vertebr. Afr. 1, cus, Afropithecus, and Aegyptopithecus is the structure of 39-51. the frontal. All three genera manifest supraorbital costae, 13. Leakey, M. G. (1985) Folia Primatol. 44, 1-14. 14. Benefit, B. R. & Pickford, M. (1986) Am. J. Phys. Anthropol. 69, 441-464. **In particular, the apparent absence of a tail (42) and the develop- 15. Benefit, B. R. & McCrossin, M. L. (1989) J. Hum. Evol. 18, ment of a lateral trochlear Keel (43) indicate a hominoid affinity for 493-499. the genus while the retention of a direct bony contact between the 16. Verheyen, W. N. (1962) Mus. R. Afr. Cent. Tervuren Belg. ulnar styloid process and the pisiform/triquetral embrasure (44, Ann. Ser. Octavo Sci. Zool. 105, 1-247. 45) clearly signals Proconsul's antecedence to the hylobatid/great 17. Fleagle, J. G. (1975) Folia Primatol. 24, 1-15. ape divergence. 18. Clarke, R. J. (1977) Thesis (Univ. of the Witswatersrand, ttData for extant primate dental dimensions are taken from Swindler South (51), those for Proconsul are from Andrews (52), and those for Johannesburg, Africa). Pliopithecus and Oreopithecus are from refs. 30-33. 19. Tobias, P. V. (1967) Olduvai Gorge (Cambridge Univ. Press, #lAegyptopithecus is referred to by the vernacular term protocatar- Cambridge, England), Vol. 2. rhine because although it possesses significant catarrhine apomor- 20. Strasser, E. & Delson, E. (1987) J. 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