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Home , Afropithecus, Ankarapithecus, Dryopithecus, Equatorius, Gigantopithecus, Griphopithecus

ANTHROPOLOGICAL SCIENCE Vol. 113, 53–64, 2005

Sivapithecus is east and is west, and never the twain shall meet DAVID R. BEGUN1*

1Department of Anthropology, University of Toronto, Toronto, Ontario, M5S 3G3, Canada

Received 26 June 2003; accepted 7 March 2004

Abstract and Dryopithecus are well-described hominids (great and ), both known since the 19th century. Over the years these genera have been combined into one (Dryopithecus) or separated up to the subfamily level. Each have been dismissed as interesting side branches, hailed as direct ancestors, or recognized as sister clades to one or more clade of extant hom- inid. Here I argue that they are each stem taxa of the two living hominid clades and Homi- ninae. A famous poem by Rudyard Kipling tells the tale of a British and Afghan soldier whose differences (in ethnicity) obscure their similarities (in character). The relationship between Sivapithe- cus and Dryopithecus is similar. On the one hand, Sivapithecus is restricted to South Asia, has thickly enameled molars, robust jaws, and superficially baboon-like forelimbs; Dryopithecus is European, has thinly enameled molars and gracile jaws, with suspensory forelimbs. On the other hand, both are great apes, both had suspensory adaptations, large brains, and delayed development, and both are closely related to living hominids. Recognition of the likely relations of Sivapithecus and Dryopithecus pro- vides insight into the causes, timing, and paleobiogeography of hominid origins.

Key words: hominid origins, Asia, Europe, climate change

Introduction [reviewed recently by Harrison (2002) and Ward and Duren (2002)] it seemed less likely to many researchers that Eur- “Sivapithecus is east and Dryopithecus is west, and never asian hominoids could be directly related to living the twain shall meet, Till climates change, shrink, taxa, though many continued to believe that Sivapithecus (or and hominids retreat. Alas, today they are neither east nor Ramapithecus) in particular had a specific relationship to west, on the continents of their birth, Since hominids moved humans (see Appendix for a classification of the Miocene South of Cancer from opposite ends of the earth” (shame- hominoids discussed here). lessly modified from Rudyard Kipling’s “The Ballad of East In the modern era most researchers now agree that Dryo- and West”, The One Volume Kipling Authorized, Double- pithecus and Sivapithecus are great apes, but there is dis- day, Doran & Company, Garden City, New York, 1928). agreement on their relations to living taxa. Most researchers Dryopithecus was first described in 1856 from conclude that Sivapithecus is a sister clade to Pongo. A few found in the foothills of the French , three years researchers, focusing primarily on differences between before Darwin’s publication of “On the Origin of ” Pongo and Sivapithecus in postcranial , but also in (Lartet, 1856). Lartet and most subsequent workers in the part on gnathic differences, have suggested that the fossil 19th century recognized the great affinities of this fossil taxon is either a stem great ape or a stem hominoid, without taxon, and a number noted the resemblances of Dryopithe- a direct relationship to Pongo (e.g. Benefit and McCrossin, cus to African apes (e.g. Gaudry, 1890). Sivapithecus was 1995; Pilbeam, 1997). In my view the case for a Pongo– first definitively described by Lydekker (1879), from fossils Sivapithecus clade, reviewed briefly below, is considerably from the Potwar Plateau of present day Pakistan, though he stronger. The relations of Dryopithecus are even less well originally named the taxon Paleopithecus [noting that Pale- agreed upon. A number of researchers also feel that Dryop- opithecus is preoccupied, Pilgrim (1910) introduced the ithecus is a stem hominid (Andrews, 1992) or hominoid nomen Sivapithecus]. Again, a number of researchers, (Benefit and McCrossin, 1995; Pilbeam, 1997). Others see including Lydekker, noted particular similarities to orangu- Dryopithecus as a member of a very diverse Pongo clade tans. Kelley (2002) and Begun (2002) review the history of that includes most Eurasian hominids, including Ouranop- these and other Eurasian hominoid discoveries. To make a ithecus and (Moyà-Solà and Köhler, 1993). long story short, once hominoids were recovered in Finally, some researchers view Dryopithecus as a member of the African ape and clade, along with Ouranopithe- * Corresponding author. e-mail: [email protected] cus, though these researchers disagree on the precise rela- phone: 1-416-978-8850; fax: 1-416-978-3217 tions among African apes and humans (e.g. de Bonis and Published online 30 September 2004 Koufos, 1993, 1997; Koufos, 1995; Begun et al., 1997; in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.04S008 Begun, 2001, 2002). I will argue here that most of the mor-

© 2004 The Anthropological Society of Nippon 53 54 D.R. BEGUN ANTHROPOLOGICAL SCIENCE phological evidence of Dryopithecus and (McCrossin et al., 1998; Ishida et al., 2004)], none show any points to a sister clade relationship to African apes and indication of any of below-branch quadrupedalism as in humans. extant and late Miocene hominoids. Both hypotheses of specific phylogenetic links between The principle distinguishing feature of the ‘griphopiths’ is Asian great apes on the one hand and Afro-European great their robust gnathic morphology, and this is probably related apes on the other are also consistent with proposed phyloge- to a novel adaptation to exploit a wider range of food types netic relations and paleobiogeographic patterns among other in the slightly more seasonal environments of the middle Miocene to recent Eurasian and African . They are Miocene of Eurasia (Heizmann and Begun, 2001). Ample also consistent with most estimates of divergence dates from evidence exists to indicate that the climate changes that molecular data and suggested patterns of dispersal caused by would lead eventually to the disappearance of tropical and changing ecological settings. The combined evidence of subtropical ecological settings in most of Eurasia were morphology, functional anatomy, phylogeny (morphology already under way at the beginning of the middle Miocene and molecular), climate change, and paleobiogeography (see below). provide the basis for a model of modern hominid origins. Eurasian Hominid Diversity Eurasian Hominid Origins It is intriguing that the ‘griphopiths’ have a European, Current evidence suggests that Eurasian hominids and Asian, and African distribution, and it is tempting to con- middle Miocene African hominoids derive from one or more clude that this represents the initial separation of both Eur- members of a group (probably paraphyletic) loosely referred asian great ape clades and the African ape clade (Figure 1). to here as the ‘griphopiths’. This includes However there is no evidence for this. Griphopithecus from Europe and Turkey, and (or Griphopithe- alpani does not share any derived character with any late cus), and from . The Miocene hominid, despite tentative suggestions to the con- cf. Griphopithecus from Engelswies, Germany and Gripho- trary (e.g. Alpagut et al., 1990). Similarly, Equatorius, Ken- pithecus alpani from Paşalar and Çandır, Turkey are appar- yapithecus, and Nacholapithecus do not share specific ently the oldest ‘griphopiths’, though some uncertainty synapomorphies with great apes, again despite a few claims persists with regard to the age of the Turkish samples. Ger- to the contrary (e.g. McCrossin et al., 1998; Ishida et al., man and Turkish Griphopithecus is currently estimated to be 2004). While the nasoalveolar clivus of Nacholapithecus has ~16–16.5 Ma (Heizmann and Begun, 2001; Begun et al., been interpreted as elongated and overlapping with the max- 2003). African and Slovakian ‘griphopiths’ are younger, at illary palatine process, resulting as well in some reduction of ~15 Ma (Steininger, 1999; Ward et al., 1999). African the incisive foramina, other similarities to great apes are ‘griphopiths’ may have evolved from Eurasian Griphopithe- lacking. These premaxillary similarities are more parsimoni- cus, though the fossil record of middle Miocene hominoids ously interpreted as homoplasies possibly related to the in Africa is very poor and the possibility that in situ ances- enlarged anterior of Nacholapithecus, apparently tors existed cannot be dismissed. ‘Griphopiths’ from all also shared by (Ishida et al., 2004). All of these three continents are united by a suite of derived characters taxa are best viewed as broadly ancestral to all hominids. that distinguish them from early Miocene hominoids such as Because the ‘griphopiths’ are distributed widely both geo- , including large, thickly enameled molars with graphically and temporally, it is not clear exactly when and low cusps and restricted dentine penetrance, some reduction where the two main clades of living hominids evolved (Fig- in cingulum development and frequency, robust jaws, and ure 1). However, by ~12.5 Ma both are established in their certain modifications to the upper . They are distin- respective regions, Sivapithecus in Chinji Formation depos- guished from Afropithecus in lacking the autapomorphic its in the Potwar plateau and Dryopithecus from St. Gaudens features of the anterior dentition, , palate, and in France and St. Stefan in Austria (Kappelman et al, 1991; (Leakey and Walker, 1997). One ‘griphopith’, Steininger, 1999). All hominids from the Potwar plateau are Nacholapithecus, more closely resembles Afropithecus in currently attributed to Sivapithecus (Kelley, 2002), though having a relatively long and more horizontal nasoalveolar the earliest specimens from Chinji are much more poorly clivus and robust, relatively low-crowned upper canines, but preserved than at later Potwar localities, from which the bulk lacks most of the dental features and the deep of of Sivapithecus is known. This is interesting because Afropithecus (Ishida et al., 2004). It may be in the end that from Anatolia, of equivalent age to much of Nacholapithecus is more closely related to Afropithecus and the Sivapithecus sample (from the Nagri Formation, which is not a ‘griphopith’. is ~10 Ma and occurs in the middle of the Potwar hominid Very little is known of the of the ‘griphopiths’ sequence) is related to Sivapithecus but lacks key derived beyond the gnathic region, but postcranially they are as a characters and is thus excluded from the Sivapithecus– group broadly similar to early Miocene hominoids (Begun, Pongo clade (Alpagut et al., 1996; Begun and Güleç, 1998; 1992, 2002; Benefit and McCrossin, 1995; McCrossin and Kappelman et al., 2003). It is possible that the Sivapithecus– Benefit, 1997; Nakatsukasa et al., 1998; Ward and Duren, Ankarapithecus–Pongo clade evolved somewhere in the 2002). While all of the later-occurring taxa from East Africa eastern Mediterranean–South Asian area and dispersed have individual postcranial autapomorphies suggestive of within the region into a number of taxa. If Chinji (the oldest) specialized adaptations [e.g. elongated, robust forelimbs in hominids are the ancestors of this radiation, then they would Nacholapithecus; indications of terrestriality in Equatorius have to be a different from Sivapithecus and Ankarap- Vol. 113, 2005 ASIAN AND AFRICAN GREAT APES DIVERGED IN EURASIA 55

opithecus is known from Spain (Can Vila, Can Mata, Castel de Barbera), France (St. Gaudens, La Grive), and Austria (St. Stefan), all of which are dated mainly on the basis of the absence of typical late Miocene taxa [true mice (murids) and three-toed horses (hipparionines)]. These localities are usu- ally attributed to the European land biochronologic zone known as MN 7/8, which is correlated to localities dated between about 14 and 11.5 Ma (Steininger, 1999). Thus they are roughly contemporaneous with earliest Sivap- ithecus, though they could be a bit older or younger. As with Sivapithecus, Dryopithecus radiates in situ into at least four species distributed from Spain in the west to Hungary and possibly Georgia in the east [the possibility of Dryopithecus in East Asia exists but is currently unsubstantiated (Kelley, 2002)]. In the late Miocene, hominids diversify at the generic level in both Europe and Asia. Between about 10 and 7 Ma, Sivapithecus radiates into a diversity of taxa in Asia and Dryopithecus does the same in Europe. Ouranop- ithecus appears in Greece and possibly Anatolia between about 9.5 and 7–8 Ma, possibly as a derived member of the Dryopithecus clade (see below). Oreopithecus may be a part of the same radiation (Harrison and Rook, 1997), though in my view this late Miocene taxon is a distinct clade (Begun, 2002). Sivapithecus apparently shares an ancestry with and . Gigantopithecus is a problematic taxon because it is known only from lower jaws and isolated teeth, the large size of which make them look similar. It is quite possible that this includes more than one genus, one represented by the Miocene specimens (Giganto- pithecus giganteus) and the other by fossils (Gigantopithecus blacki). Once again, more and better pre- served specimens are needed. Lufengpithecus is represented by large samples from Province, China, that provide evidence of a distinctive cranial morphology in combination with dental and postcranial similarities to Pongo (Schwartz, 1997; Kelley, 2002; personal observations). Because Sivap- ithecus more closely resembles Pongo in facial morphology while Lufengpithecus more closely resembles Pongo in den- tal morphology, the relations among these taxa are not com- Figure 1. Paleobiogeography of late early to early middle Miocene pletely clear, though most researchers agree that all are hominoids. (A) In the Karpatian, hominoids enter western Eurasia members of the same clade. before the Langhian transgression temporarily stops land mammal migrations between Eurasia and Africa. The source may have been East Africa (Afropithecus) or Saudi Arabia (Heliopithecus). The earlier Eurasian Hominid Phylogeny hominids (‘griphopiths’) first appear in Europe east of the Rhine gra- ben (dotted line) and in Anatolia. (B) After the Langhian (Badenian) Europe ‘griphopiths’ spread and have thus far been recovered in Slovakia and As noted earlier, relations among European middle and East Africa. Sometime toward the end of this initial dispersal period late Miocene hominids and between them and living homi- the clades of living hominids emerged. Pongines may have evolved from western Eurasian ancestors while hominines may have evolved nids are currently debated. Rather than reviewing this litera- in situ in the west. In this and in Figure 3 the shaded areas represent ture here [it is reviewed in Begun (1994, 2001, 2002), Begun exposed land surfaces as reconstructed by Rögl (1999). and Kordos (1997), and Kordos and Begun (2001b)] I will simply review the evidence that supports the conclusions my colleagues and I have reached concerning European homi- nids. ithecus, its putative descendents (Begun and Güleç, 1998). In an analysis of 240 characters in fossil and living homi- Only more complete fossils from Chinji age deposits can noids (Begun et al., 1997), more recently expanded to 247 answer this problem. characters (Begun, 2001), we found that Dryopithecus alone The origins of Dryopithecus are similarly murky. The old- or Dryopithecus and Ouranopithecus together are sister est specimens of Dryopithecus are roughly the same age as clades to the African apes and humans. The numerous char- Sivapithecus, though this is based on less reliable evidence acters that represent synapomorphies of the great from relatively small faunal samples. Middle Miocene Dry- apes  Dryopithecus and African apes  Dryopithecus 56 D.R. BEGUN ANTHROPOLOGICAL SCIENCE clades are listed in Table 1. Using a smaller number of char- trated palate, as in Proconsul [the premaxilla separated from acters from a restricted anatomical region (20 features of the the palatine process by a foramen (fenestra) rather than a face), three features have been used to suggest that Dryop- canal (Schwartz, 1983)]. In Nacholapithecus there is more ithecus is more closely related to Pongo (Moyà-Solà and overlap with the maxilllary palatine process, but the overall Köhler, 1995). The problem here, beyond their very small configuration is nonetheless similar to Afropithecus (Ishida number, is that these characters are actually variable in Dry- et al., 2004). In African apes and humans, Dryopithecus, and opithecus (Hungarian Dryopithecus differs in all of these Ouranopithecus the nasoalveolar clivus region consists of an features from Spanish Dryopithecus), or they are based on a elongated premaxilla that is thick labiolingually and bi-con- reconstruction that can be interpreted differently (Begun and cave labially. It overlaps to varying degrees with the palatine Kordos, 1997; Kordos and Begun, 2001b). So they do not process of the but is vertically displaced and not in characterize most known Dryopithecus crania. Furthermore, contact with the palate in the midline, thus contributing to a all of these characters are known to be variable, and thus of step into the nasal fossa. , Dryopithecus, and Ouran- unpredictable phylogenetic significance in hominids gener- opithecus have relatively short premaxilla and limited over- ally (Eckhardt and Eckhardt, 1995; Msuya and Harrison, lap with the palatine process while and 1996). have more elongated premaxilla with more Among the most important apparent synapomorhies of the extensive overlap. The former condition has been inter- Afro-European great ape clade are the morphology of the preted as primitive for the African ape and human clade temporal bone, the premaxilla and the basic architecture of (including the Eurasian fossil taxa) and the latter a synapo- the cranium. Although the temporal bone of Ouranopithecus morphy of the Pan–hominin clade (Begun, 1992, 1994). is not known, in Dryopithecus the tympanic and articular The remaining synapomorphies of the Afro-European portions are fused, the entoglenoid process is strongly devel- hominid clade are too numerous to summarize here (Table oped, and the glenoid fossa is relatively deep. These are 1). It is simply worth noting that these features come from detailed developmental and morphological features shared many regions of the cranium, as do the synapomorphies of with African apes and humans in a region that has been the great apes found in Dryopithecus. It seems highly found to have a strong phylogenetic signal in hominids unlikely that they are all functionally or structurally interre- (Brown and Ward, 1988). A new specimen of Dryopithecus lated (though some may be), and more likely that most rep- from Rudabánya, Hungary shows clearly for the first time resent distinct evolutionary transformations. Given their that the face of this taxon is klinorhynch, or ventrally number and diversity it is therefore very unlikely that all rotated, as in African apes and humans. While it is less well appear in parallel in European and African taxa. preserved, the cranium of Ouranopithecus was probably kli- norhynch as well (Begun, 1994; Begun and Kordos, 1997; Asia Kordos and Begun, 2001b). Ventral rotation of the face rela- A comprehensive review of the evidence for an Asian tive to the neurocranium in African apes has been related to great ape clade is beyond the scope of this paper, especially the development of the supraorbital structures (supraorbital since several recent reviews are available (Ward, 1997; tori/supratoral sulci), both of which are also more strongly Kelley, 2002). I touched earlier on the possible relations developed in Dryopithecus and Ouranopithecus than in other Miocene apes, though less strongly developed than in Africa apes and most humans (Shea, 1988; Begun, 1994). Finally, three specimens from Rudabánya preserve partial Table 1. Great ape and African ape cranio-dental premaxillae and anterior nasal fossae, all indicating the pres- character states of Dryopithecus ence of a stepped subnasal fossa and a true incisive canal Great ape character states African ape character states (Begun, 1992, 1994; Begun and Kordos, 1997; Kordos and Labiolingually thick incisors Bi-convex premaxilla Begun, 2001b). All three specimens (RUD 12, RUD 44/47, Compressed canines Stepped subnasal fossa and RUD 200) are damaged in this region, but together a Elongated premolars and molars Patent incisive canals good picture of the morphology of the region emerges, espe- M1  M2 Broad, flat nasal aperture base cially in light of newly recovered fragments and teeth that No cingula Shallow canine fossa are associated with RUD 44/47 (Kordos and Begun, 2001a; Reduced Supraorbital torus Begun, 2002). The Dryopithecus fossil evidence in its heteromorphy High root of the zygomatic Inflated glabella entirety has not been considered in previous interpretations Elongated midface Frontal sinus above and below of this region (e.g. Ward and Kimbel, 1983; Ward and Pil- nasion beam, 1983; McCollum and Ward, 1997). While other fossil Broad nasal aperture Projecting entoglenoid process taxa have been said to demonstrate a stepped subnasal fossa below the orbits or an elongated premaxilla, none other than Dryopithecus Reduced midfacial prognathism Fused articular and tympanic and Ouranopithecus among Miocene apes has the full suite temporal Elongated, robust premaxilla Broad temporal fossa of features that typify this region in living African apes and Premaxilla–palatine overlap Deep glenoid fossa in ‘’. For example, Afropithecus and Shallow subarcuate fossa Elongated neurocranium Nacholapithecus have moderately elongated premaxillae but Enlarged Moderate alveolar prognathism ones that are relatively horizontal, labiolingually com- Large brain Klinorhynchy pressed with little or no overlap with the palatine process. High cranial base Afropithecus has the typical mammalian pattern of a fenes- Modified from Kordos and Begun (2001b). Vol. 113, 2005 ASIAN AND AFRICAN GREAT APES DIVERGED IN EURASIA 57

Figure 2. Phylogenetic relations and geographic distribution of some of the taxa discussed in the text. To save space, Griphopithecus repre- sents the ‘griphopiths’ Griphopithecus, Equatorius, Kenyapithecus, and Nacholapithecus. among Sivapithecus, Ankarapithecus, Lufengpithecus, and nids it is almost certainly the primitive condition, being Gigantopithecus (see Figure 2). I will focus briefly on some found in the ‘griphopiths’ and to some extent in earlier problem areas. clades (e.g. Afropithecus), though it recurs periodically Sivapithecus is widely believed to be the sister taxon to (Ouranopithecus, Australopithecus, Gigantopithecus). Thus Pongo (Pilbeam, 1979, 1982; Andrews and Cronin, 1982; it is not too surprising that Sivapithecus may retain a number Ward and Pilbeam, 1983; Kelley and Pilbeam, 1986; Brown of primitive features while sharing other characters with and Ward, 1988; Andrews, 1992; Ward, 1997; Kelley, 2002). Pongo, an example of one of the most commonly observed Disagreement comes from two main sources. On the one phenomena in paleobiology, mosaic evolution. hand, certain aspects of the morphology of Sivapithecus are Other apparent homoplasies are more difficult to explain. distinctly unlike that of Pongo. On the other hand, for some Several authors have noted that Sivapithecus lacks a number of these anatomical regions fossils more closely resembling of postcranial characters present in Pongo. While some of Pongo are known. From the perspective of larger patterns of these can also be attributed to the fact that Pongo and its dispersals and origins discussed here there are two important ancestors have experienced millions of years of selection questions that arise from these objections. Are any of the since Sivapithecus (e.g. the absence of a fovea for the liga- Asian fossil great apes specifically related to Pongo and if mentum teres of the in Pongo), others are not so easily so, which clade is the most likely sister taxon? dismissed as mosaic evolution. In particular, the upper fore- Most of the researchers cited above have noted that the limb morphology of Sivapithecus is said to be too primitive face of Sivapithecus is remarkably similar to that of Pongo for the taxon to be related to Pongo (Benefit and McCrossin, in many details of the premaxilla, subnasal fossa, anterior 1995; Pilbeam, 1996, 1997). This is based primarily on the nasal and periorbital regions, temporal bone morphology, observations that the proximal half of the shaft of the dental implantation, and various aspects of dental propor- humerus in Sivapithecus is retroflexed or bent posteriorly tions. However, most of these authors and others who have and distally (concave posteriorly), as in early Miocene hom- described this material (e.g. Pilbeam et al., 1980; Kelley, inoids, monkeys, and indeed most mammals (Pilbeam et al., 1988; Brown, 1997) also note that Sivapithecus gnathic mor- 1990; Rose, 1997; Madar et al., 2002). The region is also phology is generally more robust, particularly the mandible characterized by a very strongly developed platform for the and zygomatic, than in similarly sized Pongo (only the insertion of the pectoralis major and deltoideus muscles. In larger specimens of Sivapithecus fall within the range of contrast, the proximal humerus of Dryopithecus and all other Pongo, and even here they are for the most part within the hominids is anteroflexed (smoothly concave anteriorly), or female Pongo range). The canine crowns tend to be shorter straight, depending on the taxon. The humeral morphology and more robust and the postcanine dentition is large, thickly of Sivapithecus has impressed many researchers for a num- enameled with broad, low, rounded cusps, shallow basins, ber of good reasons. Sivapithecus is uniquely different from and low dentine penetrance. This suite of characters has all other hominids; it appears to share a morphology with been related by many authors to powerful mastication (e.g. most other mammals; this morphology of the humerus is Kay, 1981) and in fact occurs in many living and extinct pri- associated with a fundamental aspect of behavioral ecology mate clades (Begun, 2001, 2002). In the case of the homi- (retroflexed humeri are associated with pronograde quadru- 58 D.R. BEGUN ANTHROPOLOGICAL SCIENCE peds and anteroflexed humeri with suspensory hominoids). Eurasian Hominid Dispersals and These considerations have led some to question the phyletic link between Sivapithecus and Pongo (e.g. Pilbeam, 1997; The phylogeny depicted in Figure 2 has implications for Larsen, 1998). the origin of the modern clades of the great apes and There is a risk here of throwing the baby out with the bath humans. Cladistic relations among Eurasian and African water. Anatomical complexes that contribute in an inte- extinct and living hominids suggest that African hominids grated fashion to specific adaptations (i.e. suspensory posi- derive from a European ancestor and Pongo derives from an tional behavior) can be modified with various characters Asian ancestor (Begun, 1994, 2001; Begun et al., 1997). decoupled from others in response to specific selective pres- This view has been supported by genetic evidence (Stewart sures. Good examples include the and and Disotel, 1998) and criticized based on differences in the hip of Pleistocene to recent . Both are clearly interpretations of phylogeny discussed above and on per- adapted to and thus integrated tightly to numer- ceived limitations of the fossil record. With regard to the lat- ous other postcranial attributes, but both are easily distin- ter, it has been noted that Africa is huge and barely sampled, guished from one another (Lovejoy, 1974; Stern and especially in the late Miocene, but a large number of late Susman, 1983). Differences in the paleobiology of each Miocene localities are in fact known, many preserving taxon accounts, at least in part, for dramatic differences in a paleoecological indications of forested settings (Begun, part of the anatomy that is otherwise critical to the normal 2001). The hypothesis that African hominids originated in functioning of an essential aspect of their adaptation. If one Europe or western Asia is not based simply on the absence were to predict that a fossil with a -sized femoral of evidence from Africa. It is based on two phylogenetic head could not have been from a biped, one would be wrong conclusions. Firstly, the hominine clade is present in Europe in the case of Australopithecus despite strong correlations in the late Miocene (Begun et al., 1997; Begun, 2001). Sec- and good biomechanical arguments. We know this because ondly, the few contemporaneous hominoids from Africa are we have a relatively good knowledge of the anatomy of the not cladistically hominid (Begun, 2001). is hip of Australopithecus. We do not have a good knowledge clearly primitive (Begun, 1994; Singleton, 2000). Sambu- of the shoulder of Sivapithecus. The proximal humerus of rupithecus superficially resembles in a few aspects Sivapithecus, like the proximal femur of Homo, may have of molar morphology but retains many primitive dental and been modified in response to selection for a biomechanically maxillary characters (Begun, 2001). The isolated teeth from different form of an otherwise similar positional behavior, Ngorora have been described as having affinities primarily antipronograde quadrupedalism, without losing the adapta- with the Proconsuloidea or middle Miocene East African tion entirely. hominoids (e.g. Equatorius) (Hill and Ward, 1988; Begun, In the end, Sivapithecus has more hominid-like postcra- 2001; Hill et al., 2002). nial attributes than not, and those, primarily of the proximal Even if the absence of the hominine clade in Africa before humerus, that are non-hominid like are probably autapomor- the latest Miocene represents a sampling bias, why is it phies of that genus, and have no bearing on the issue of its present in Europe? If European hominids are not related to relationship to Pongo (Begun et al., 1997; Rose, 1997). Par- African hominids, then why do they share so many charac- simony and an appeal to other examples in the hominoid fos- ters with African hominids? These may be homoplasies, but sil record both support the phylogeny depicted in Figure 2. as noted above this is highly unlikely. In other words, Eur- For the purposes of this paper it is not necessary to resolve asian late Miocene hominids are most reasonably interpreted the issue of which Asian late Miocene hominid is most as hominids: those from Europe are stem hominines (Afri- closely related to Pongo. Recent discoveries of Lufengpithe- can apes and humans), and the Asian late Miocene hominids cus in Thailand with postcanine teeth more closely resem- are stem pongines (Pongo). It is on this basis that I would bling those of Pongo may help resolve this debate explain the fact that a crown hominid (related to both Afri- (Chaimanee et al., 2003), especially when cranial and post- can and Asian hominids) has not yet been found in Africa. cranial material is recovered. Despite the fact that Pongo, On the other hand it may well be that the Afro-European Lufengpithecus from China, and cf. Lufengpithecus from hominine clade was widely distributed across Europe, west- Thailand share complexly crenulated molar occlusal sur- ern Asia, and Africa, but that up until now they have only faces, the faces of Sivapithecus and Pongo much more been found in Europe. It is certainly possible that new fossil closely resemble one another than do the faces of Pongo and discoveries will show that the African ape and human clade Lufengpithecus. As with European hominids, it seems that remained in part in Africa; that the clade expanded into there is great diversity in this radiation of Asian great apes. Europe but a core remained in Africa; and that in the end Sivapithecus is more likely to be the sister clade to Pongo. It European hominines went extinct and African taxa, cur- could be that attributes characteristic of Pongo in Lufeng- rently unknown, are the true ancestors of the African ape and pithecus and cf. Lufengpithecus are emergent in the mor- human clade. phology or development of the postcanine dentition of this I have suggested that hominids moved south from Eurasia clade (they occur occasionally in Sivapithecus as well), in response to global climate changes that produced more providing a plausible explanation for the homoplastic seasonal conditions in Eurasia toward the end of the appearance of this feature. Miocene [Begun (2001) based in part on Quade et al. (1989), Leakey et al. (1996), Cerling et al. (1997) and many others]. This scenario seems to hold up reasonably well in the east. Whichever Miocene taxon is ultimately related to Pongo, all Vol. 113, 2005 ASIAN AND AFRICAN GREAT APES DIVERGED IN EURASIA 59 occur north of the current range of the living taxon, consis- tent with a climatic change that made it more challenging for hominids to live north of the Tropic of Cancer. In the west, if hominines originated in Europe or western Asia, the paleo- biogeographic model is consistent with that from East Asia; they moved south at the end of the Miocene as well. If an unknown core of hominines has yet to be found in Africa, this model needs revision to account for the origin of the hominines (Figure 3).

Corroborating evidence Ample evidence now exists for a gradual degradation in climate throughout much of Eurasia in the late Miocene, which with additional factors, mainly tectonic, culminated in the development of markedly more seasonal conditions and a number of dramatic ecological changes. The most spectac- ular in the Miocene is the Messinian salinity crisis that led to the dessication of the at the end of the Miocene (Hsü et al., 1973; Clauzon et al., 1996; Krijgsman et al., 1999). Other consequences include the development of Asian , desertification in North Africa, the early phases of polar ice cap expansion and the expan- sion of North American grasslands (Garcés et al., 1997; Hoorn et al., 2000; Zhisheng et al., 2001; Griffin, 2002; Guo et al., 2002; Janis et al., 2002; Liu and Yin, 2002; Wilson et al., 2002). In both Europe and Asia subtropical forests retreated and were increasing replaced by more open coun- try, including true grasslands and steppes (Bernor et al., 1979; Bernor, 1983; Fortelius et al., 1996; Cerling et al., 1997; de Bonis et al., 1999; Magyar et al., 1999; Solounias et al., 1999; Fortelius and Hokkanen, 2001). It is important to note that in some places forests persisted and elsewhere more severe changes occurred, creating a number of refugia, some of which continued to host hominids well into the period of climatic deterioration. This is the case for the Oreopithecus localities of Tuscany and Sardinia (Harrison and Rook, 1997). Other well known localities such as Dorn- Dürkheim in Germany retained a strongly forested character though they lack hominoids (Franzen, 1997; Franzen and Storch, 1999). For the most part though, hominids disappeared from Europe and western Asia in the late Miocene, but not all at Figure 3. Paleobiogeography of late Miocene hominids. (A) At once. There is a gradient of extinctions of forms from the end of the middle Miocene into the late Miocene hominines diver- west to east, corresponding to the gradient of appearance of sify in western Eurasia and pongines in South and East Asia, while hominids in Africa become extinct. The one exception to the title of more open country faunas from west to east (Bernor et al., this paper may be in central Anatolia (doubled ended arrow) where 1979; Fortelius et al., 1996; Begun, 2001). Between about one clade of pongine (Ankarapithecus) appears after the earliest 12 and 10 Ma Dryopithecus disappeared from localities in appearance of the clade in South Asia, though in fact no hominines are Europe, becoming very rare by 9.5 Ma in Spain and Ger- known from Anatolia at this time. (B) After ~9 Ma hominids progres- many, and there represented only by one or two specimens. sively go extinct in most of Eurasia, starting in the west and moving east. During this time hominines first appear in Africa, and probably in This is despite the persistence locally of apparently suitable Southeast Asia as well. ecological settings such as at Dorn-Dürkheim (Franzen, 1997). This wave of extinctions ends coincident with an important faunal event in western Europe known as the mid- Vallesian event, when a major turnover of terrestrial faunas to Udabnopithecus from the 8–8.5 Ma locality of Udabno in led to the widespread of local taxa generally Georgia (Gabunia et al., 2001). attributed to the development of more open conditions In the eastern Mediterranean hominids persisted to the (Moyà-Solà and Agustí, 1990; Fortelius et al., 1996). The end of this time period and perhaps somewhat beyond. youngest specimens possibly attributable to Dryopithecus Ouranopithecus in Greece is mainly known from the end of are so far east that they are actually Asian, though still west the hominid reign in Europe, and may be a terminal taxon of of Sivapithecus localities. These teeth are currently assigned the Dryopithecus clade (Begun and Kordos, 1997). In Ana- 60 D.R. BEGUN ANTHROPOLOGICAL SCIENCE tolia at the eastern edge of the faunal province that includes ties to later hominins (Begun, 2004)]. They did not. Dryo- Greece and the eastern Mediterranean [the Greco-Iranian pithecus and Ouranopithecus are sister taxa to the ancestor province (de Bonis et al., 1999)] a new, very large hominid of the African ape and human clade. The actual last common resembling Ouranopithecus may be as young as 7–8 Ma in ancestor of that clade is not known. However, the distribu- age (Sevim et al., 2001). During this time, forest taxa were tion of characteristics of modern and fossil hominines sug- increasingly replaced by more open country forms. This is gests that this last common ancestor would most likely have true of virtually all mammalian orders. Among the , been woodland or forest dependent and but strongly terres- hominoids declined and cercopithecoids were on the trial, that is, a knuckle-walker (Richmond et al., 2001). increase (Andrews et al., 1996). Grazing ungulates and grassland or dry ecology adapted micromammals also Conclusions become more common (Fortelius et al., 1996; Agustí et al., 1999; de Bonis et al., 1999; Solounias et al., 1999). The phylogenetic divide between Asian and Afro-Euro- The dispersal of late Miocene faunas between Eurasia and pean great apes is deep. The east and west have been sepa- Africa is complex and has intercontinental sources. Though rated for at least 14–16 Ma. On the other hand, both lineages the dominant signature was the rise of open country taxa, responded in similar ways to the changing ecological set- forest forms persisted and dispersed as well, including hom- tings of late Miocene Eurasia. Both for the most part inids. Among the more open country forms horses dispersed remained true to their forest ecology origins, and both from North America to the Old World, and modern bovids moved south as the forests retreated in that direction. and giraffids appear to have dispersed from Europe to Africa (Dawson, 1999; Solounias et al., 1999; van der Made, 1999; Acknowledgments Agustí et al., 2001). Among the more closed-setting mam- mals, hippos moved from Africa to Europe, and pigs of vary- I am grateful to the organizers of the international sympo- ing ecological preferences moved from Asia to Europe and sium “Asian Paleoprimatology: Evolution of the Tertiary Africa (Fortelius et al., 1996; van der Made, 1999). Small Primates in Asia” for inviting me to participate and to the carnivores (mustelids, felids and viverrids), larger carni- editors of Anthropological Science for producing this spe- vores (ursids, hyaenids), porcupines, rabbits, and chalico- cial volume. Special thanks go to Masanaru Takai as editor theres, most of which also prefer more closed settings, also of this special volume for all his hard work. I am also grate- dispersed from Eurasia to Africa (Leakey et al., 1996; Gins- ful to Masato Nakatsukasa and an anonymous reviewer for burg, 1999; Heissig, 1999; van der Made, 1999; Winkler, thoughtful comments that improved this manuscript. 2002). In sum, phylogenetic analysis suggests that the ances- tors of many African mammals had appeared in the Valle- sian of Eurasia. Ecologically many of these new taxa were References adapted to more open country conditions (hypsodonty, cur- Agustí J., Cabrera L., Garcés M., and Llenas M. 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Appendix. Classification of hominoids included in this analysis Hominoidea ‘Eohominoidea’ Proconsul Afropithecidae Afropithecus Heliopithecus ‘Eohominoidea’ indet. (‘griphopiths’) Griphopithecus cf. Griphopithecus Equatorius Nacholapithecus Kenyapithecus ‘Euhominoidea’ Hominidae Dryopithecus Ouranopithecus Pan Gorilla Homo Ponginae Sivapithecus Lufengpithecus Pongo Gigantopithecus Ankarapithecus Not all possible ranks are named here. The ranks ‘Eohominoidea’ and ‘Euhominoidea’, hominoids of primitive and modern aspect, respectively, are informally used here. See text.