Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

David R. BEGUN University of Toronto, Department of Anthropology, 19 Russell Street, Toronto, ON, M5S 2S2 (Canada) [email protected]

Begun R. D. 2009. — Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade. Geodiversitas 31 (4) : 789-816.

ABSTRACT Darwin famously opined that the most likely place of origin of the common ancestor of African apes and humans is Africa, given the distribution of its liv- ing descendents. But it is infrequently recalled that immediately afterwards, Darwin, in his typically thorough and cautious style, noted that a fossil ape from Europe, Dryopithecus, may instead represent the ancestors of African apes, which dispersed into Africa from Europe. Louis de Bonis and his collaborators were the fi rst researchers in the modern era to echo Darwin’s suggestion about apes from Europe. Resulting from their spectacular discoveries in Greece over several decades, de Bonis and colleagues have shown convincingly that African KEY WORDS ape and human clade members (hominines) lived in Europe at least 9.5 million Mammalia, years ago. Here I review the fossil record of hominoids in Europe as it relates to Primates, Dryopithecus, the origins of the hominines. While I diff er in some details with Louis, we are Hispanopithecus, in complete agreement on the importance of Europe in determining the fate Rudapithecus, of the African ape and human clade. Th ere is no doubt that Louis de Bonis is Ouranopithecus, hominine origins, a pioneer in advancing our understanding of this fascinating time in our evo- new subtribe. lutionary history.

GEODIVERSITAS • 2009 • 31 (4) © Publications Scientifi ques du Muséum national d’Histoire naturelle, Paris. www.geodiversitas.com 789 Begun D. R.

RÉSUMÉ Les Dryopithèques, Darwin, de Bonis et l’origine européenne du clade des grands singes d’Afrique et de l’homme. L’avis réputé de Darwin était que l’endroit le plus probable de l’origine de l’ancêtre commun des grands singes africains et de l’homme est l’Afrique, étant donné la distribution des descendants actuels. Mais il est rarement rappelé que immédia- tement après, Darwin, dans son style typiquement minutieux et prudent, indi- quait qu’un grand singe européen, Dryopithecus, représentait peut-être un ancêtre potentiel des grands singes d’Afrique, qui se seraient dispersés de l’Europe vers l’Afrique au cours du Miocène. Louis de Bonis et ses collaborateurs furent parmi les premiers chercheurs de l’ère moderne à adopter cette suggestion de Darwin. Suite à leurs découvertes spectaculaires en Grèce pendant plusieurs décennies, de Bonis et ses collègues ont démontré d’une façon convaincante que des mem- bres du clade des grands singes d’Afrique et de l’homme ont persisté en Europe MOTS CLÉS jusqu’à 9,5 millions d’années au moins. Je résume ici l’histoire des découvertes Mammalia, en Europe concernant l’origine des hominiens. Bien que mes conclusions se dis- Primates, Dryopithecus, tinguent dans les détails de celles de Louis, nous sommes entièrement d’accord Hispanopithecus, sur l’importance de l’Europe dans le destin du clade des grands singes africains Rudapithecus, et de l’homme (Bonis & Koufos 2004). Il n’y a pas de doute que Louis de Bonis Ouranopithecus, origines des hominiens, est un pionnier qui a contribué d’une façon exceptionnelle à nos connaissances sous-tribu nouvelle. de cette période fascinante de notre histoire évolutive.

INTRODUCTION humans to the exclusion of orangutans) was not overwhelming, and the gradistic resemblances In 1871, Charles Darwin published the fi rst serious, among extant great apes are undeniable. I think comprehensive and well-informed analysis of human it is fair to say that Darwin and Huxley were not evolutionary history. In this work, “Th e Descent vindicated until genetic technology was able to es- of Man, and Selection in Relation to Sex”, Darwin tablish with little doubt that chimpanzees are more compares the morphology of extant great apes to closely related to humans than they are to gorillas, humans, and he concludes that among other things and that the group of African apes and humans as humans and African apes are more closely related a whole is more closely related to each other than to one another than either are to orangutans. Here any of them are to orangutans. he was drawing heavily on the work of Th omas During this time, researchers were trying to inte- Henry Huxley and his most important publication, grate fossil discoveries with our understanding of ape “Evidence as to Man’s Place in Nature” (Huxley and human evolution. Darwin felt it most likely that 1863). While today we recognize the phyletic link African apes and humans evolved in Africa, stating between African apes and humans, based both on the following: “In each great region of the world morphological and molecular evidence, it is often the living mammals are closely related to the extinct forgotten that for much of the 20th century Dar- species of the same region. It is therefore probable win and Huxley’s conclusions were rejected, and that Africa was formerly inhabited by extinct apes the great apes were routinely linked together, with closely allied to the gorilla and chimpanzee; and as humans set apart. In fairness to historically strong these two species are now man’s nearest allies, it is advocates of the Pongidae (great apes), such as somewhat more probable that our early progeni- Adolph Schultz (1936, 1950), the morphological tors lived on the African continent than elsewhere.” evidence for a hominine clade (African apes and (Darwin 1871: 199).

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However, Darwin knew of a discovery in France from these three most important locations, along of a fossil with close similarities to living great apes. with isolated discoveries from Turkey and Bulgaria, Here is what he had to say about that fossil on the to try to make some sense of the fossil evidence of very next line: “But it is useless to speculate on this hominids in the Miocene of Europe (see below for subject, for an ape nearly as large as a man, namely terminology used in this paper). the Dryopithecus of Lartet, which was closely al- lied to the anthropomorphous Hylobates, existed ABBREVIATIONS in Europe during the upper Miocene period; and Institutions since so remote a period the earth has certainly AU Ankara University; undergone many great revolutions, and there has AUT Aristotle University of Th essaloniki; GMH Geological Museum of Hungary, Budapest; been ample time for migration on the largest scale.” IPS Institut Paleontologic, Sabadell (Institut (Darwin 1871: 199). Català de Paleontologia); Lartet himself spoke of the similarities between NMB Naturhistorisches Museum Basel. Dryopithecus Lartet, 1856 and African apes, and these observations were repeated by later research- Localities ers commenting on newer discoveries in France CO Çorakyerler collection (in AU); and Germany (Lartet 1856; Gaudry 1890; Branco RUD Rudabánya primate collection (in GMH); XIR Xirochori collection (in AUT). 1898; Harlé 1898; Schlosser 1901; Abel 1902). However, following impressive discoveries fi rst in Asia and then in Africa, attention shifted away EUROPEAN HOMININE TAXONOMY from Europe. “Th e Dryopithecus of Lartet” was eventually lumped in with most other fossil apes, Before reviewing the fossil record of European which were distinguished from what were then hominines it is necessary to explain the taxonomic taken to be the putative ancestors of humans, the usage adopted here. With regard to the sample ramapi thecines (Simons & Pilbeam 1965). At- from Greece, I recognize a genus level distinction tention was turned away from Europe until the between Ouranopithecus Bonis & Melentis, 1977 and early 1970’s, when discoveries from Greece and Graecopithecus von Koenigswald, 1972 (Begun 2002, Hungary, and an emerging understanding of the 2007a; Koufos & Bonis 2005). In Graecopithecus evolutionary position of the Siwalik fossil apes, the M2 is close in size to male Ouranopithecus, but were leading to a renewal of interest in Europe (see the mandible is the size of a female Ouranopithecus. Begun [2002] for a more detailed history). In 1974, In fact, the breadth of the M2 is greater than the a new species of Dryopithecus, D. macedoniensis mandibular breadth at that level. Th is suggests an (Bonis, Bouvrain, Geraads & Melentis, 1974), important diff erence in relative tooth size between was recognized on the basis of fossil specimens the two taxa. In addition, the symphysis in Graeco- from northern Greece. In the same year Kretzoi pithecus is more vertical in orientation, and the M1 (1975) published an account of a genus of fossil is smaller relative to the M2 (Begun 2002). While ape, Rudapithecus Kretzoi,1969, from Hungary. they are often lumped together by virtue of the fact In both cases, but based on very diff erent lines of that both appear to have thickly enameled teeth and evidence, Europe was being repositioned as an area both are found in Greece, it is worth noting that of great importance in interpretations of ape and the shortest distance between an Ouranopithecus human evolutionary history. locality (Nikiti) and Pyrgos Vassilissis (Graeco- In the intervening 30 years or so, many new pithecus) is about 250 km as the crow fl ies today. In discoveries have been made in both Greece and the late Miocene the Th ermaikos Gulf and Aegean Hungary, as well as in Spain, and these have shaped Sea intervened between the Chalkidiki Peninsula the debate on the relevance of Europe in the evolu- and mainland Greece as it does today, so the land tionary history of the African apes and humans. For distance between the two localities is even greater. the remainder of this paper I will review the data In addition, Nikiti, the youngest Ouranopithecus

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locality, is estimated to be about 9 Ma (Koufos diffi cult to compare to the Can Llobateres and Ruda- 2003), and Pygros Vassilissis, though diffi cult to bánya samples because it is distorted. It is unlikely date, is likely to be MN 12, or 6-8 Ma, and the that the face of Pierolapithecus resembled Afropithecus ecology of Greece during these diff erent time periods Leakey & Leakey, 1986, as suggested by Moyà- was quite diff erent (Solounias 1981; Bernor 1983; Solà et al. (2004), after the distortion is corrected Bonis et al. 1994; Bernor et al. 1996; Mein 1999; (Begun & Ward 2005; Begun 2007a). Th e teeth are Solounias et al. 1999; Steininger 1999; Agustí et al. quite similar to MN 9 dryopithecins but, interest- 2003; Begun & Nargolwalla 2004; Begun 2005; ingly, the I1 and M3 most closely resembles those Merceron et al. 2005a; Agustí 2007; Strömberg et attributed to Dryopithecus fontani from La Grive al. 2007). Th is taxonomic interpretation is consist- (Begun & Ward 2005) (Fig. 1). In addition, the ent with Bonis & Melentis (1984). canines are relatively large, as is the case for the lower A recent review of the taxa usually attributed to canines of Dryopithecus fontani from St-Gaudens. Like Dryopithecus has led to a revised taxonomy (Begun MN 7/8 Dryopithecus, Pierolapithecus has partial molar et al. 2008). With the discovery of a number of cingula, short premolars and a smaller M1 relative partial crania, diversity among the dryopithecins to M2. Th e lower dentition of Dryopithecus from has become clearer. Th e large sample from the Vallès France also has relatively lower premolar talonids, a Penedès expanded dramatically with the discovery primitive character, compared to MN 9 European of a partial skeleton from Can Llobateres (Begun & hominines. Two previously known isolated lower Moyà-Solà 1992; Moyà-Solà et al. 1992; Moyà- molars also from Can Vila share attributes with Solà & Köhler 1993, 1995, 1996), a second partial French Dryopithecus, including partial buccal cingula skeleton from Hostalets de Pierola (Moyà-Solà et al. and a well-developed tuberculum sextum on the M3 2004), a palate from Can Mata (Moyà-Solà et al. (Fig. 1B) (Begun & Moyà-Solà 1990; Begun 2002). 2009a) and a partial face from Can Mata (Moyà-Solà In summary, the samples from Can Vila and France et al. 2009b). When compared to the postcranial are the same age and have many attributes in common, sample and the three partial crania now known and they are generally more primitive than MN 9 from Rudabánya, there are a suffi cient number of hominines. I therefore recognize Pierolapithecus as a diff erences to warrant the recognition of separate junior subjective synonym of Dryopithecus (Begun et genera for each sample (Begun et al. 2008). al. 2008). Th is interpretation is further supported by Pierolapithecus catalaunicus Moyà-Solà, Köhler, the recent discovery of a Dryopithecus fontani palate, ALba, Casanovas-Villar & Galindo, 2004, from from the nearby MN 7/8 locality of Can Mata, and a Barranc de Can Vila 1 in Catalonia, Spain, is known partial face attributed to the new genus Anoiapithecus from a partial skeleton including much of the face Moyà-Solà, Alba, Almécija, Casanovas-Vilar, Köh- and portions of the postcranial skeleton (Moyà-Solà ler, Esteban-Trivigno, Robles, Galindo & Fortuny, et al. 2004). Th e locality is dated to MN 7/8, and is 2009, also from Can Mata, which are both very therefore older than Can Llobateres and Rudabánya, similar dentally to Pierolapithecus (Moyà-Solà et al. both of which are MN 9 or early Vallesian (Begun 2009a, b). Th ese new specimens are all attributed 2002). Barranc de Can Vila 1 is the same age as Dryo- to Dryopithecus (Begun et al. in press). pithecus fontani Lartet, 1856 from St-Gaudens and As noted above, MN 9 dryopithecins are derived La Grive (France) and from Can Vila and Can Mata relative to Dryopithecus as defi ned here. Th e best (Spain). Pierolapithecus Moyà-Solà, Köhler, ALba, samples of MN 9 dryopithecins are from Can Llo- Casanovas-Villar & Galindo, 2004 is distinct from bateres and Rudabánya. Here I recognize separate and more primitive than the Can Llobateres and/ genera for each of these two samples, Hispanopithecus or Rudabánya samples in that the lumbar vertebrae Villalta & Crusafont, 1944 at Can Llobateres and have somewhat more anteriorly positioned transverse Rudapithecus at Rudabánya, as originally suggested processes (not known at Rudabánya) and the proximal by Kretzoi (1969) and Villalta & Crusafont (1944). hand phalanges are shorter, less curved with proximal Th e best preserved and most informative specimens articular surfaces oriented more dorsally. Th e face is from Can Llobateres are a face and partial skeleton,

792 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

A B C D

A-D

AEF

E, F

FIG. 1. — Comparisons between Pierolapithecus Moyà-Solà, Köhler, Alba, Casanovas-Villar & Galindo, 2004 and D. fontani Lartet, 1 1 3 3 1856: A, Pierolapithecus I ; B, La Grive I , NMB g. a. 9; C, Pierolapithecus M , NMB; D, la Grive M ; E, left M3 from Can Vila; F, left M3 from D. fontani. Images of the Pierolapithecus specimens are modifi ed from Moyà-Solà et al. (2004). Scale bars: 1 cm.

IPS 18000 and IPS 18800 (Moyà-Solà & Köhler surface of the zygomatic process of the frontal (the 1993, 1995; Begun 1994; Almécija et al. 2007). superolateral corner of the orbit) in Hispanopithecus Th ese fossils were originally attributed to the same also diff ers from the three Rudapithecus specimens in individual. In the cranial specimen the frontal being more anteriorly oriented. In Hispanopithecus squama of Hispanopithecus is strongly biconcave the body of the zygomatic bone is fl at and faces more transversely and anteroposteriorly, while in Rudapi- anteriorly than in Rudapithecus, in which all three thecus it is smoothly bi-convex. In Hispanopithecus specimens have more convex zygoma facing more there is a groove separating the supraorbital ridge laterally (Begun 1994). Although highly variable in from the supraorbital torus. Th e anterior temporal extant hominoids, the position, size and number of lines in Hispanopithecus are very strongly developed the zygomaticofacial foramina also diff er between and raised above the cranial surface immediately the two taxa, with those in Hispanopithecus being anterior and medial to it. IPS 18000 is a male, as relatively large, more numerous, and higher on the is RUD 44. Th e latter is larger than IPS 18000 but zygomatic frontal process (Begun 1994; Moyà- with less strongly developed temporal ridges. Th e Solà & Köhler 1995).

GEODIVERSITAS • 2009 • 31 (4) 793 Begun D. R.

TABLE 1. — Principle taxa discussed in this paper and their most important diagnostic craniodental characters.

Dryopithecus Short, vertical premaxilla with evidence of a subnasal step (associated with maxillary over- Lartet, 1856 lap), biconvex premaxilla, modest supraorbital tori and supratoral sulcus, broad interorbital space, robust lateral orbital margins, square orbits, subvertical nasal aperture margins, high zygomaticoalveolar crest, relatively broad canines, short premolars and small M1, low lower premolar talonids, partial molar cingula, thin occlusal enamel, tall crowned postcanines, M3 tuberculum sextum, somewhat robust mandibles, mesio-distally short, tall crowned I1 Hispanopithecus Short, vertical premaxilla with evidence of a subnasal step (associated with maxillary overlap), Villalta & Crusafont, 1944 biconvex premaxilla, modest supraorbital tori and supratoral sulcus, strongly developed anterior temporal lines, biconcave vertical frontal squama, reduced subarcuate fossa, ro- bust lateral orbital margins, square orbits, broad interorbital space, ethmoidal frontal sinus, subvertical nasal aperture margins, high zygomaticoalveolar crest, more anteriorly oriented zygoma, thin enamel, mesio-distally short, tall crowned I1, peg-shaped I2 Rudapithecus Short, vertical premaxilla with some maxillary overlap, relatively narrow, posteriorly divergent Kretzoi, 1969 palate, biconcave premaxilla, modest supraorbital tori and supratoral sulcus, vertical frontal squama, elongated, klinorhynch crania, inion high on the skull, reduced subarcuate fossa, fused tympanic and articular temporal, large brain, robust lateral orbital margins, square orbits, broad interorbital space, ethmoidal frontal sinus, subvertical nasal aperture margins, high zygomaticoalveolar crest, convex and more laterally facing zygoma, more compressed canines and elongated postcanines, strongly tapered M3, more peripheral cusp positions, mesio-distally short, tall crowned I1, peg-shaped I2 Ouranopithecus Short, vertical premaxilla with some maxillary overlap, modest supraorbital tori and supra- Bonis & Melentis, 1977 toral sulcus, vertical frontal squama, robust lateral orbital margins, subvertical nasal aperture margins, low zygomaticoalveolar crest, strongly heteromorphic upper incisors, reduced ca- nine size and premolar sectoriality, hyperthick occlusal enamel, tall crowned and megadont postcanines, broad rounded cusps, robust to very robust mandibles Çorakyerler hominine Very short premaxilla, upper canines nearly aligned with incisors transversely, homomorphic upper premolars, extremely large postcanine, teeth, narrow palate, thick, diamondshaped upper canines cervix reduced in size relative to the molars, thin palatine process, low crowned I1, peg-shaped I2

Th e palate of Rudapithecus is narrower than that elongated, strongly tapered, and are smaller than of Hispanopithecus, and the zygomaticoalveolar the M2s in Rudapithecus. Males of Rudapithecus crests are thicker anteroposteriorly. Th e mandible diff er from males of Hispanopithecus in having large of Rudapithecus is generally more robust and oval in lower premolars, strongly triangular (beaked) P3, cross section. Th e only identifi ably male mandible of large P3 fovea of equal height with buccal crista Hispanopithecus (IPS 1764) has a triangular shaped of equal length, and broad, wrinkled lower molar cross section between P4-M1. Dentally, the upper basins with marginalized cusps (Begun & Kordos incisor crowns are narrow compared to H. laietanus 1993; Begun 1994). Villalta & Crusafont, 1944, with concave lingual Postcranially, Rudapithecus diff ers from Hispano- surfaces and single central pillars. Hispanopithecus pithecus in having much less robust manual proximal laietanus I1s have complicated cresting on their phalanges with a more proximally oriented proximal lingual surfaces, and H. crusafonti Begun, 1992 articular surface and broader trochlea. Th e metacarpal I1s are extremely narrow with very prominent me- is also less robust transversely. Th e femoral neck in sial, distal and central labial pillars (Begun 1992a, Rudapithecus is larger superoinferiorly relative to head 1994). In Rudapithecus the canines are smaller diameter compared to Hispanopithecus (MacLatchy and more compressed buccolingually and the up- et al. 2001; Köhler et al. 2002; and pers. obs.). Table per postcanine teeth tend to be more elongated 1 lists the most important European hominine taxa relative to breadth. Th e upper and lower M3s are and their main diagnostic characters.

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Th e classifi cation of European hominines fol- Genus Ouranopithecus Bonis & Melentis, 1977 lowed here is as follows: Ouranopithecus macedoniensis Bonis & Melentis, 1977 Subfamily HOMININAE Gray, 1825 Genus Graecopithecus von Koenigswald, 1972 Tribe DRYOPITHECINI Gregory & Hellman, 1939 Graecopithecus freybergi von Koenigswald, Subtribe DRYOPITHECINA 1972 Gregory & Hellman, 1939 Gen. et sp. nov. (Çorakyerler) (see below)

DIAGNOSIS. — Th e Dryopithecina is diagnosed as follows: MACEDONIA, GREECE medium to large bodied hominines (20-45 kg) with thinly As noted above, in 1974 de Bonis and colleagues enameled teeth, robust and generally mesiodistally short upper incisors, tall crowned lower incisors, compressed named a new species of Dryopithecus in Macedonia, canines, large, elongated premolars, M1 close in size to from the locality of Ravin de la Pluie. Although M2, peripheralized molar cusps, seven day cross striation from Europe, this fossil is strikingly diff erent from periodicity, short premaxilla, stepped subnasal fossa, short, other European fossil apes known at the time, par- large caliber incisive canal, larger incisive foramen and ticularly in the robust morphology of the mandible fossa, robust palatine process, broad, fl at inferior margin and the large and thickly enameled postcanine of the nasal aperture, high zygomatic root, large maxil- lary sinus, large ethmoid sinus continuous with a well- teeth (Bonis & Melentis 1976, 1977a, b, 1978, developed frontal sinus, thick interorbital space, weakly 1980; Begun & Kordos 1997). Th e canines are developed supraorbital tori, prominent anterior temporal also unusually small, although the type specimen lines, elongated brain case, inion slightly above glabella, is a female, and over the years, the relative canine large brain, fused articular and tympanic temporal, deep size in this taxon even in males has proven to be temporal fossa, prominent entoglenoid process, robust a diffi cult issue to resolve (Bonis & Koufos 2001; mandible, large ramus, posteriorly diverging tooth rows, Kelley 2001). More discoveries of the same taxon elongated, tapered M . 3 at Ravin de la Pluie as well as two other localities in Macedonia, Xirochori and Nikiti, have made clear Genus Dryopithecus Lartet, 1856 the diff erences from other European and African Dryopithecus fontani Lartet, 1856 Miocene fossil apes from the same time period and Dryopithecus catalaunicus before as well. Moyà-Solà & Köhler, 2004 De Bonis and Melentis attributed the new taxon Dryopithecus carinthiacus Mottl, 1957 from Greece to Dryopithecus, but they later re- Genus Rudapithecus Kretzoi, 1969 vised their taxonomic conclusions in light of the Rudapithecus hungaricus Kretzoi, 1969 similarities they saw with Sivapithecus Pilgrim, Genus Hispanopithecus 1910, Gigantopithecus von Koenigswald, 1935 and Villalta & Crusafont, 1944 australopithecines (Bonis & Melentis 1977b). Hispanopithecus crusafonti Begun, 1992 Th ese include the large, robust jaws and thickly Hispanopithecus laietanus enameled teeth that distinguish Ouranopithecus Villalta & Crusafont, 1944 from Dryopithecus, but also details of canine and premolar morphology and the structure of the palate Subtribe OURANOPITHECINA new subtribe (Bonis & Melentis 1977b, 1978; Bonis 1983). Ad- ditional preparation of the palate of Ouranopithecus DIAGNOSIS. — Th e Ouranopithecina is diagnosed as would lead de Bonis and Melentis to interpret it as follows: Large bodied hominines (45+? kg) with thickly a direct link between Miocene apes and australo- enameled teeth, low, rounded cusps, broad, shallow oc- pithecines, sharing synapomorphies with the tribe clusal basins, enlarged M3’s, anterior teeth and dental proportions as in Dryopithecina, except small male Hominini Grey, 1825, in which they include Homo canine crown dimensions, premaxilla and maxilla as Linnaeus, 1758 and Australopithecus Dart, 1925 in Dryopithecina except low, thick zygomaticoalveolar (Bonis 1983; Bonis & Melentis 1984). In eff ect, crest, periorbital region as in Dryopithecina. they are attributing Ouranopithecus to the Hominini,

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though they do not say this directly. Bonis (1983) in the relative size of the canine, changes in canine- also attributes Dryopithecus and Hispanopithecus premolar relationships, postcanine megadontia and to the Dryopithecini Gregory & Hellman, 1939, increases in gnathic robusticity and enamel thick- in which he includes Pan Oken, 1816 and Gorilla ness characterize several lineages of fossil hominids Geoff roy-Saint-Hilaire, 1852, which is very close (Sivapithecus, Ankarapithecus Ozansoy, 1965, Gripho- to the phylogeny followed here. pithecus Abel, 1902, Gigantopithecus, Paranthropus Begun & Kordos (1997) make the case for a Broom, 1939, Paraustralopithecus Arambourg & slightly diff erent interpretation of Ouranopithecus Coppens, 1968). Th ese features leave an overwhelm- and Dryopithecus, but one that still places them ing impression on facial and dental morphology, fi rmly among the hominines (African apes and though they are all closely interrelated and essen- humans in both Bonis [1983] and Begun [1992b]). tially constitute a single trait complex that results Whether the African apes and humans have separate from selection for more powerful mastication. As origins in Africa during the early/middle Miocene noted, the history of interpretation is quite revealing (Bonis & Melentis 1977a, b; Bonis 1983; Bonis & in this regard. At one time or another, all thickly Koufos 1993) or a common origin in the middle enameled middle and late Miocene hominoids Miocene of Europe (Bonis 1987; Bonis & Koufos were grouped into the same genus (Sivapithecus) 1994; Begun & Kordos 1997; Begun 2000, 2002, and linked phyletically to one another and to other 2003, 2005, 2007a; Begun & Nargolwalla 2004), similar taxa such as Gigantopithecus (Andrews & in both scenarios Europe is central to hominine Tobien 1977; Bonis & Melentis 1977a, b, 1978; origins as the place in which they evolved and pre- Andrews & Tekkaya 1980; Andrews 1983, 1985). sumably acquired their diagnostic characteristics However, when all available characters are consid- before returning to Africa. ered, Ouranopithecus consistently falls out among Louis de Bonis and George Koufos have made the hominines as the sister clade of the African ape a strong case for the phyletic link between Our- and human clade (Begun et al. 1997; Begun 2001, anopithecus and Australopithecus (Bonis & Koufos 2002, 2005, 2007a) (Fig. 2B). 1993, 1994, 1997, 2001, 2004; Koufos 1993, Most signifi cantly, Ouranopithecus lacks several 1995, 2007; Bonis et al. 1998; Koufos & Bonis characters shared between chimpanzees and early 2004). Important characters interpreted as synapo- fossil humans such as Australopithecus. Th ese include morphies of an Ouranopithecus-Australopithecus the structure of the premaxilla, which is more similar clade include a relatively vertical face, narrow and to that of Gorilla and Rudapithecus than Australo- convex mandibular condyle, distal accessory cusps pithecus and Pan (Bonis & Melentis 1987; Bonis & on the upper and lower M3, rounded P3 lacking Koufos 1993; Begun 2001, 2002; Koufos 2007). a buccal honing facet, relatively small male upper Ouranopithecus shares the primitive condition for canine more rounded in cross section at the cervix, hominines, a relatively short and vertical premaxilla, small deciduous canines, and molarized deciduous a strongly stepped subnasal fossa and a large incisive premolars (Koufos 2007). Th is hypothesis is rep- fossa and canal. Th e nasal border of the premaxilla resented in Figure 2A. overlaps minimally with the palatine process of the Begun (2007b) and Begun & Kordos (1997) maxilla. In Pan and Australopithecus the premaxilla argue that all of the similarities between Ourano- is longer and more horizontally oriented, and its pithecus and Australopithecus are homoplasies because, nasal border overlaps the maxillary palatine process 1), this is consistent with the most parsimonious to a considerably greater degree, which produces a cladogram (Begun et al. 1997; Begun 2001), and reduced subnasal step, a smaller incisive fossa and 2), they are all related to a single functional com- a longer, narrower incisive canal (Ward & Kimbel plex, powerful mastication. Interestingly, Bonis & 1983; Begun et al. 1997; Begun 2001, 2002). It Melentis (1977a, 1978) suggested that Ourano- could be argued that these premaxillary features pithecus might be closely related to Gigantopithecus also constitute a single character (Schwartz 1997). based on many of the same characteristics. Reduction However, this complex actually cross cuts functional

796 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

A Proconsul Griphopithecus alpani Griphopithecus darwini Kenyapithecus kizili Pongo Hominini Ouranopithecus macedoniensis New genus from Turkey Graecopithecus freybergi Pan Gorilla Dryopithecus fontani Dryopithecus catalaunicus Rudapithecus hungaricus Neopithecus brancoi Hispanopithecus crusafonti Hispanopithecus laietanus

B Proconsul Griphopithecus alpani Griphopithecus darwini Kenyapithecus kizili Pongo Hominini Pan Gorilla ? New genus from Turkey Ouranopithecus macedoniensis Graecopithecus freybergi Hispanopithecus crusafonti Hispanopithecus laietanus Rudapithecus hungaricus Neopithecus brancoi Dryopithecus fontani Dryopithecus catalaunicus

FIG. 2. — Cladograms depicting alternative hypotheses discussed in the text. Modifi ed from Begun et al. (1997) and Begun (2001, 2002, 2007). Griphopithecus alpani Tekkaya, 1974 and Kenyapithecus kizili Kelley, Andrews & Alpagut, 2008 are thickly enameled middle Miocene hominoids from Paşalar (Turkey). Griphopithecus darwini Abel, 1902 is the type species, from DevínskᢠNová Ves (Slovakia). Neopithecus brancoi Schlosser, 1901 is an isolated M3 that is most similar to Rudapithecus Kretzoi, 1969 but with insuffi cient anatomy preserved to justify synonomy. Other taxa are discussed in the text. In A, Ouranopithecus is a hominin; in B, it is a dryopithecin.

GEODIVERSITAS • 2009 • 31 (4) 797 Begun D. R.

and phylogenetic boundaries. Th e very similar In both cases the nomen Rudapithecus hungaricus morphology of the Pan and Australopithecus lower was used, but without a diagnosis or type specimen face exists despite dramatic diff erences in functional designated, and with no taxonomically useful char- morphology and probably diet. In addition, there acters described. In 1969 a publication appeared is evidence of de-coupling of premaxillary length/ with a short diagnosis (Kretzoi 1969). Th us the fi rst orientation and incisive fossa/canal morphology available nomen for the sample from Rudabánya in in Ankarapithecus, which shares the former with my view is Rudapithecus hungaricus Kretzoi, 1969 Sivapithecus and the latter with hominines (Be- (Kordos & Begun 2001). In Kretzoi (1975) a new gun & Güleç 1998). Ouranopithecus also lacks the taxon, Bodvapithecus altipalatus Kretzoi, 1975 is spatulate upper lateral incisor of Pan and all Ho- named. Kretzoi interpreted Bodvapithecus Kretzoi, minini, and in this way also shares the primitive 1975 to be related to Sivapithecus, and Rudapithecus morphotype with Gorilla, other dryopithecins and to Ramapithecus (Kretzoi 1975), and this hypothesis all other anthropoids (Begun et al. 1997). Begun was widely accepted (Pilbeam 1979; Szalay & Delson (2002) lists a number of additional characters shared 1979; Wolpoff 1980). Kay & Simons (1983) were between Pan and Hominini that are not found in the fi rst, to my knowledge, to recognize that the Ouranopithecus, and would have to have evolved smaller of the two hominid taxa from Rudabánya, independently if Ouranopithecus were more closely Rudapithecus, had close affi nities to Dryopithecus. In related to hominins than Pan. Th ese include lower subsequent years most researchers have interpreted crowned, fl ared molars, less robust lateral orbital Rudapithecus and Bodvapithecus to be females and pillars, more strongly developed supraorbital tori males respectively of the same taxon, Dryopithecus and sulci, a more horizontal frontal squama, and brancoi Schlosser, 1901 (Begun & Kordos 1993). better developed supraorbital and glabellar pneu- As noted earlier, here this sample is now returned matization. Unlike the characters that are shared to Rudapithecus. by Ouranopithecus and Australopithecus that are all Th e Rudabánya hominid sample includes three seemingly related to a single functional constraint partial crania, two of which preserve signifi cant (heavy mastication), the characters shared by Pan and portions of the brain case. One of these specimens, hominins that are not found in Ouranopithecus are RUD 200, preserves the connection between the not obviously related to a single functional complex, brain case and face, and provides our only glimpse and cannot easily be explained as a consequence of the architecture of the cranium of a European of a single, simple and common adaptive response. hominid. Th is specimen is associated with a man- For these reasons, I consider Ouranopithecus to be dible, RUD 212, making it the only well preserved in the outgroup of the extant hominines (Fig. 2B). skull (cranium and mandible) of a Eurasian hominid In the phylogenetic analysis on which Figure 2B (a facial skeleton and mandible is known for Siva- is based (Begun et al. 1997; Begun 2001), it is pithecus, but no neurocranium, and a crushed and equally parsimonious to place Ouranopithecus as distorted skull of Oreopithecus is also known). the sister clade to the African apes and humans as Th e craniodental sample of Rudapithecus is criti- it is to link it with dryopithecins as a group that cal in interpretations of hominine relations. Begun is the sister clade to African apes and humans, as (2005) and Kordos & Begun (2001) list 16 charac- represented in Figure 2B. ters of the dentition and cranium shared between Rudapithecus and extant great apes, and 15 ad- RUDABÁNYA, HUNGARY ditional characters shared exclusively with extant In 1967 an anonymous newspaper announcement hominines. In contrast to the characters shared was made describing the discovery of an ape jaw from between Ouranopithecus and Australopithecus, these deposits surrounding the large open pit ore mine 31 characters come from throughout the cranium at Rudabánya, in northern central Hungary. In the and dentition. Th ere is no obvious functional inter- same year the discovery was covered in a popular relationship among such hominine characters as a bi- science magazine article (Tasnádi Kubacska 1967). convex premaxilla, supraorbital torus, frontal sinus,

798 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

fused articular and tympanic temporal, elongated resembles those of Hispanopithecus in being strongly neurocranium and klinorhynchy. Where known, constricted dorsally, with large collateral ligament these characters are for the most part also shared pits. A talus has a typical hominid morphology with with Ouranopithecus. One signifi cant exception is a broad, shallow body and an elongated neck, most the position of the root of the zygomatic process reminiscent of Pongo. Th e phalanges are typical of of the maxilla, which is low in Ouranopithecus and suspensory hominoids and are long and strongly primitive hominoids such as Proconsul Hopwood, curved, with well-developed fl exor sheath ridges 1933, and high in Rudapithecus and most other and a proximally oriented proximal articular surface hominids (Begun & Kordos 1997). However, this (Begun 1993; Deane & Begun 2008). is a good example of the exception that proves the rule. Th e low position of the root of the zygo- VALLÈS PENEDÈS, SPAIN matic process in Ouranopithecus is not only shared In 1944 Villalta & Crusafont described a new genus with Proconsul and Hylobates, but also with robust of hominoid from the Vallès Penedès of Catalonia, australo pithecines (Begun & Kordos 1997b; Begun northeastern Spain. Th e type specimen of Hispano- 2007b). In the case of Ouranopithecus and Paran- pithecus laietanus comes from La Tarumba, but the thropus, the morphology of the zygomatic has been vast majority of the sample attributed to this taxon related to elevated levels of stress generated by their comes from Can Llobateres (Begun & Moyà-Solà greatly enlarged masticatory apparatus (Rak 1983; 1990; Golpe Posse 1993). A number of other taxa Begun & Kordos 1997b; Begun 2007b). While have been recognized based on the Can Llobateres low on the alveolar process, the zygomatic bone sample (reviewed in Simons & Pilbeam [1965]), in robust australopithecines and Ouranopithecus is but only Hispanopithecus is recognized today. very diff erent in morphology from the same bone As noted earlier, a major advance in our under- in Proconsul and Hylobates. I would interpret the standing of European hominine phylogeny and apparently primitive position of the zygomatic adaptation occurred with the discovery and analysis root in Ouranopithecus as a clear homoplasy, given of a craniofacial specimen and partial skeleton of the known phylogeny of extant hominoids, the Hispanopithecus from Can Llobateres (Begun & inferred phylogeny of fossil apes, and the probable Moyá-Solá 1992; Moyà-Solà et al. 1992; Moyà- functional integration of this character within the Solà & Köhler 1993, 1995, 1996; Begun 1994; heavy mastication morpho-functional complex Köhler et al. 2002). Details of the diff erences be- (Begun 2007b). tween Hispanopithecus and Rudapithecus are listed Th e postcrania of Rudapithecus also reveal a suite above. In general, Hispanopithecus is smaller than of great ape affi nities. Th e distal end of a humerus Rudapithecus, though they overlap in size. Males of and the proximal end of an ulna show the typical Hispanopithecus are intermediate in size between suite of great ape characters (large trochlea and males and females of Rudapithecus. Th e vertebral capitulum well diff erentiated from each other by column is known only in Hispanopithecus. Th e a deep zona conoidea, well-developed coranoid, lumbar vertebrae show the important hominid radial and olecranon fossae, large, medial oriented character of a dorsal position of the transverse proc- medial epicondyle, strong ulnar trochlear keel, large ess, a feature that is associated with the short, stiff radially oriented radial notch, robust ulnar shaft lower backs and orthogrady of great apes (Ward [Morbeck 1983; Begun 1992c]). Several carpal bones 1993, 1997, 2007; MacLatchy et al. 2000). Other are known from Rudabánya. Th e scaphoid most great ape characters of the postcranium of Hispano- closely resembles Pongo Lacépède, 1799, and like pithecus include a large lunate and robust hamate, Pongo and nearly all non-hominine primates, it is the latter with a well-developed hamulus, and large, not fused to the os centrale (Kivell & Begun 2009). long and curved manual proximal phalanges with Th e capitate is also Pongo-like but retains primitive well-developed fl exor sheath ridges. Although the characters found in some cercopithecoids (Kivell & important great ape character of a reduced ulnar Begun 2009). Th e distal end of a metacarpal closely styloid process, resulting in the absence of ulnar-

GEODIVERSITAS • 2009 • 31 (4) 799 Begun D. R.

triquetral contact, is not known for either Hispano- Th e key is the size and position of the sinus. In pithecus or Rudapithecus, the absence of a facet for dryopithecins, African apes, and humans, the sinus the ulnar styloid on the triquetrum of Dryopithecus occupies most of the interorbital space from below catalaunicus strongly suggests that the same was nasion to glabella, and has a variable pneumatization true for the Vallesian taxa. into the frontal squama. Th is has been interpreted Moyà-Solà and colleagues have concluded that as a true ethmoidal frontal sinus, given the large Hispanopithecus is a member of the Sivapithecus involvement of the interorbital space and hence and Pongo clade (Moyà-Solà & Köhler 1993, 1995, the ethmoidal air cells (Begun 1994, 2007a). Siva- 1996; Köhler et al. 2001). Th ey base this conclu- pithecus and Pongo lack expansion of the ethmoidal sion on a small number of characters of the face, air cells, which invade neither the interorbital region including the size and position of the zygomatico- nor the frontal squama. On the other hand, there facial foramina, the shape and orientation of the are many taxa in which the frontal is pneumatized zygomatic bone, the position of the frontozygomatic from behind, by the sphenoidal air sinus (Cave & suture, the size of the frontal sinus and the presence Haines 1940). Th ere are diff ering interpretations of supraorbital costae. of the signifi cance of various paranasal sinus con- Th e number and size of the zygomaticofacial fi gurations (Begun 1994; Rossie et al. 2002; Rossie foramina are highly variable in extant anthropoids 2005), but researchers agree that the loss of the (Msuya & Harrison 1996). Pongo does tend to have ethmoidal and frontal sinus expansion in Pongo a higher number of foramina than other great apes, and Sivapithecus is an important synapomorphy of but there is signifi cant overlap. In addition, it is dif- that clade (Ward & Brown 1986). Hispanopithecus fi cult to say exactly how many foramina are present clearly does not share this synapomorphy with Asian in IPS 18000 given preservation in the area (Fig. 3). great apes (Fig. 3). As Figure 3 shows, the position and orientation of Th e frontozygomatic suture in IPS 18000 is said the zygomatic bone is unclear as it is not attached to to be in a depressed position relative to the superior either the maxilla or the frontal bone. Th e small part orbital margin, which is a tendency seen in Pongo of the body of the zygomatic bone that is preserved (Moyà-Solà & Köhler 1995; Köhler et al. 2001). inferolateral to the orbital margin is fl attened, and In Moyà-Solà & Köhler (1995: 123, fi g. 17) it is resembles Pongo in this regard, but so little of the clear that there is very substantial overlap between bone is preserved that it is not possible to describe Pan and Pongo, with Hispanopithecus values falling in it reliably as overall Pongo-like. In addition, in the the range of overlapping values. Furthermore, they case of both the zygomaticofacial foramina and the use internal biorbital breadth to standardize for body orientation of the zygomatic bone, three specimens mass, despite the fact that Pongo and Sivapithecus of Rudapithecus lack the Pongo-like morphology that have relatively smaller biorbital breadths given their has been suggested for IPS 18000. RUD 44, 77 narrow interorbital regions and their tall, narrow and 200 all preserve more of the zygomatic bone, orbits. Figure 3 shows a more likely position of and they have neither large and supernummary the zygomatic relative to the frontal in IPS 18000. zygomaticofacial foramina nor a fl at and anteriorly Insets b and c show views of the frontozygomatic facing zygomatic body. suture surfaces. On the zygomatic bone the surface Inset a in Figure 3 is a view of the partially pre- is nearly complete. On the frontal it is preserved served frontal sinus of IPS 18000. It is not reduced, but somewhat eroded. Th is corresponds to the as described in Köhler et al. (2001). In fact, it is description of the bones in Moyà-Solà & Köhler quite large, and occupies most of the interorbital (1995). When the mirror imaged frontal with its space and indeed it does invade the space between frontozygomatic suture surface is matched to the the endocranial and orbital plates. In dryopithecins right zygomatic with its suture surface, the posi- this is the typical pattern, which is only found in tion of the suture itself is clear. It is relatively high African apes and humans. It departs most mark- on the orbit as in most anthropoids, and lacks the edly from the pattern in Pongo and Sivapithecus. condition found in Sivapithecus and some Pongo.

800 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

A

B

C

D

FIG. 3. — Views of IPS 18000 from Can Llobateres: A, frontal view of the periorbital region with the right side reconstructed based on a mirror image of the better preserved left side; B, view from below of the interorbital space of IPS 18000 showing the extensive frontal sinus, outlined on the right side; C, lateral view of the frontal fragment showing the frontal’s joint surface of the frontozygomatic suture; D, view from superiorly and medially showing the zygomatic’s joint surface of the frontozygomatic suture. Scale bar: 1 cm.

Th e orbits are also squared and the interorbital space tori emanating from a mildly infl ated glabella, both large, unlike Sivapithecus and Pongo. running superolaterally. Superior to the glabella-tori Th e presence of supraorbital costae is also said to complex is a deep biconcave depression, which is unite Hispanopithecus with the Sivapithecus/Pongo unique to Hispanopithecus (although such a de- clade (Moyà-Solà & Köhler 1995). Figure 3 shows pression is suggested by the morphology of Xir-1 the disposition of ridges or costae in the midfrontal [Ouranopithecus], this is not clear due to damage). region. Supraorbital costae appear on Pongo crania, In addition to the supraorbital tori, there are su- and in Sivapithecus, and consist of ridges that rim perior orbital margins but they are not thickened the superior orbital margin and the upper part of and do not project anteriorly from the supraorbital the medial orbital margins. Th ey do not meet in surface as they do in Pongo and Sivapithecus. Th is the midline, nor do they reach glabella or attach to plus the fact that they do not rim the orbits as any eminence at glabella. In contrast, supraorbital described above means that they are unlikely to tori meet in the midline at glabella, and are usually be homologous to the supraorbital costae of Asian continuous with an eminence at glabella (Begun great apes. In the end there are no characters shared 1994). In Figure 3 highlights mark the path of two uniquely between Hispanopithecus and Asian great

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apes and a large number of characters shared be- size, lower crowned male canines, low crowned I1 tween dryopithecins and African apes (Begun et al. with a highly complicated labial surface morpho- 1997; Begun 2001). logy, extreme upper incisor heteromorphy, incisors nearly aligned with the canines (modifi ed from TURKEY Güleç et al. [2007]). In 2007 Güleç et al. published a new species of Th e Çorakyerler sample shares characters with Ourano pithecus, O. turkae, from Çorakyerler, Tur- Ouranopithecus related to a heavily masticated key. Th e Çorakyerler fossil assemblage is correlated diet, which is often associated with an adaptation to MN 11, or between 8.7 and 7.4 Ma (Güleç et to more open habitats than those of living great al. 2007). I had the opportunity to examine and apes. Indeed, both genera occur in Eurasia at a prepare the type specimen, a very large male palate. time of considerable decline in forest cover, drier As noted elsewhere (Begun et al. 2003; Güleç et al. climates and increased seasonality (Bernor 1983; 2007), the specimen resembles Ouranopithecus more Bonis et al. 1994; Bernor et al. 1996; Solounias closely than any other fossil ape. Th e specimen is et al. 1999; Agustí et al. 2003; Begun & Nargol- considerably larger than the largest Ouranopithecus walla 2004; Begun 2005; Merceron et al. 2005a; specimen, and in fact it fi ts comfortably on the Koufos et al. 2006; Agustí 2007; Strömberg et al. mandible of Indopithecus giganteus Pilgrim, 1915 2007). As noted earlier, many of these characters (often referred to as Gigantopithecus bilaspurensis occur in Pliocene hominins, but also in other fos- Simons & Chopra, 1969). Th ere are also important sil hominids with large jaws and thickly enameled diff erences from Ouranopithecus, which justify in teeth. Because the Çorakyerler sample has derived my view the re cognition of a new genus. characters shared with African apes and humans not Th e Çorakyerler maxilla (CO 205) is a large found in Ouranopithecus, it is considered diff erent presumed male palate with LI1-M3, RC-M2, pre- at the genus level. serving portions of the right palatine process to the Th e Çorakyerler specimens are great apes, with midline, a small fragment of the left palatine proc- affi nities to European and African taxa and not ess, most of the left alveolar process, and much of with Ankarapithecus or South or Southeast Asian the palatal surface of the right premaxilla. Th ere is taxa (Begun et al. 2003; Begun 2005; Güleç et al. some distortion along both tooth rows, but a good 2007). Th e sample shows its greatest similarities estimate of dental arcade shape is possible (Fig. 4). to gorillas, chimpanzees and Ouranopithecus, and Th e specimen preserves a portion of the right edge is intermediate in age between Ouranopithecus and of the nasal aperture along the canine root. Th e the earliest known African hominids (Brunet et left side preserves the base of the zygomatic proc- al. 2002; Vignaud et al. 2002; Güleç et al. 2007; ess and the inferior extension of the canine fossa Lebatard et al. 2008). Previous interpretations of (Fig. 4). Th e canine and M3 are fully erupted and Ouranopithecus had suggested this genus as a good lightly worn. candidate for Pliocene hominid ancestry based on Th e new genus from Turkey is distinguished derived dentognathic features shared with later Af- from other hominoids including Ouranopithecus rican Pliocene Australopithecus (see above). While macedoniensis, by the following dentognathic charac- the upper premolars of CO 205 and non-robust teristics: a short, vertical premaxilla and lower face: Australopithecus strongly resemble one another, narrow palate relative to postcanine size: broad, A. anamensis Leakey, Feibel, McDougall & Walker, higher zygomatic root: broad, diamond-shaped 1995 and A. afarensis Johanson, White & Cop- canine cross-section at the cervix: homomorphic pens, 1978 have more primitive postcanine teeth P3 and P4: oval and symmetrical P3 with pre- and (White 1977; Ward et al. 2001; Güleç et al. 2007). postparacrista of equal length: M3 larger than M2. In Furthermore, all late Miocene African hominids addition to the characters noted above, it is further (Orrorin Coppens, Senut, Pickford, Gommery, distinguished from Ouranopithecus in the follow- Mein & Cheboi, 2001, Ardipithecus White, As- ing characters: larger size, smaller relative canine faw & Suwa, 1994, and Sahelanthropus Brunet et

802 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

A

B

CD

FIG. 4. — Views of the Çorakyerler hominine: A, palatal; B, lateral; C, medial; D, frontal. Scale bar: 1cm. al., 2002) lack dentognathic specializations associ- including narrow palates, reduced premolar occlu- ated with heavily masticated diets (Haile-Selassie sal outline and cusp heteromorphy, peg-shaped I2, 2001; Senut et al. 2001; Brunet et al. 2002; Haile- short premaxilla and vertically implanted anterior Selassie et al. 2004; Güleç et al. 2007). Evidence teeth, and a thin maxillary palatine process. Some from functional morphology and known relations of these characters, such as the peg-shaped I2, are among fossil and living hominids strongly suggests primitive for the African ape and human clade, as that Ouranopithecus and the Çorakyerler hominine suggested on the basis of previous comparisons to evolved many or all of these dietary adaptations Dryopithecus and Ouranopithecus (Begun 1994, in parallel with later African hominids (Begun & 2001, 2002; Begun & Kordos 1997). Kordos 1997b; Begun 2007b). On the other hand, Th e presence of a fossil great ape in a relatively the features the Çorakyerler hominine shares with open habitat in the Turolian of Turkey will require a African apes and humans and not Ouranopithecus rethinking of ideas of Eurasian hominoid extinctions, may indicate a closer relationship to this larger clade previously attributed to environmental changes at (Fig. 2B). A number of characters are shared with this time (Bonis & Koufos 1999; Bonis et al. 1999; Gorilla, and occasionally found in other hominids, Solounias et al. 1999; Eronen & Rook 2004; Rook &

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Bernor 2004; Agustí 2007). Th e fauna associated resemble living chimpanzees in molar occlusal with the Çorakyerler hominoids indicates a relatively morpho logy, enamel thickness, gross and microwear, open habitat (Güleç et al. 2007). Th e large, thickly and shearing quotients (Begun 1994; Ungar 1996; enameled, low-cusped postcanine teeth are likely Begun & Kordos 1997b; Kay & Ungar 1997; Smith associated with a heavily masticated diet. However, et al. 2003). Th is has been widely interpreted as an the canine/premolar complex in the Çorakyerler adaptation to a soft fruit diet. However, there are hominine, unlike Sahelanthropus, Orrorin or Ardip- some diff erences between thinly enameled dryo- ithecus, retains functional honing, at the same time pithecins and chimpanzees. Th e incisors of the fossil that the male canines are reduced compared to the taxa tend to be narrow compared to chimpanzees, large, sharp, and prominently projecting canines of and relatively tall crowned. It has been suggested most other late Miocene Eurasian and extant great that this may be a response to the need to process apes. Th e Çorakyerler hominine is the youngest and foods with tough protective coverings (Begun & largest of all Turkish Miocene hominoids and dif- Kordos 1997). Th e narrow mesiodistal length of fers from all modern and fossil great apes in what is the teeth may have served to generate higher more known of its anatomy and environment. Th e antici- focused occlusal forces, and the crown height may pated recovery of additional cranial and postcranial be a response to wear. Strongly developed lingual remains at Çorakyerler will clarify the adaptations marginal ridges and labial pillars may also have and phylogenetic status of this new genus. served to resist labiolingual bending and torsion. Th is interpretation is supported by a recent analysis BULGARIA of incisor crown curvatures that also links thinly Spassov & Geraads (2008) describe a hominid P4 enameled dryopithecins to hard object feeders from a Turolian locality in the Chirpan district of (Deane 2007). Th e combination of a soft fruit southern Bulgaria. Th ey estimate the age of this fossil frugivore signal from molar occlusal morphology, assemblage at about 7 Ma, which makes it most likely microwear, shearing quotients and enamel thickness somewhat younger that the Çorakyerler homi nine. and a hard object feeding signal from the incisors Spassov & Geraads (2008) indicate that the new is unique and may indicate that hard object pro- Bulgarian specimen resembles Ouranopithecus. Th ey cessing was part of a fall back feeding strategy that do not speculate on the ecological context of the allowed dryopithecins to exploit a wider range of new hominid from Bulgaria, though the presence more diffi cult to process foods in times of resource of the proboscidean Anancus Aymard, 1855 and shortage. Th e mandibular corpora of these thinly the spiral horned antelope Protragelaphus Dames, enameled dryopithecins are also somewhat more 1883 suggests perhaps a relatively open woodland robust than in chimpanzees, which is consistent with environment (Cerling et al. 1999; Merceron et al. this interpretation. Rudapithecus and Hispanopithecus 2005b; Spassov & Geraads 2008), which would localities are interpreted as closed forests but with be broadly consistent with the paleoecology of a greater degree of seasonality than is typical for Ourano pithecus localities (Bonis et al. 1999; Mer- tropical or many subtropical forests today (Andrews ceron et al. 2007a). et al. 1997; Agustí et al. 1999, 2003; Bernor et al. 2004; Rook et al. 2004; Agustí 2007; Merceron et al. 2007b). Th is suggests periods of resource shortage ECOLOGICAL DIVERSITY IN EUROPEAN that would have made an eff ective fall back feeding MIOCENE HOMININES strategy of paramount importance for survival. It is possible that the ability to exploit more embed- Th e large number of European Miocene hominine ded foods also represents a pre-adaptation that led taxa bear witness to a broad range of dietary and eventually to a more extreme and committed hard positional behavior adaptations. In terms of diet there object feeding strategy in Ouranopithecus. are two major patterns. Th e older dryopithecins, As noted above, Ouranopithecus had a robust Dryopithecus, Hispanopithecus and Rudapithecus masticatory apparatus with all the classic indica-

804 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

tors of a hard object diet. Th ese include hyperthick of palmigrady (Almécija et al. 2007). Like Rudap- enamel, large postcanine teeth with low, rounded ithecus, Hispanopithecus has long, strongly curved cusps, robust mandibles and powerfully developed phalanges with strongly developed fi brous fl exor attachment sites for the muscles of mastication sheath ridges, all of which is associated in living (Bonis & Koufos 1993, 1994, 1997; Begun & primates with a specialized adaptation to suspensory Kordos 1997b; Begun 2007b). Th is is supported positional behavior (Susman 1979; Begun 1993; by dental microwear analyses as well (Ungar & Richmond & Whalen 2001; Deane & Begun 2008). Kay 1995; Ungar 1996; Merceron et al. 2005c). However, the metacarpal heads in Hispanopithecus Ouranopithecus also appears to have some reduction are strongly constricted dorsally, with deep collat- in the size of the canines, at least in the maxilla, eral ligament pits expanded dorsally. Th e proximal which leaves more room in the jaw for enlarged articular surfaces of the proximal phalanges are postcanine teeth. Th e anterior teeth are often very said to be oriented more dorsally than in modern strongly worn, suggesting intensive anterior dental hominoids. Th ese characters and the presence of processing, which is often associated with embedded short metacarpals are interpreted to indicate that the foods. Th e paleoecology of Ouranopithecus locali- hand postures of Hispanopithecus included frequent ties is widely regarded as more open than earlier hyperextension at the metacarpo-phalangeal joint, dryopithecins (Bonis et al. 1999), and this is also which is a feature of palmigrade primates (Almécija consistent with a feeding strategy emphasizing et al. 2007). However, palmigrade monkeys do not embedded foods, with perhaps a greater percentage have metacarpal heads as dorsally constricted as coming from terrestrial sources. Hispanopithecus. Hominoids, in contrast, lack these Th ere is an interesting functional parallel between joint characteristics and, given the great develop- the dryopithecins and crown hominines (African ment of their fl exor musculature, they have limited apes and fossils and living humans). Both clades mobility in extension (Tuttle 1969). Th e metacarpal are very diverse and speciose when all fossil taxa heads also lack the typical palmar grooves, or fl ut- are considered. And both clades run the spectrum ing, of the joint surface proximally that are found from soft fruit frugivores (e.g., Rudapithecus, Pan) in most palmigrade monkeys that are related to the to extreme hard object feeders (Ouranopithecus, presence of sesamoid bones (Lewis 1977; Almécija Paranthropus). Th is could be revealing of an emer- et al. 2007). While the proximal articular surfaces gent property of cranial biology in hominines. of the proximal phalanges have some dorsal expan- Hominine cranial form and possibly other adapta- sion, they are large, deep and rounded, and extend tions such as brain size channel a radiation of taxa palmarly between the two large palmar tubercles, that tended to fi ll the same niches independently, again unlike the condition in palmigrade mon- fi rst in Europe in the middle to late Miocene, and keys in which they tend to be broad, shallow and later in Africa in the late Miocene and Pliocene in a more dorsal position. Th e proximal end of (Begun & Kordos 1997). the proximal phalanges are clearly tilted palmarly Diversity in positional behavior in dryopithecins and do not really face dorsally to any signifi cant is less well documented, mainly because postcrania extent. Th e shortness of the metacarpals relative to are not described for Ouranopithecus. Hispano- the phalanges is also not clear cut. Comparisons pithecus and Rudapithecus are both interpreted are limited to the fourth digital ray, in which the as highly arboreal (Begun 1988, 1992b, c, 1994, metacarpal is in two pieces. Although the authors 2007b; Moyà-Solà & Köhler 1996; Begun & Ko- indicate that the length can be easily reconstructed, rdos 1997; Almécija et al. 2007). Interpretations the result is a fourth metacarpal that is signifi cantly diff er however on the precise nature of the arboreal shorter than the second metacarpal, much more locomotion in the two genera. Hispanopithecus is so than in extant anthropoids, except hylobatids, thought by some to have been a strong climber with which otherwise have very slender metacarpals. It well-developed characters related to orthogrady is also very unusual to see a large second metacar- and suspension while retaining features indicative pal and small second proximal phalanx compared

GEODIVERSITAS • 2009 • 31 (4) 805 Begun D. R.

to the fourth digital ray. In hylobatids the fourth strong suspensory signal (Morbeck 1983; Begun ray proximal phalanx is shorter and smaller in ar- 1988, 1992c, 1993, 1994; Begun & Kordos 1997; ticular dimensions than the second. If the fourth Deane & Begun 2008). Preliminary analysis of the meta carpal were really as short as is indicated in femora, pelvis and hand bones is consistent with Almécija et al. (2007), one would expect a similar this interpretation. In most cases the great ape that pattern with the proximal phalanges. Rudapithecus most closely approaches is Pongo. While the metacarpal robusticity and phalangeal Dryopithecus (including Pierolapithecus) is rep- relative size are uncertain in Hispanopithecus, the resented by an exquisite skeleton including well- morphology of the metacarpal heads and the proxi- preserved ribs, vertebrae and hand bones (Moyà-Solà mal articular surfaces of the proximal phalanges, et al. 2004). Th e ribs point to a broad, shallow which are neither monkey-like nor ape-like, may hominoid-like thorax and the carpals are great suggest a unique feature of the positional repertoire ape like in the absence of contact between the of Hispanopithecus. Frequent palmigrady would sug- triquetrum and ulna. Th e vertebrae are intermedi- gest the need to stabilize the metacarpo-phalangeal ate in the position of the transverse processes and joint in hyperextension, which should lead to dorsal the phalanges are shorter and less curved than in expansion of the distal metacarpal articular surface Hispanopithecus (Moyà-Solà et al. 2004). Moyà-Solà and collateral ligament pits that are more palmarly et al. (2004) interpret this mixture of characters to displaced. Th e opposite is the case in Hispanopithecus. refl ect a unique combination of behaviors, including Large dorsal collateral ligament pits would cause powerful climbing and orthogrady and palmigrade the collateral ligaments to become taut and bring hand posture, but not suspension. Begun & Ward the joint into maximum close packed position in (2005) suggest that the vertebral and phalangeal a relatively wide range of fl exion, as expected in a characters of Dryopithecus catalaunicus do not pre- suspensory animal. Th e joint would be relatively clude suspension, and the strongly developed sec- loose in extension. Instead of palmigrady, the un- ondary shaft characters of the phalanges are most usual morphology of the metacarpo-phalangeal consistent with suspension, despite the somewhat joint may simply refl ect the need to stabilize the reduced length compared to Hispanopithecus. It is joint in a wide range of fl exed postures. noteworthy that many Old and New World monkeys Th e other especially informative aspects of the practice suspensory positional behaviors, though postcrania of Hispanopithecus are the femur and perhaps not as adeptly as hominoids, and in some lumbar vertebrae. Th e best preserved vertebrae show cases with the aid of a prehensile tail, despite lack- the typical great ape character of a dorsally displaced ing the hominoid-like characters of Dryopithecus. transverse process, which has been related to the Either way, Dryopithecus is the oldest hominid with presence of a short, stiff lower back (Moyà-Solà & well-preserved and unambiguous evidence of a great Köhler 1996; Ward 2007). Th e well-preserved femur ape body plan (Moyà-Solà et al. 2004). has features of the hip joint related to suspension and high hip mobility (Köhler et al. 2002). In sum, the postcranial skeleton of Hispanopithecus preserves AFRICAN LATE MIOCENE HOMININES much evidence of a highly arboreal, climbing, sus- AND THE PALEOBIOGEOGRAPHY pensory hominoid. Possible retention of relatively OF HOMININE ORIGINS frequent palmigrady has been suggested but the evidence in my view is inconclusive. As noted earlier, there is agreement among many Rudapithecus from Rudabánya is known from researchers that the dryopithecins are hominines, a number of phalanges, hand and foot bones, the even if there is some disagreement on their precise distal end of the humerus, proximal ends of a radius relationships to crown hominines. Th ere are, how- and ulna, two partial femora and a partial pelvis. ever, hominines in the African late Miocene, and Th e phalanges, humeral, radial and ulnar specimens some suggest that these evolved not from European are very similar to extant great apes with a clear hominines but in situ in Africa. Th e European taxa

806 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

are either dismissed as non-hominine or consid- of the most likely dispersal route between Europe ered to have dispersed into Europe in the middle and Africa, the eastern Mediterranean, was already Miocene from an unknown middle Miocene Af- too inhospitable for apes (Rook & Bernor 2004), rican ancestor (Rook & Bernor 2004; Pickford & is misleading for several reasons. Firstly, the drying Senut 2005; Kunimatsu et al. 2007; Suwa et al. that is typical of the broadly defi ned “Pikermian 2007). Th e evidence of the hominine affi nities of biome” begins to show an impact on environments the dryopithecins is actually quite strong, both from after 10 Ma, and it was not until 8-9 Ma that the the analysis of Ouranopithecus and the Dryopithecus- eff ects become pronounced (Solounias et al. 1999; Hispanopithecus-Rudapithecus group (see above and Agustí et al. 2003; Eronen & Rook 2004; Fortelius the numerous references cited). Th e real question et al. 2006; Agustí 2007). Th ere is no paleoecologi- is not whether European late Miocene hominids cal evidence to suggest that the eastern Mediter- are hominines, but, do the European hominines ranean was inhospitable to forest living primates represent one or more side branches of hominine before 10 Ma. Secondly, many recent analyses evolution, having dispersed into Europe one or more question the overall “savanna-like” quality of the times from unknown ancestors, or is the much larger eastern Mediterranean in the late Miocene, and record of Miocene hominines in Europe the true several stress the persistence of forest even after source of later hominines that dispersed into Africa 10 Ma, despite the overall drying trend. Akgün et in the late Miocene? Th ere is strong evidence for al. (2007) identify mixed mesophytic and swamp the latter hypothesis in data from the morphology, forest assemblages in western Anatolia in the late geochronology and paleobiogeography of European Miocene. Bruch et al. (2006) found evidence for a hominines and other land mammals (Begun 2001, warm and humid climate overall in the Pannonian 2005, 2007a; Begun & Nargolwalla 2004; Nargol- basin and well into the Balkans in many fossil plant walla 2009). Th e morphological evidence is reviewed localities until 9 Ma, with no indication of a Medi- above. Hominines occur in Europe more than 2 terranean climate. Pickford et al. (2006) identify a million years before they appear in Africa. Th ey are humid climate in the southern Mediterranean be- more widespread and diverse than African hominines. tween 10-11 Ma. Fortelius et al. (2006) produced Many land mammals are known to have expanded palaeoprecipitation maps for the late Miocene, their ranges between Africa and Europe in the late through to about 9.5 Ma, which show very little Miocene, during the temporal interval between the regional diff erentiation between central Europe and fi rst appearance of Vallesian European hominines the eastern Mediterranean. Ivanov et al. (2002) and and the fi rst appearance of African hominines, Griffi n (2002) describe fl uctuating cycles of warm/ including many taxa with preferences for forests humid and cooler/dryer conditions in the northern (Fortelius et al. 1996; Leakey et al. 1996; Dawson Balkans in the late Miocene. Finally, the ape that 1999; Ginsburg 1999; Heissig 1999; Made 1999; dispersed from Europe to Africa is undiscovered Solounias et al. 1999; Agustí et al. 2001; Winkler at present, and therefore we have no knowledge of 2002; Lehmann et al. 2006; Agustí 2007; Likius its ecological preferences, but if it was like many et al. 2007; Nargolwalla 2009). Th ese dispersals or living primates it was probably capable of surviv- range expansions are widely believed to be related to ing in a diversity of environments. Th us, there is changing climatic conditions in Europe, including no reason a priori to believe that hominines could increases in seasonality and a decline in forest cover not have taken part in the general dispersal of land (Bernor et al. 1979; Bernor 1983; Quade et al. 1989; mammals between Europe and Africa during the Fortelius et al. 1996; Leakey et al. 1996; Agustí et late Miocene, and in fact Darwin speculated 150 al. 1999, 2001, 2003; Bonis & Koufos 1999; Cer- years ago that this may well have taken place. ling 1999; Cerling et al. 1999; Magyar et al. 1999; Th ere is a good chance that African hominines Solounias et al. 1999; Fortelius & Hokkanen 2001; evolved from a European ancestor. What is the nature Koufos 2003; Eronen & Rook 2004; Fortelius et of this ancestor and the dynamics of early homi- al. 2006; Agustí 2007). Th e claim that the ecology nine evolution in Africa? While the broad picture

GEODIVERSITAS • 2009 • 31 (4) 807 Begun D. R.

of paleoecology in the eastern Mediterranean may microCT analysis revealing several characters of the favor the view that a more open woodland taxon enamodentine junction (EDJ) that support this al- such as Ouranopithecus or a relative is more likely location. Pickford et al. (2009) recently described to have expanded its range from Europe to Africa as hominoid a very poorly preserved mandibular than a forest form such as Rudapithecus, there were specimen from Niger with an estimated age of opportunities for expansion by forest dwelling taxa 5-11 Ma. Th is specimen, along with other isolated as well (Nargolwalla & Begun 2009). Th e small but teeth from Kenya in the same temporal range growing record of hominines from Africa does not (Pickford & Senut 2005), are too poorly preserved help resolve this question. Nakalipithecus Kunimatsu to be assigned to any known hominoid clade with et al., 2007, a hominine candidate from 9.8 Ma any confi dence. deposits in Kenya, is similar in many features to Chororapithecus Suwa, Kono, Katoh, Asfaw & Ouranopithecus (Kunimatsu et al. 2007). Th e main Beyene, 2007, represented by a handful of isolated specimen, a mandible, preserves the molars but they teeth from 10-10.5 Ma deposits in Ethiopia, is are very strongly worn, with indications of partial said to possibly be an early member of the Gorilla buccal cingula, unlike Ouranopithecus and more like clade (Suwa et al. 2007). Th e overall morphology the Proconsul-like molars from 10.5 Ma deposits at of the molars resembles many thickly enameled Ngorora (Hill & Ward 1988). However, an upper late Miocene hominid molars, but the EDJ, while female canine is very similar to Ouranopithecus, es- mostly fl at like most hominids with thick enamel, pecially in the morphology of the cervix and lingual has a subtle cresting pattern that Suwa et al. (2007) aspect (Kunimatsu et al. 2007). Kunimatsu et al. interpret to be homologous to a much better devel- (2007) suggest that Nakalipithecus may be ances- oped crest on gorilla molars. Again, the connection tral to Ouranopithecus, given its slightly older age to Gorilla is possible, though much more data are and more primitive morphology. Th is may be the needed to make a strong case for this relationship. case, although more fossils are needed to eff ectively Chororapithecus is at least 2 Ma younger than Dryo- distinguish Nakalipithecus from the late surviving pithecus, and does not therefore directly challenge the proconsulids from Ngorora. Even if Nakalipithecus hypothesis that hominines fi rst appear in Europe. is broadly ancestral to Ouranopithecus, they are so However, it does present an interesting potential close in known age (9.8 vs. 9.6 Ma) that they should scenario for the evolution of thinly enameled teeth be considered essentially contemporaneous, and from a thickly enameled ancestor. Rook & Bernor either one could have originated fi rst. In addition, (2004) consider it unlikely that Ouranopithecus range expansions of late Miocene hominines are could be ancestral to Aridpithecus, the latter hav- likely to have been complex and multidirectional, ing thin molar enamel, although morphologically with expansions and contractions contributing the teeth are broadly similar to one another and to complex patterns of speciation and extinction. to australopithecines generally. Th e transformation Whatever the relationship is between Ourano- from a Chororapithecus dental morphology to that pithecus and Nakalipithecus, the oldest hominine of the extant gorilla is much more dramatic, and is is still Dryopithecus, from localities in Europe that a cautionary tale about what it is wise to consider are more than 2 Ma older. likely or unlikely a priori in evolutionary history. Samburupithecus Ishida & Pickford, 1997 has also been proposed as an early hominine based on its overall robust morphology and thickly enameled CONCLUSIONS molars (Ishida & Pickford 1997). However, Begun (2007a) notes that Samburupithecus retains many Th is review stresses the phyletic unity and ecologi- primitive characters with Proconsul that are lack- cal diversity of European middle and late Miocene ing in hominids, concluding that it is most likely hominines, and explicitly recognizes the pioneer- to be a late surviving member of the Proconsuloi- ing eff orts of Louis de Bonis in providing strong dea. Olejniczak et al. (2009) recently conducted a evidence for decades to support the Afro-European

808 GEODIVERSITAS • 2009 • 31 (4) Dryopithecins, Darwin, de Bonis, and the European origin of the African apes and human clade

Miocene hominine connection. Diversity in Euro- to changing conditions in the late Miocene, and pean Miocene hominines parallels that of Pliocene disperse into Southeast Asia and Africa. Specifi - to recent hominines, with a range of ecological cally, the adaptations that developed in European preferences from suspensory, highly arboreal soft hominines persist in extant hominines, and set fruit frugivores living in closed forests, to hard ob- the stage for the development of further changes ject feeders, possibly much more terrestrial, living in positional behavior, diet and eventually brain in more open settings. size that characterize the evolutionary history of Th e conclusion that hominines originate and the hominins. experience their initial adaptive radiation in Europe is signifi cant in setting the ecological and temporal context for the evolution of our subfamily. Homi- Acknowledgements nines and pongines are likely to have evolved from I am grateful to Stéphane Peigné and Gildas Mer- early middle Miocene thickly enameled taxa, such ceron for asking me to contribute to this volume as Griphopithecus from Europe and Western Asia honoring the career of Louis de Bonis. Th anks as or a close relative from later localities in Africa well to Gildas Merceron, George Koufos and an (Nacholapithecus Ishida, Kunimatsu, Nakatsukasa & anonymous reviewer who provided many useful Nakano, 1999, Equatorius Ward, Brown, Hill, Kel- comments. I thank the many curators who have al- ley & Downs, 1999, Kenyapithecus Leakey, 1962). lowed me to study the fossils in their care, especially While it may seem unnecessarily complicated to Louis, who hosted me during my fi rst visit to examine suggest that multiple dispersals and/or range exten- European Miocene fossils, in 1984. His generosity sions occurred between Africa and Eurasia during and patience with an upstart graduate student will the evolution of the hominids before the hom- always be fondly remembered. I wish him much inines disperse from Europe to Africa a fi nal time continued success in all his endeavours. in the late Miocene (Begun 2002, 2005, 2007a; Andrews & Kelley 2007), this is the scenario pro- posed for several taxa including aardvarks, several REFERENCES carnivores, antelopes, hippos and probably at least one lineage of proboscidean (Leakey et al. 1996; ABEL O. 1902. — Zwei neue Menschenaff en aus den Leit- Ginsburg 1999; Heißig 1999a, b; Made 1999; hakalkbildungen des Wiener Beckens. Sitzungsberichte der Akademie der Wissenschafen Wien 111 (1): 1171- Boisserie et al. 2003; Werdelin 2003; Begun & 1202. Nargolwalla 2004; Lehmann et al. 2006; Likius et AGUSTÍ J. 2007. — Th e biotic environments of the al. 2007; Koufos & Bonis 2008). late Miocene hominids, in HENKE W. & TATTER- Th e major changes experienced by both the SALL I. (eds), Handbook of Paleoanthropology. Vol. hominines and the pongines in Eurasia include 2: Primate Evolution and Human Origins. Springer, Berlin: 979-1009. diversifi cation of positional behavior and the de- AGUSTÍ J., CABRERA L. & GARCÉS M. 2001. — Chronology velopment of the extant hominid suspensory body and zoogeography of the Miocene hominoid record in plan, specialization of dietary adaptations, increases Europe, in BONIS L. DE, KOUFOS G. & ANDREWS P. in overall body and brain size, and an overall slow- (eds), Hominoid Evolution and Environmental Change ing of life history (Begun & Kordos 2004; Kelley in the Neogene of Europe. Volume 2: Phylogeny of the Neogene Hominoid Primates of Eurasia. Cambridge 2004; Russon & Begun 2004). Th e one aspect of University Press, Cambridge: 2-18. hominid biology that unites all of these charac- AGUSTÍ J., CABRERA L., GARCÉS M. & LLENAS M. 1999. — teristics is behavioral fl exibility and the ability to Mammal turnover and global climate change in the late cope with diverse and changing ecological condi- Miocene terrestrial record of the Vallès Penedès basin tions (Potts 2004; Russon & Begun 2004). Th ese (NE Spain), in AGUSTÍ J., ROOK L. & ANDREWS P. (eds), Hominoid Evolution and Climate Change in adaptations fi rst appear in Eurasia in response to Europe. Volume 1: Th e Evolution of Neogene Terrestrial Eurasian ecological conditions, and they are likely Ecosystems in Europe. Cambridge University Press, to have permitted hominids to survive and adapt Cambridge: 397-412.

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Submitted on 16 December 2008; accepted on 9 October 2009.

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