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Home , Afropithecus, Anoiapithecus, Equatorius, Gorillini, Griphopithecus, Homininae

A unique Middle European hominoid and the origins of the great and Salvador Moya` -Sola` a,1, David M. Albab,c, Sergio Alme´ cijac, Isaac Casanovas-Vilarc, Meike Ko¨ hlera, Soledad De Esteban-Trivignoc, Josep M. Roblesc,d, Jordi Galindoc, and Josep Fortunyc aInstitucio´Catalana de Recerca i Estudis Avanc¸ats at Institut Catala`de Paleontologia (ICP) and Unitat d’Antropologia Biolo`gica (Dipartimento de Biologia , Biologia Vegetal, i Ecologia), Universitat Auto`noma de Barcelona, Edifici ICP, Campus de Bellaterra s/n, 08193 Cerdanyola del Valle`s, Barcelona, ; bDipartimento di Scienze della Terra, Universita`degli Studi di Firenze, Via G. La Pira 4, 50121 Florence, ; cInstitut Catala`de Paleontologia, Universitat Auto`noma de Barcelona, Edifici ICP, Campus de Bellaterra s/n, 08193 Cerdanyola del Valle`s, Barcelona, Spain; and dFOSSILIA Serveis Paleontolo`gics i Geolo`gics, S.L. c/ Jaume I nu´m 87, 1er 5a, 08470 Sant Celoni, Barcelona, Spain

Edited by , Harvard University, Cambridge, MA, and approved March 4, 2009 (received for review November 20, 2008) The great ape and human clade (: ) currently sediments by the diggers and bulldozers. After 6 of includes , , , , and . fieldwork, 150 fossiliferous localities have been sampled from the When, where, and from which taxon hominids evolved are among 300-m-thick local stratigraphic series of ACM, which spans an the most exciting questions yet to be resolved. Within the Afro- interval of 1 million years (Ϸ12.5–11.3 Ma, Late Aragonian, pithecidae, the Kenyapithecinae (Kenyapithecini ؉ Equatorini) Middle Miocene). To date, 38,000 macrovertebrate remains and have been proposed as the sister taxon of hominids, but thus far thousands of small teeth have been recovered from the the fragmentary and scarce Middle Miocene record has above mentioned localities, some of which have yielded hampered testing this hypothesis. Here we describe a male partial remains (3–5). These localities can be accurately dated because face with of a previously undescribed fossil hominid, of detailed litho-, bio-, and magnetostratigraphic control (4). An brevirostris gen. et sp. nov., from the Middle Mio- age close to 11.9 Ma can be estimated for ACM/C3-Aj, from cene (11.9 Ma) of Spain, which enables testing this hypothesis. which IPS43000 was excavated. Morphological and geometric morphometrics analyses of this ma- terial show a unique facial pattern for hominoids. This taxon Description. The face of IPS43000 (Fig. 1) lacks the nasals and the combines autapomorphic features—such as a strongly reduced right , some parts of the orbits, and parts of both facial prognathism—with kenyapithecine (more specifically, keny- zygomatics. The palate is nearly complete, lacking only the left apithecin) and hominid synapomorphies. This combination sup- C1 and M3,aswellastheincisors;partofthefrontalalsois ports a sister-group relationship between kenyapithecins (Gripho- preserved. The mandible preserves the symphysis and a large pithecus ؉ ) and hominids. The presence of both portion of the 2 corpora, but lacks the 2 rami; the left I1 and groups in Eurasia during the Middle Miocene and the retention in C1-M2 series and the right C1-M1 series are preserved. Complete kenyapithecins of a primitive hominoid postcranial body plan eruption of the M3 indicates that IPS43000 belongs to an adult support a Eurasian origin of the Hominidae. Alternatively, the two individual, because the slight displacement of this from the extant hominid ( and ) might have alveolar plane merely results from bone distortion at the level of independently evolved in and Eurasia from an ancestral, M2-M3. Middle Miocene stock, so that the supposed crown-hominid syna- pomorphies might be homoplastic. Systematic . Systematic paleontology is as follows: Primates Linnaeus, 1758; suborder Anthropoidea Mivart, Anoiapithecus gen. nov. ͉ ͉ Hominidae ͉ Hominoidea ͉ 1864; infraorder Geoffroy, 1812; superfamily Homi- Paleoprimatology noidea Gray, 1825; family Hominidae Gray, 1825; subfamily incer- tae sedis; tribe Dryopithecini Gregory and Hellman, 1939; Anoia- here is a general consensus on the relevance of Middle pithecus gen. nov. type A. brevirostris gen. et sp. nov. TMiocene hominoids for understanding hominid origins (1, Etymology is from Anoia (the region where the site is situated) and 2). However, the question of the initial great-ape/human radi- the Greek pithekos (ape). Generic diagnosis is as for the type ation still remains elusive. In this paper we describe a previously species, A. brevirostris gen. et sp. nov. Holotype is IPS43000, a partial underscribed Middle Miocene thick-enameled hominid [see face with mandible of an adult male individual, housed at the supporting information (SI) Text and Table S1,regardingthe Institut Catala`de Paleontologia (Fig. 1; see Table 1 for dental systematic framework used in this paper], which displays a measurements). Type locality is ACM/C3-Aj (Abocador de Can unique and unusual combination of facial characteristics with Mata, Cell 3, locality Aj), in the municipal term of Els Hostalets de significant phylogenetic implications. Anoiapithecus brevirostris Pierola (Catalonia, Spain). Age is subchron C5r.3r (Middle Mio- gen. et sp. nov. shows the basic great-ape synapomorphies and cene, Ϸ11.9 Ma), on the basis of the local ACM magnetostrati- some generalized afropithecid and several kenyapithecine- graphic series (4), corresponding to the local biozone Megacricet- derived features, coupled with a striking reduction of the face. odon ibericus ϩ Democricetodon larteti (MN 7 Mammal Neogene This combination is unknown from any fossil or extant great ape, biozone), on the basis of biostratigraphic data (3, 4). Etymology is which has important implications for reconstructing the initial from the Latin brevis (short) and rostrum (snout). evolutionary history of the great ape and human clade.

Stratigraphic Setting. The description of this taxon is based on a Author contributions: S.M.-S. designed research; S.M.-S., D.M.A., and M.K. performed hominoid partial face with mandible (IPS43000) discovered at research; J.F. contributed new reagents/analytic tools; D.M.A., S.A., I.C.-V., S.D.E.-T., J.M.R., locality Abocador de Can Mata (ACM)/C3-Aj, in the area of Els J.G., and J.F. analyzed data; and S.M.-S., D.M.A., and M.K. wrote the paper. Hostalets de Pierola (Valle`s-Penede`s Basin, Catalonia, Spain). Conflict of interest: The authors declare no conflict of interest. This region is characterized by thick Middle to This article is a PNAS Direct Submission. stratigraphic sequences. The construction of a rubbish dump 1To whom correspondence should be addressed. E-mail: [email protected].

(ACM) near the country house of Can Mata (Fig. S1)prompted This article contains supporting information online at www.pnas.org/cgi/content/full/ ANTHROPOLOGY apaleontologicalinterventiontocontroltheremovalofMiocene 0811730106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811730106 PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ no. 24 ͉ 9601–9606 AB C D

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Fig. 1. Cranium and mandible of Anoiapithecus brevirostris (IPS43000, holotype). (A) Right lateral view. (B) Frontal view. (C) Left lateral view. (D) Superior view. (E) Palatal view. (F) Occlusal view of the mandible. (G) CT scan of the right M2, showing enamel thickness. All photographs were taken with the tooth row oriented horizontally. For safety reasons, the cranial reconstruction (A–D) is based on casts of the original specimens.

Specific Diagnosis. The face is characterized by reduced nasal and the posterior part of the C1 (with the alveolar plane horizontal). alveolar prognathism with a very short premaxilla. The anterior Nasal aperture edges are vertical. The zygomatic root is mod- border of the orbit is situated over the P3–P4 limit, the glabella erately high and situated over the M1.Theanteriorsurfaceofthe is over the P4,andtheanteriormostnasomaxillarycontactisover zygomatic root is downwardly inclined. The frontal sinus is well developed, filling the glabellar area and part of the frontal squama. The maxillary sinus is reduced, situated well above the Table 1. Dental measurements (in millimeters) of Anoiapithecus roots of the molars, occupying a small area below the medial side brevirostris gen. et sp. nov. from ACM/C3-Aj of the orbit. The zygomatic root is not pneumatized. Coalescent Upper teeth Lower teeth temporal lines indicate the presence of a . Thin superciliary arches are evident. A large and open incisive MD BL MD BL foramen, with the posterior border located at the level of the P3, is shown. The palate is short, wide, and deep. The pyriform L I1 — — 4.8 6.7 R C1 14.2 9.6 12.9 8.5 aperture is wide, widest close to the base. is charac- L C1 — — 13.2 9.2 terized by thick enamel (relative enamel thickness, RET ϭ 20) R P3 — — 12.7 7.3 with low dentine penetrance. Low crowns show globulous cusps, L P3 7.0 11.7 12.3 7.6 blunt crests, and restricted basins with nonperipheralized cusps; R P4 — — 7.6 8.8 there are remnants of cingula in lower teeth. Canines and P3 are L P4 7.2 10.4 7.8 8.6 low-crowned whereas upper canines are relatively small and very R M1 9.4 11.2 9.1 8.9 compressed. A robust mandible shows highly divergent rami and L M1 9.4 11.4 9.5 9.1 reduced mandibular length; strong and long inferior torus and R M2 11.3 11.8 — — weak superior torus that forms a shelf. L M2 10.7 12.1 11.5 10.0 R M3 10.2 10.4 — — Differential Diagnosis. Anoiapithecus differs from all known Mio- MD, mesiodistal; BL, buccolingual; R, right; L, left. cene Eurasian hominoids by the very orthognathous face, be-

9602 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811730106 Moya`-Sola`et al. Fig. 2. Craniofacial angle (CFA) in living and fossil catarrhines. CFA is the angle formed by the line joining glabella and prosthion with the tooth row plane (in lateral view). Extinct taxa are represented by individual values, whereas living taxa are represented by the mean and the 95% confidence interval for the mean. Note that Anoiapithecus differs from both extant cercopithecoids and nonhuman hominoids by displaying a CFA well above 60°, most closely resembling members of the . cause of reduced mid- and lower facial prognathism, with the glabella and orbits situated very anteriorly (close to the premo- lars and C1 on the vertical plane); it further differs from the above-mentioned taxa except by the presence of a sagittal crest. More specifically, Anoiapithecus further differs from proconsulids and afropithecids by the possession of hom- inid facial synapomorphies, including the wide nasal aperture widest at the base, the high face, the deep palate, and the configuration of the nasals. With regard to kenyapithecins, it further differs from Kenyapithecus by the reduced heteromorphy of the upper and low-crowned canines and from by the strongly reduced cingula and the high zygomatic root. As compared to other Middle Miocene dryo- pithecins, among others it differs from by the presence of a frontal sinus, by the thicker enamel, the less peripheralized cusps, and the downward inclination of the zygomatic root; and from by the lower degree of nasoalveolar prognathism and the more posteriorly situated anterior zygomatic root. Finally, as compared to the short-faced, Fig. 3. Results of the geometric morphometrics analysis. (A) Scatter diagram Late Miocene Oreopithecus, Anoiapithecus further differs by the showing the 2 first canonical axes (CA) of a canonical variate analysis (CVA), higher face, the shorter muzzle, the reduced maxillary sinus, the reflecting the differences in the facial profile of living and fossil catarrhines vertical nasals, the lack of a nasoalveolar clivus covering (see Materials and Methods and SI Text for further information). Visualiza- the palatine fenestra, and the morphology of the dentition. tions of the shape changes along the CA are also shown; to facilitate the interpretation, the grids are rotated so that the alveolar plane is horizontal. CA1 reflects the degree of midfacial concavity, while CA2 reflects the degree Morphometric Analyses. Craniofacial angle. The most outstanding of alveolar prognathism. Note that, regarding these axes, Anoiapithecus characteristic of A. brevirostris is the strong reduction of the facial closely approaches hylobatids and colobines, far away from stem hominoids, skeleton, because of the combination of an anteriorly positioned extant great , and Pierolapithecus.(B) UPGMA cluster based on Euclidean glabella with limited nasal and reduced alveolar prognathism. distances computed from centroids (for extant taxa) and discriminant scores Measurements of the craniofacial angle (CFA) clearly show this (for extinct taxa). Note that Anoiapithecus clusters with colobines, unlike both pattern (Fig. 2; see also SI Text and Tables S2 and S3). In fossil African stem hominoids (which cluster with Macaca and stem catarrhines) and and living catarrhines, CFA does not surpass 60°, with colobines Eurasian fossil great apes (which cluster with living great apes). and hylobatids displaying the highest values, because of their anteriorly placed glabella. The value of A. brevirostris is even higher and only comparable to that of fossil Homo.Thediffer- anterior glabella, thus forming the midfacial concavity typical of ences in CFA between Anoiapithecus and other fossil taxa this group (Fig. 3A). Several Miocene great apes such as included in the analysis clearly exceed the normal range of , , ,andSivapithe- variation within extant taxa, as reflected by their 95% confidence cus fit this pattern. More primitive taxa, however, such as the intervals, thus confirming the distinctiveness of the unique stem hominoids , Turkanapithecus,andProconsul taxon. rather match the pattern of extant cercopithecines, whose facial Geometric morphometrics. To further evaluate the uniqueness of the profile is characterized by strong alveolar and midfacial progn- pattern of Anoiapithecus,weanalyzedtheshapeofthefacial athism, with glabella placed posteriorly from nasion, and rhinion profile using a geometric morphometrics approach (Fig. 3; see being much more anteriorly situated. The stem hominid Piero- also SI Text and Tables S4 and S5). Extant great apes are lapithecus displays a similar or even higher degree of alveolar

characterized by strong alveolar prognathism, because of the prognathism, while the degree of midfacial concavity is inter- ANTHROPOLOGY posteriorly placed rhinion and nasion in relation to the more mediate between stem hominoids and living great apes. Anoia-

Moya`-Sola`et al. PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ no. 24 ͉ 9603 A

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Fig. 4. Simplified cladogram depicting the phylogenetic hypothesis and biogeographic scenario favored in this paper. The Afropithecinae include the Afropithecini; the Equatorini include and ; the Kenyapithecini include Kenyapithecus and Griphopithecus; and the Dryo- Fig. 5. CT scans in a parasagittal plane of (A) the left maxilla of Anoiapithe- pithecini include Pierolapithecus, Dryopithecus s.s., and Anoiapithecus. cus brevirostris gen. et sp. nov. (IPS43000, holotype) and (B) the right maxilla Nodes: 0, taillessness and other postcranial and cranial features; 1, thick of Pierolapithecus catalaunicus (IPS21350, holotype), to the same scale. Each enamel, dental morphology, robust mandible, procumbent premaxilla; 2, CT scan is accompanied by a virtual model showing the plane represented by anterior position of the zygomatic root, strong mandibular inferior torus; 3, the scans. Note the lack of sinus over the roots in the preserved maxilla reduction of maxillary sinus, very deep canine fossa, reduced mandibular of Anoiapithecus. The more completely preserved Pierolapithecus specimen length; 4, high face, high zygomatic root, wide nasal aperture (widest at the similarly shows a small and restricted maxillary sinus (the lower and anterior base), flat nasals that project anteriorly beneath the level of the inferior limits of the sinus are marked by white points), which does not reach the apices orbital rim, orthograde-related features (as judged from Pierolapithecus). of the dental roots and anteriorly does not surpass the level of posterior M1. This hypothesis implies a back-to-Africa dispersal of the Homininae and a reversal of some features of node 3 in this group, but assumes that features of node 4 are homologous between pongines and hominines. lids (1, 2, 6–8, 10) and can be hence interpreted as derived features that might reflect a phylogenetic link between keny- apithecines and stem Eurasian hominids (Fig. 4). pithecus differs from great apes by the lack of midfacial concav- Among others, Anoiapithecus shares with all afropithecids a ity, but unlike Pierolapithecus,itdisplaysaveryorthognathous thick-enameled condition (Fig. 1G), with a RET value of 20, face, with rhinion situated very close to and vertically aligned which is in the upper range of Griphopithecus alpani from Pas¸alar with nasion. It, thus, approximates the pattern observed in (11). This feature is further combined with other shared den- colobines and, to a lesser extent, (Fig. 3B). tognathic features, such as low dentine penetrance, globulous Given the distinctiveness of the facial morphology of Anoia- and nonperipheralized cusps with restricted basins, thick and pithecus,ascomparedtobothlivingandfossilhominoids,itis rounded crests, a robust mandible, and a procumbent premaxilla. likely that it represents an autapomorphically derived condition Anoiapithecus also shares derived features with the Keny- of this taxon. To ensure that great differences found by the apithecinae (Equatorius, Nacholapithecus, Kenyapithecus,and canonical analysis between Anoiapithecus and other extinct taxa Griphopithecus cannot be accommodated by the normal range of variation that ). These synapomorphies include the anterior is customarily found within extant hominoid genera, we followed position of the zygomatic root, indicating a shorter face than in arandomizationapproachonthebasisofdiscriminantscores. the Afropithecinae, and a strong mandibular inferior torus The results of this analysis (SI Text)allowustorefutethe entailing a simian shelf (1, 6–8, 10, 12–16). Moreover, Anoia- hypothesis that differences between Anoiapithecus and Piero- pithecus shares with Eurasian Middle Miocene Kenyapithecini lapithecus might be attributable to interindividual variation (Kenyapithecus and Griphopithecus)anextremereductionofthe within a single genus with P Ͻ 0.001, which confirms the need maxillary sinus, which is situated well above the roots of the to erect a previously undescribed taxon. molars (Fig. 5A). The extent of the maxillary sinus should be interpreted with great care, because it can increase throughout Discussion life. Nevertheless, the holotype of A. brevirostris belongs to a fully 3 Despite its autapomorphic facial morphology, A. brevirostris adult individual, as evidenced by the fully erupted M and the retains primitive stem-hominoid features (1, 6–8), such as presence of some dental wear on both M2 and M3 (albeit with no low-crowned teeth (especially the P3 and canines), cheek teeth dentine exposure, given the thick-enameled condition of this with flaring labial and lingual walls, short canine roots converg- taxon). Moreover, additional CT scans of the of Piero- ing toward the midline, heteromorphic upper cusps, lapithecus (Fig. 5B)haverevealedthatthisstemhominidalso and a frontal sinus that invades the glabella and the frontal retains this kenyapithecin trait. Further synapomorphies of squama. These features, like the autapomorphic facial pattern, Anoiapithecus and kenyapithecins are a very deep canine fossa are not phylogenetically informative (1, 9). However, A. bre- and reduced mandibular length with anteriorly placed mandib- virostris shares an array of significant features with both Middle ular rami (1, 6–7, 10, 12–17). The extreme shortening of the face Miocene afropithecids (here included within the Kenyapitheci- in Anoiapithecus denotes a step further in the tendency toward nae) and Middle to Late Miocene hominids (see SI Text and facial reduction that characterizes kenyapithecins. Table S1 for further details on the systematics used in this Significantly, Anoiapithecus also exhibits the basic facial hom- paper). These features are lacking in Early Miocene proconsu- inid synapomorphies (8), indicating that this taxon is a stem

9604 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811730106 Moya`-Sola`et al. member of the great ape and human clade: high face, high convergence would be far more common during hominoid zygomatic root, pyriform nasal aperture widest at the base, deep evolution than the principle of parsimony, customarily applied to palate, and nasals that project slightly anteriorly beneath the cladistic analyses, generally assumes. We expect that future level of the lower orbital rims (observed from the nasomaxillary discoveries, particularly in the long Middle to Late Miocene sutures). The same modern facial pattern is also shared by stratigraphic sections of Els Hostalets de Pierola section (Cata- Pierolapithecus (5), despite the striking differences in facial lonia, Spain) (3, 4), may help to disentangle the complex profile as compared to Anoiapithecus. question of the initial diversification of the great apes. The retention of highly specialized, derived kenyapithecine features in a stem hominid such as Anoiapithecus has important Materials and Methods implications for understanding the origin of the Hominidae. The The Primate Sample. The facial profile of A. brevirostris was compared to that presence in Eurasia of kenyapithecin hominoids (Kenyapithecus of living and extinct catarrhines by means of univariate and multivariate and Griphopithecus)ofputativeAfricanoriginbyϷ16.5 Ma (18) techniques (see below). Several fossil specimens and many different individ- or 15–14 Ma (19, 20) has led some authors to hypothesize that uals from several living genera (Table S6) were included in the analyses. Data later Middle and Late Miocene Eurasian hominids evolved from were taken from photographs of crania in lateral view, taken with the lens parallel to the midsagittal plane. Regarding the extant comparative sample, these taxa (2, 7, 8, 10, 16, 18–24). Hitherto, however, the photographs were taken by the authors at the Koninklijk Museum voor apparent lack of synapomorphies between both groups pre- Midden-Africa (Tervuren, Belgium) and at the Anthropologisches Institut und cluded testing this hypothesis (7). The unique facial specimen of Museum (Zu¨rich, Switzerland), were kindly provided by Xavier Jordana (in the Anoiapithecus provides strong support for a sister-group rela- case of living humans from the Colecc¸o˜ es Osteolo´gicas Identificadas from the tionship between the Kenyapithecini and Hominidae. Addi- Museu Antropolo´gico of the Universidade de Coimbra), and were taken from tional support for this hypothesis comes from the association of the ‘‘Mammalian Crania Photographic Archive’’ Second Edition, which is kenyapithecine traits with cranial and postcranial great-ape available from the Internet (http://1kai.dokkyomed.ac.jp/mammal/en/ synapomorphies in the stem hominid Pierolapithecus (5). mammal.html). Kenyapithecus has been considered a good candidate for the ancestral form of the Hominidae because it shares several CFA. To quantify the degree of orthognathism/prognathism, we measured CFA as the angle comprised between the plane defined by the nasion– features with hominids, including the moderately high zygomatic prosthion and that defined by the occlusal plane. It was measured in 256 root, the high-crowned canine, the reduced molar cingula, and individuals belonging to 11 extant genera (Table S6), including the 5 extant distal humeral morphology (2, 6, 10, 13, 14, 16, 25). The genera of hominoid primates, 3 cercopithecines (Cercopithecus, Macaca, and hominids Anoiapithecus and Pierolapithecus retain plesiomor- Papio) and 3 colobines (the latter being grouped into a single group Colobi- phic low-crowned canines and heteromorphic premolar cusps, nae). Comparisons were carried out by means of ANOVA and post hoc multiple although they do not exhibit the autapomorphies of Kenyapithe- comparisons (Bonferroni method). cus.Furthermore,Pierolapithecus catalaunicus shares with G. alpani the highly distinctive spatulate central with a Geometric Morphometrics. We used a thin-plate spline approach with gener- lingual pillar continuous with the lingual cingulum. This is a alized least-squares (GLS) Procrustes superimposition. A canonical variate feature shared with later, more derived, Eurasian hominoids analysis (CVA) was performed on the resulting matrix of partial warp scores (26–27). This contradictory evidence makes it difficult to de- and the similarities between the several taxa were depicted by means of a cluster analysis based on centroids (extant taxa) and discriminant scores termine which of the 2 kenyapithecin genera is more closely (extinct ones). related to hominids, while it clearly stresses the role of ho- Seven landmarks, defined on the lateral facial profile and projected onto moplasy in hominoid evolution. the midsagittal plane, were used (Fig. S2). Most of these landmarks (nos. 2–7) When currently available evidence is taken into account, the are located at intersections between bones or bone tissues and must be hypothesis suggesting a Eurasian origin for the Hominidae is therefore considered type 1 landmarks following Bookstein’s classification favored, given the following facts: (i)thepresenceinthe (30), while landmark no. 1 (glabella) is of type 2. These landmarks were Eurasian Middle Miocene of both kenyapithecins and hominids, measured in 255 individuals from the same genera included in CFA analysis (ii)theirlikelysister-grouprelationships,and(iii)theirremark- (Table S6) except for Papio and Homo, which were excluded given their able consistent consecutive time span (kenyapithecins, 15–13 extreme condition as compared to the remaining taxa; similarly, fossil Homi- Anoiapithecus Pierolapithecus nini were also excluded from the analysis. Landmarks were digitized using the Ma; dryopithecins such as and , tpsDig software (31). Landmark configurations were superimposed by means 11.9 Ma; and Late Miocene hominids, Ͻ11.1 Ma). Keny- of GLS Procrustes superimposition (32). GLS was conducted using the tpsRelw apithecins retain not only a primitive facial pattern for homi- program (33). A thin-plate spline approach (30, 34) was adopted for visualiz- noids, but also—as far as it can be ascertained—a pronograde ing shape differences and producing a set of variables (the partial warps, postcranial body plan (21–23, 28, 29). Anoiapithecus and other including the uniform components of deformation) amenable to statistical dryopithecins (Dryopithecus s.s. and Pierolapithecus)sharewith analysis. The partial warp scores (weight matrix), indicating the position of Late Miocene Eurasian hominids and extant great apes a derived each individual relative to the reference along the partial warps, were calcu- facial morphology (4, 5) and, at least Pierolapithecus,anortho- lated using the program tpsRelw (33). grade postcranial body plan (5). This combination of characters The canonical variate analysis was performed with SPSS 15.0 on the basis of supports the view that crown hominids originated in Eurasia the weight matrix for extant taxa alone, to define a morphospace reflecting the facial differences between living catarrhines. Groups were defined on the from more primitive, kenyapithecin ancestors and radiated in basis of the different genera included in the analysis, except for Colobus, this continent into pongines and hominines (Fig. 4). Presbytis, and , which were grouped as . Extinct genera This scenario entails a subsequent ‘‘back to Africa’’ dispersal were left ungrouped and classified on the basis of squared Mahalanobis of the hominine clade (African apes and humans) (9, 18). distances a posteriori. A cluster analysis was also performed with SPSS 15.0 on Alternatively, the basic putative facial and postcranial synapo- the basis of Euclidean distances computed from centroids (for extant taxa) and morphies of the Hominidae could be homoplastic between discriminant scores (for extinct taxa) for all canonical axes, by means of the pongines and hominines, with both groups having independently unweighted pair group method with arithmetic mean (UPGMA) and by evolved in Eurasia and Africa, respectively, from different rescaling distances to values comprised between 0 and 25 (Tables S4 and S5). afropithecid ancestors. Independent evolution of suspensory To take into account the range of variation displayed by extant taxa when interpreting the differences found between different fossil individuals (par- capabilities has been previously hypothesized (5). However, ticularly between the holotypes of Anoiapithecus and Pierolapithecus) in the given the lack of both cranial and postcranial crown-hominid geometric morphometrics analysis, we followed a randomization approach. synapomorphies in afropithecids, this alternative, to the back- In particular, on the basis of the discriminant scores of the CVA, we computed

to-Africa hypothesis would entail a more pervasive role for the squared distance for each pair of individuals within several genera (, ANTHROPOLOGY homoplasy than previously suggested. If so, parallelism and , Pongo, and Macaca separately). The distribution of these distances

Moya`-Sola`et al. PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ no. 24 ͉ 9605 was then used to test the null hypothesis that the distance between Anoia- ACKNOWLEDGMENTS. We thank D. Pilbeam and 3 anonymous reviewers for pithecus and Pierolapithecus fits interindividual variation within a single helpful comments and suggestions. We are also indebted to Cespa Gestio´ n de extant genus. This null hypothesis was rejected when the probability of Residuos, S.A. for financing the fieldwork and to the Ajuntament dels Hosta- lets de Pierola, the Departament de Cultura i Mitjans de Comunicacio´ de la finding such a distance was lower than 5%, on the basis of the distribution of Generalitat de Catalunya, the Mu´tua de Terrassa, and the staff of the Institut the selected extant genera separately. Catala` de Paleontologia M. Crusafont for their collaboration. We thank I. Pellejero and S. Val for the excellent preparation of the specimens, W. van Enamel Thickness. RET was measured in a coronal plane through the mesial Neer and Ana Luisa Santos for access to collections, and John Kappelman and cusps of the right M2 as (area of the enamel cap/length of the dentinoenamel Xavier Jordana for kindly providing photographic material. This study has junction)/(area of the dentine)1/2 ϫ 100 (35). The teeth were scanned with been supported by the Comissionat d’Universitats i Recerca [predoctoral fellowship 2006 FI 00065 (to S.A.), postdoctoral grant 2005 BP-B1 10253 (to high-resolution computed tomography (Xylon Compact) at Burgos University D.M.A.), the Searching for the Origins of Modern Hominoids Initiative project, (Spain). Images were analyzed with NIH Image software (developed at the U.S. and Grup de Recerca Consolidat 2005 00397-GGAC], the National Science National Institutes of Health and available from the Internet at http:// Foundation (RHOI-Hominid-NSF-BCS-0321893), and the Spanish Ministerio de rsb.info.nih.gov/nihimage/). Ciencia e Innovacio´n (CGL2008–00325/BTE).

1. Ward SC, Brown B, Hill A, Kelley J, Downs W (1999) Equatorius: a new hominoid genus 18. Begun DR, Gu¨lec¸ E, Geraads D (2003) Dispersal patterns of Eurasian hominoids: from the middle Miocene of . Science 285:1382–1386. Implications from Turkey. Deinsea 10:23–39. 2. Begun DR (2001) In Hominoid Evolution and Environmental Change in the Neogene 19. Agustí J, Cabrera L, Garce´s M (2001) In Hominoid Evolution and Environmental Change of Europe. Volume 2. Phylogeny of the Neogene Hominoid Primates of Eurasia, eds in the Neogene of Europe. Volume 2. Phylogeny of the Neogene Hominoid Primates de Bonis L, Koufos G, Andrews P (Cambridge Univ Press, Cambridge, UK), pp 231–268. of Eurasia, eds Bonis L de, Koufos GD, Andrews P (Cambridge Univ Press, Cambridge, 3. Alba DM, et al. (2006) The fossil vertebrates from Abocador de Can Mata (Els Hostalets UK), pp 2–18. de Pierola, l’Anoia, Catalonia), a succession of localities from the late Aragonian (MN6 20. Van der Made J (1999) In The Miocene Land of Europe, eds Ro¨ssner GE, and MN7ϩ8) of the Valle`s-Penede`s Basin. Campaigns 2002–2003, 2004 and 2005. Est Heissig K (Friedrich Pfeil Verlag, Mu¨nchen), pp 457–472. Geol 62:295–312. [in Spanish] 21. Andrews P, Martin L (1987) Cladistic relationships of extant and fossil hominoids. J Hum 4. Moya`-Sola`S, et al. (2009) First partial face and upper dentition of the Middle Miocene Evol 16:101–118. hominoid Dryopithecus fontani from Abocador de Can Mata (Valle`s-Penede`s Basin, 22. Begun DR, Ward CV, Rose MD (1997) In Function, Phylogeny and : Miocene Catalonia, NE Spain): taxonomic and phylogenetic implications. Am J Phys Anthropol, Hominoid Evolution and Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New in press. York), pp 389–415. 5. Moya`-Sola` S, Ko¨ hler M, Alba DM, Casanovas-Vilar I, Galindo J (2004) Pierolapithecus 23. McCrossin ML, Benefit BR (1993) Recently recovered Kenyapithecus mandible and catalaunicus, a new Middle Miocene great ape from Spain. Science 306:1339–1344. its implications for great ape and human origins. Proc Natl Acad Sci USA 90:1962– 6. Andrews P (1992) Evolution and environment in the Hominoidea. 360:641–646. 1966. 7. Gu¨lec¸ E, Begun DR (2003) Functional morphology and affinities of the hominoid 24. Begun DR, Nargolwalla MC, Hutchinson MP (2006) Primate diversity in the Panonian mandible from C¸andir. Cour Forsch-Inst Senckenberg 240:89–112. Basin: In situ evolution, dispersal, or both? Beitr Pala¨ontol 30:43–56. 8. Kelley J, Andrews P, Alpagut B (2008) A new hominoid species from the Middle 25. Begun DR (2007) In Handbook of , eds Henke W, Tattersall I Miocene site of Pas¸alar, Turkey. J Hum Evol 54:455–479. (Springer, Heidelberg), pp. 921–977. 9. Rossie JB (2005) of the nasal cavity and paranasal sinuses in 26. Pilbrow V (2006) Lingual incisor traits in modern hominoids and an assessment of the and early Miocene African catarhines. Am J Phys Anthropol 126:250–267. utility for fossil hominoid . Am J Phys Anthropol 129:323–338. 10. Begun DR (2005) is east and Dryopithecus is west, and never the twain 27. Kelley J, Ward S, Brown B, Hill A, Duren DL (2002) Dental remains of Equatorius shall meet. Anthropol Sci 113:53–64. africanus from Kipsaramon, Tugen Hills, Baringo District, Kenya. J Hum Evol 42:39–62. 11. Smith TM, Martin LB, Leakey MG (2003) Enamel thickness microstructure and devel- 28. Begun DR (1992) Phyletic diversity and locomotion in primitive European hominids. opment in Afropithecus turkanensis. J Hum Evol 44:283–306. Am J Phys Anthropol 87:311–340. 12. Kunimatsu Y, et al. (2004) Maxillae and associated gnathodental specimens of Na- 29. Ishida H, Kunimatsu Y, Takano T, Nakano Y, Nakatsukasa M (2004) Nacholapithecus cholapithecus kerioi, a large-bodied hominoid from Nachola, northern Kenya. J Hum skeleton from the Middle Miocene of Kenya. J Hum Evol 46:69–103. Evol 46:365–400. 30. Bookstein FL (1991) Morphometric Tools for Landmark Data: Geometry and Biology 13. Pickford M (1986) Hominoids from the Miocene of and the phyletic position (Cambridge Univ Press, Cambridge, UK), 456 pp. of Kenyapithecus. Z Morphol Anthropol 76:177–130. 31. Rohlf FJ (2005) TpsDig, Digitize Landmarks and Outlines, Version 2.05 (Department of 14. Harrison TA (1992) Reassessment of the taxonomic and phylogenetic affinities of the Ecology and Evolution, State University of New York, Stony Brook, NY). fossil catarrhines of Fort Ternan, Kenya. Primates 33:501–522. 32. Rohlf FJ, Slice D (1990) Extensions of the Procrustes method for optimal superimposi- 15. Alpagut B, Andrews P, Martin L (1990) New hominoid specimens from the Middle tion of landmarks. Syst Zool 39:40–59. Miocene site at Pas¸alar, Turkey. J Hum Evol 19:397–422. 33. Rohlf FJ (2003) TpsRelw, Relative Warps Analysis, Version 1.36 (Department of Ecology 16. McCrossin ML, Benefit BR (1997) In Function, Phylogeny and Fossils: Miocene Hominoid and Evolution, State University of New York, Stony Brook, NY). Evolution and Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New York), pp 34. Bookstein FL (1996) In Advances in Morphometrics, eds Marcus LF, Corti M, Loy A, 327–362. Naylor GJP, Slice DE (Plenum, New York), pp 153–168. 17. Cameron DW (2004) Hominid Adaptations and (University of New South 35. Martin L (1985) Significance of enamel thickness in hominoid evolution. Nature Wales Press, Sydney), 235 pp. 314:260–263.

9606 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0811730106 Moya`-Sola`et al. Supporting Information

Moya`-Sola`et al. 10.1073/pnas.0811730106 SI Text netic relationships between all these taxa by classifying them all Systematic Framework. In Table S1 we provide a systematic into a single family Afropithecidae with 2 subfamilies (Keny- classification of living and fossil Hominoidea to the tribe level, apithecinae and Afropithecinae). by further including extant taxa and extinct genera discussed in The systematic scheme used here requires several nomencla- this paper. Hominoidea are defined as the group constituted by tural decisions, which deserve further explanation. The nomina Hylobatidae and Hominidae, plus all extinct taxa more closely Kenyapithecini and Kenyapithecinae are adopted instead of related to them than to Cercopithecoidea. Hominidae, in turn, Griphopithecinae and Griphopithecini (see also ref. 25) merely are defined as the group containing Ponginae and Homininae, because the former have priority. It is unclear why neither Begun plus all extinct forms more closely related to them than to (1) nor Kelley (2) specify the authorship of Griphopithecinae (or Hylobatidae. While this broad concept of Hominidae is currently Griphopithecidae), but, to our knowledge, the authorship of the used by many paleoprimatologists (e.g., refs. 1–2), the systematic latter nomina must be attributed to Begun (ref. 4, p. 232: Table position of primitive (or archaic) putative hominoids is far from 10.1), which therefore do not have priority over Kenyapithecinae clear (see below). Begun (3–5) employs the terms ‘‘Eohomi- Andrews, 1992. Griphopithecinae thus remains potentially valid noidea’’ and ‘‘Euhominoidea’’ to informally refer to hominoids only if Kenyapithecus (and Afropithecus,seebelow)areexcluded of primitive and modern aspect, respectively. These terms, from it. This notwithstanding, there has been some confusion however, are roughly equivalent to stem-lineage and crown- regarding the authorship of the nomen Kenyapithecinae. Both group hominoids, respectively, and are not further used here. Begun (1) and Ward and Duren (20) attribute its authorship to The systematic status of many Late Oligocene and Early- Leakey (26). However, the earliest usage of a suprageneric Middle Miocene fossil catarrhines, lacking both cercopithecoid nomen with Kenyapithecus as the type genus is attributable to synapomorphies and crown hominoid synapomorphies, has been Andrews (6), who erected it as a previously undescribed tribe, subject to different interpretations (6–8). Harrison (8) argues Kenyapithecini, in the same paper that he erected Afropithecini that most fossil ‘‘apes’’ from the Late Oligocene and Early (27). To our knowledge, Kenyapithecus and Afropithecus have not Miocene of Africa have not crossed the hominoid ‘‘cladistic been previously included into a single family with the exclusion threshold’’ and classifies them into 2 distinct superfamilies of Hominidae (as in ref. 20), but we have chosen the nomen (Dendropithecoidea and Proconsuloidea), which he considers to Afropithecidae (instead of Kenyapithecidae) because the former be successive sister taxa of stem catarrhines, more derived than has been already used at the family level—albeit with a different propliopithecoids and pliopithecoids, but presumably preceding meaning—by some previous workers (2, 5). If, as suggested in the cercopithecoid–hominoid split (8–12). On the other ex- this paper, there is a close phylogenetic relationship between treme, a few authors have considered that proconsuloids might Kenyapithecinae (in particular, the Kenyapithecini) and Hom- be stem hominids (13–15). Although the latter view is apparently inidae, Afropithecidae as conceived here would be paraphyletic. abandoned (16), most authors consider that Early Miocene Transferring the Kenyapithecinae into the Hominidae (25), forms, especially ,aremorecloselyrelatedtoextant however, would not solve this problem, since the remaining hominoids than to cercopithecoids (3, 6–7, 16–20). The system- Afropithecidae (including only the Afropithecinae) would re- atic scheme used here (Table S1)followsHarrison(8)in main paraphyletic in excluding the Kenyapithecinae. recognizing that proconsulids and dendropithecids are distinct can be transferred from one group or rank to another, but cannot clades, but considers that at least the former are stem hominoids. be completely eliminated unless Linnean ranks are aban- These putative stem hominoids lack crown hominoid synapo- doned—a view that is not advocated here. morphies, in particular, features functionally related to ortho- The Late Miocene genera Hispanopithecus and Ouranopithe- grady that are presumably homologous between hylobatids and cus are not classified here at the tribe level. Both genera have hominids. Yet stem hominoids already share with both hylo- been previously suggested to be either pongines (28) or homi- batids and hominids some facial (16) and several postcranial nines (4), but this issue is not definitively resolved and lies (17–18, 21) synapomorphies. Prominently, the lack of external outside the scope of this paper. Nevertheless, it is worth men- tail in Proconsul (17, 19, 21), albeit disputed by some authors tioning that Hispanopithecus was recently resurrected (29) for (22), is now firmly established (23) and has been further ascer- Late Miocene species previously included in Dryopithecus,so tained in the putative stem hominoid Nacholapithecus (24). that the latter genus is restricted to its type species, Dryopithecus Among putative stem hominoids, the position of Afropithecus fontani.Asaresult,thetribeDryopitheciniishereusedwitha and other related taxa is the most problematic. Harrison (8) different meaning from previous usages, to refer to Middle distinguishes a single family with 3 distinct sub- Miocene stem hominids that apparently do not belong to any of families (Proconsulinae, Nyanzapithecinae, and Afropitheci- the 2 crown-hominid subfamilies; this tribe includes Pierolapithe- nae), while other authors (20) take an opposite approach by cus, Dryopithecus s.s., and Anoiapithecus gen. nov., but most classifying their Afropithecinae (including Nacholapithecus and likely excludes Hispanopithecus.Giventheuncertainphyloge- Equatorius)withintheHominidae,andothers(2)considerthe netic relationships between the several dryopithecin genera, it is former to be a distinct family. Especially problematic is the currently unclear whether this tribe is paraphyletic or represents placement of Kenyapithecus and Griphopithecus:insomesys- acladeofstemEuropeanhominids. tematic schemes (20, 25), the latter taxa are classified into the subfamily Kenyapithecinae within the Hominidae; others (2) Results distinguish a subfamily Griphopithecinae (for Griphopithecus) Morphometric Analyses. ANOVA comparisons show that there within the Afropithecidae; and Begun reunites both Keny- are significant differences (P Ͻ 0.001; F ϭ 178.6) among several apithecinae and Griphopithecinae into a distinct family Gripho- extant catarrhines regarding the CFA (Table S2 and S3), with pithecidae (2) or combines these taxa into an informal grouping gorillas, colobines, and hylobatids displaying the highest values, (‘‘griphopiths’’) of stem hominoids (5). The systematic scheme which nevertheless generally do not surpass 60°. Living humans, followed in this paper (Table S1)recognizestheclosephyloge- on the contrary, differ from all of the remaining taxa (P Ͻ 0.001)

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 1 of 10 by the much higher CFA of the former, while extinct hominins ape to have ever displayed a colobine-like facial profile, to which display intermediate values. Most extinct catarrhines clearly fall it may have autapomorphically converged from an ancestral within the ranges of extant nonhuman cercopithecoids and condition more similar to that displayed by stem hominoids and hominoids, with the exception of Anoiapithecus.Thelattertaxa living cercopithecines. display values of CFA beyond the maximum value recorded in Squared distances based on the CVA discriminant scores, and extant nonhuman catarrhines, and Ϸ20° higher than other fossil computed for pairs of fossil individuals included (Table S5), apes, most closely resembling the values displayed by extinct indicate that Anoiapithecus is particularly far from the 2 other members of the genus Homo. Miocene hominoids from Spain included in the analysis (Piero- The canonical variate analysis (CVA) indicates that Anoia- lapithecus and Hispanopithecus); D. fontani could not be included pithecus displays a unique morphology, previously unknown in the analysis because of incomplete preservation, although a among living and fossil hominoids, which confirms the need to previous analysis of facial morphology based on new remains erect a previously undescribed genus. This analysis (Table S4 and from Abocador de Can Mata indicates a gorilla-like morphology Table S5)correctlyclassifies93%oftheoriginalcases,onlywith (29), which is thus quite different from the Anoiapithecus minor confusion between some chimpanzees and gorillas and condition. The results of the randomization approach further between very few colobines, cercopithecines, and hylobatids. confirm that differences between Anoiapithecus and other fossil Stem catarrhines, stem hominoids, and even the stem great ape individuals cannot be accommodated within the range of vari- Pierolapithecus most closely resemble cercopithecines, whereas ation of a single genus. When the , the , or all previously known putative crown hominids show a more the gorilla distributions of intrageneric individual pair differ- derived condition that closely resembles one of the several extant ences are used, the null hypothesis can be rejected with at least great ape genera (Table S5). Anoiapithecus differs from crown P Ͻ 0.05 with the single exception of Ankarapithecus.Thelatter hominids not only by the lack of facial concavity (as reflected by is the fossil individual closest to Anoiapithecus when all canonical CA1, which explains 66% of variance), but also by the highly axes are taken into account (Table S5), although both taxa verticalized (orthognathous) facial profile (as reflected by CA2, display a different facial profile—as shown by the highly diver- which explains 23% of variance). Anoiapithecus,inparticular, gent discriminant scores for CA1 and, especially, CA2 (Fig. displays a vertical alignment of glabella, nasion, rhinion, and 3A)—and cluster very far from one another (Fig. 3B). In any nasospinale in relation to the alveolar plane. Glabella and case, when the distribution is used, the null hypothesis rhinion are more anteriorly situated, whereas rhinion and na- can be rejected with P Ͻ 0.05 in all instances, including An- sospinale are slightly more posteriorly placed. Thus, in Anoia- karapithecus.WithregardtoPierolapithecus and Hispanopithe- pithecus,therhinionissituatedverycloseandonlyslightlymore cus,thenullhypothesiscanberejectedwithP Ͻ 0.001 in all anterior than the nasion. In regard to the latter, Anoiapithecus instances, i.e., irrespective of the distribution used. All this shows the opposite condition from Pierolapithecus,mostclosely evidence clearly indicates that differences between Anoiapithe- resembling hylobatids and colobines. In fact, Anoiapithecus cus and other fossil individuals cannot be interpreted as repre- clusters with colobines when the several canonical axes are taken senting the extremes of the range of variation within a single into account simultaneously. It is thus the only known fossil great taxon, so that the erection of a genus is fully justified.

1. Begun DR (2002) In The Primate Fossil Record, ed Hartwig WC (Cambridge Univ Press, 16. Rae TC (1999) Mosaic evolution in the origin of the Hominoidea. Folia Primatol Cambridge, UK), pp 339–368. 70:125–135. 2. Kelley J (2002) In The Primate Fossil Record, ed Hartwig WC (Cambridge Univ Press, 17. Kelley J (1997) In Function, Phylogeny and Fossils: Miocene Hominoid Evolution and Cambridge, UK), pp 369–384. Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New York), pp 173–208. 3. Begun DR, Ward CV, Rose MD (1997) In Function, Phylogeny and Fossils: Miocene 18. Rose MD (1997) In Function, Phylogeny and Fossils: Miocene Hominoid Evolution and Hominoid Evolution and Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New York), pp 79–100. York), pp 389–415. 19. Ward CV (1997) In Function, Phylogeny and Fossils: Miocene Hominoid Evolution and 4. Begun DR (2001) In Hominoid Evolution and Environmental Change in the Neogene Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New York), pp 101–130. of Europe. Volume 2. Phylogeny of the Neogene Hominoid Primates of Eurasia, eds 20. Ward SC, Duren DL (2002) In The Primate Fossil Record, ed Hartwig WC (Cambridge de Bonis L, Koufos G, Andrews P (Cambridge Univ Press, Cambridge, UK), pp 231–268. Univ Press, Cambridge, UK), pp 385–397. 5. Begun DR (2005) Sivapithecus is east and Dryopithecus is west, and never the twain 21. Ward CV, Walker A, Teaford MF (1991) Proconsul did not have a tail. J Hum Evol shall meet. Anthropol Sci 113:53–64. 21:215–220. 6. Andrews P (1992) Evolution and environment in the Hominoidea. Nature 360:641–646. 22. Harrison T (1998) Evidence for a tail in Proconsul heseloni. Am J Phys Anthropol 7. Fleagle JG (1999) Primate Adaptation and Evolution (Academic, San Diego), 2nd Ed, 26(Suppl):93–94. 608 pp. 23. Nakatsukasa M, et al. (2004) Tail loss in Proconsul heseloni. J Hum Evol 46:777–784. 8. Harrison T (2002) In The Primate Fossil Record, ed Hartwig WC (Cambridge Univ Press, 24. Nakatsukasa M, et al. (2003) Definitive evidence for tail loss in Nacholapithecus, an East Cambridge, UK), pp 311–338. African Miocene hominoid. J Hum Evol 45:179–186. 9. Harrison T (1987) The phylogenetic relationships of the early catarrhine primates: a 25. Cameron DW (2004) Hominid Adaptations and Extinctions (University of New South review of the current evidence. J Hum Evol 16:41–80. Wales Press, Sydney), 235 pp. 10. Harrison T (1988) A taxonomic revision of the small catarrhine primates from the early 26. Leakey LSB (1962) A new lower fossil primate from Kenya. Ann Mag Nat Hist Miocene of East Africa. Folia Primatol 50:59–108. 11. Harrison T, Rook L (1997) In Function, Phylogeny and Fossils: Miocene Hominoid 4(Ser 13):689–697. Evolution and Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New York), pp 27. Pickford M, Kunimatsu Y (2005) Catarrhines from the Middle Miocene (ca. 14.5 Ma) of 327–362. Kipsaraman, Tugen Hills, Kenya. Anthropol Sci 133:189–224. 12. Rossie JB, Simons EL, Gauld SC, Rasmussen DT (2002) Paranasal sinus anatomy of 28. Ko¨hler M, Moya`-Sola` S, Alba DM (2001) In Hominoid Evolution and Environmental Aegyptopithecus: Implications for hominoid origins. Proc Natl Acad Sci USA 99:8454– Change in the Neogene of Europe. Volume 2. Phylogeny of the Neogene Hominoid 8456. Primates of Eurasia, eds de Bonis L, Koufos G, Andrews P (Cambridge Univ Press, 13. Walker A, Teaford M (1989) The hunt for Proconsul. Sci Am 260:76–82. Cambridge, UK), pp 192–212. 14. Walker A (1997) In Function, Phylogeny and Fossils: Miocene Hominoid Evolution and 29. Moya`-Sola`S, et al. (2009) First partial face and upper dentition of the Middle Miocene Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New York), pp 209–224. hominoid Dryopithecus fontani from Abocador de Can Mata (Valle`s-Penede`s Basin, 15. Rae T (1997) In Function, Phylogeny and Fossils: Miocene Hominoid Evolution and Catalonia, NE Spain): Taxonomic and phylogenetic implications. Am J Phys Anthropol, Adaptation, eds Begun DR, Ward CV, Rose MD (Plenum, New York), pp 59–77. in press.

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 2 of 10 Fig. S1. Situation of Abocador de Can Mata (ACM). The old rubbish dump is indicated in yellow, whereas the area under exploitation and/or excavation is indicated in orange. The location of the classical sites of this area is indicated by circles, whereas the location of the published hominoid-bearing localities is indicated by a cranium. Three hominoid-bearing sites are geographically close (albeit at different stratigraphic horizons) at C3: C3-Aj and C3-Az, which have yielded remains of Dryopithecus fontani, and C3-Aj, which is the type locality of Anoiapithecus brevirostris gen. et sp. nov.; BCV1 is the type locality of Pierolapithecus catalaunicus. Abbreviations: BCV, Barranc de Can Vila; BDA, Bassa de Decantacio´d’Aigu¨es Pluvials; BDL, Bassa de Lixiviats; CCV, Camí de Can Vila; VIE, Vial Intern d’Explotacio´; C, Cel⅐la.

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 3 of 10 Fig. S2. Composite polarity stratigraphy of the ACM local series and correlation with the astronomically tuned geomagnetic polarity timescale ATNTS2004. The stratigraphic situation of the classical sites of Can Mata I and III, together with that of the published hominoid-bearing localities, is indicated. Stratigraphy is modified from ref. 5.

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 4 of 10 Table S1. Systematic classification of living and fossil Hominoidea at the tribe level, including all extant genera and extinct taxa included in this paper

Order Primates, Linnaeus, 1758 Semiorder Haplorrhini, Pocock, 1918 Suborder Anthropoidea, Mivart, 1864 (ϭ Simiiformes, Hoffstetter, 1974) Infraorder Catarrhini, É. Geoffroy Saint-Hilaire, 1812 Superfamily incertae sedis Family Dendropithecidae*, Harrison, 2002 Superfamily Hominoidea, Gray, 1825 Family Proconsulidae*, L.S.B. Leakey, 1963 Subfamily Proconsulinae*, L.S.B. Leakey, 1963 Genus Proconsul*, Hopwood, 1933 Subfamily Nyanzapithecinae*, Harrison, 2002 Genus Turkanapithecus*, R. E. Leakey and M. G. Leakey, 1986 Family Afropithecidae*, Andrews, 1992 Subfamily Afropithecinae*, Andrews, 1992 Tribe Afropithecini*, Andrews, 1992 Genus Afropithecus*, R. E. Leakey and M. G. Leakey, 1986 Genus Heliopithecus*, Andrews and Martin, 1987 Genus *, Gebo et al., 1997 Subfamily Kenyapithecinae*, Andrews, 1992 Tribe Kenyapithecini*, Andrews, 1992 Genus Kenyapithecus*, L. S. B. Leakey, 1962 Genus Griphopithecus*, Abel, 1902 Tribe Equatorini*, Cameron, 2004 Genus Equatorius*, Ward et al., 1999 Genus Nacholapithecus*, Ishida et al., 1999 Family Hylobatidae, Gray, 1870 Genus , Illiger, 1811 Family Hominidae, Gray, 1825 Subfamily incertae sedis Tribe Dryopithecini*, Gregory and Hellman, 1939 Genus Dryopithecus*, Lartet, 1856 Genus Pierolapithecus*, Moyà-Solà et al., 2004 Genus Anoiapithecus*, gen. nov. Tribe incertae sedis Genus Hispanopithecus*, Villalta and Crusafont, 1944 Genus Ouranopithecus*, de Bonis and Melentis, 1977 Subfamily Ponginae, Elliot, 1913 Tribe Pongini, Elliot, 1913 Genus Pongo, Lacépède, 1799 Genus Sivapithecus*, Pilgrim, 1910 Genus Ankarapithecus*, Ozansoy, 1957 Subfamily Homininae, Gray, 1825 Tribe , Frechkop, 1943 Genus Gorilla, I. Geoffroy Saint-Hilaire, 1853 Genus Pan, Oken, 1816 Tribe , Gray, 1825 Genus Homo, Linnaeus, 1758 Genus *, Dart, 1925 Genus *, Broom, 1938

*Extinct taxa.

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 5 of 10 Table S2. Descriptive statistics of the craniofacial angle (CFA) in extant genera and values for extinct taxa included in the analysis Taxon N Mean SD 95% CI Range

Macaca 55 46.8 4.3 45.6 47.9 35 56 Cercopithecus 16 52.7 5.1 50.0 55.4 37 61 Colobinae 26 55.7 5.1 53.7 57.8 48 65 Pongo 17 44.4 5.6 41.5 47.2 34 52 Hylobates s.l. 21 57.8 4.7 55.7 60.0 50 67 Pan 63 51.1 4.3 50.0 52.2 40 59 Gorilla 14 54.5 3.8 52.3 56.7 47 58 Homo 31 78.5 3.9 77.0 79.9 68 85 Papio 13 35.8 2.9 34.0 37.5 30 40 Anoiapithecus 1 72 Ankarapithecus 1 45 Proconsul 1 46 Pierolapithecus 1 43 Sivapithecus 1 52 Aegyptopithecus 2 43 0.0 43.0 43.0 43 43 Ouranopithecus 1 47 Afropithecus 1 36 Hispanopithecus 1 52 Turkanapithecus 1 46 1 49 Paranthropus 3 62.0 7.5 43.2 80.8 54 69 Australopithecus 2 66.0 0.0 66.0 66.0 66 66 Fossil Homo 4 71.5 6.4 61.3 81.7 65 77

N, sample size; SD, standard deviation; CI, confidence interval.

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 6 of 10 Table S3. ANOVA and Bonferroni results for comparisons of the craniofacial angle (CFA) among extant taxa Taxon Macaca Cercopithecus Colobinae Pongo Hylobates Pan Gorilla Homo

Cercopithecus 0.000 Colobinae 0.000 0.000 Pongo 0.000 1.000 0.000 Hylobates s.l. 1.000 0.000 0.000 0.000 Pan 0.000 0.026 0.000 1.000 0.000 Gorilla 0.000 1.000 0.000 0.001 0.000 0.000 Homo 0.000 1.000 0.000 1.000 0.000 1.000 0.424 Papio 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 Cercopithecus *** Colobinae *** NS Pongo NS *** *** Hylobates s.l. *** * NS *** Pan *** NS *** *** *** Gorilla *** NS NS *** NS NS Homo *** *** *** *** *** *** *** Papio *** *** *** *** *** *** *** ***

***, significant at P Ͻ 0.001; *, significant at P Ͻ 0.05; NS, nonsignificant.

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 7 of 10 Table S4. Main results of the canonical variate analysis (CVA) performed on the matrix of partial warp scores (PW), including the uniform component (UNI) Discriminant functions (canonical axes)

CA1 CA2 CA3 CA4 CA5 CA6

Eigenvalues 9.512 3.355 0.870 0.436 0.143 0.067 % of variance 66.1 23.3 6.0 3.0 1.0 0.5 Cumulative % 66.1 89.5 95.5 98.5 99.5 100.0 Canonical correlation 0.951 0.878 0.682 0.551 0.354 0.251

Standardized coefficients of the canonical discriminant functions CA1 CA2 CA3 CA4 CA5 CA6 X1-PW1 Ϫ0.162 0.391 Ϫ0.417 0.253 0.088 0.522 Y1-PW2 0.503 Ϫ0.185 0.046 0.405 Ϫ0.230 Ϫ0.106 X2-PW3 Ϫ0.098 Ϫ0.186 0.616 0.790 0.187 Ϫ0.123 Y2-PW4 0.442 Ϫ0.215 0.521 0.157 0.738 0.363 X3-PW5 0.136 Ϫ0.106 Ϫ0.125 Ϫ0.453 Ϫ0.336 0.423 Y3-PW6 Ϫ0.17 Ϫ0.099 Ϫ0.327 Ϫ0.146 Ϫ0.108 0.242 X4-PW7 Ϫ0.842 Ϫ0.232 0.502 0.056 0.162 0.348 Y4-PW8 Ϫ0.029 0.401 0.069 0.425 0.517 0.007 X5-UNI1 0.617 0.059 0.37 0.273 Ϫ0.288 0.707 Y5-UNI2 Ϫ0.214 0.573 0.841 Ϫ0.134 Ϫ0.353 Ϫ0.058

Functions at group centroids CA1 CA2 CA3 CA4 CA5 CA6 Cercopithecus 4.513 Ϫ1.819 0.261 1.059 0.300 Ϫ0.747 Colobinae 3.025 Ϫ3.100 0.228 Ϫ1.366 Ϫ0.185 0.041 Gorilla Ϫ2.898 0.554 Ϫ1.596 Ϫ0.770 1.160 Ϫ0.057 Hylobates s.l. 1.698 Ϫ2.631 Ϫ1.656 1.239 Ϫ0.055 0.505 Pan Ϫ4.017 Ϫ0.171 Ϫ0.189 0.041 Ϫ0.316 Ϫ0.131 Pongo Ϫ4.035 Ϫ2.131 3.175 0.592 0.659 0.359 Macaca 1.819 1.848 0.207 Ϫ0.004 Ϫ0.036 0.073 Discriminant scores for fossil taxa CA1 CA2 CA3 CA4 CA5 CA6 Afropithecus turkanensis 3.157 2.870 2.584 Ϫ0.566 Ϫ1.345 Ϫ0.574 Anoiapithecus brevirostris 0.942 Ϫ4.093 1.834 Ϫ1.603 0.750 Ϫ0.457 Hispanopithecus laietanus Ϫ5.002 0.657 Ϫ1.852 Ϫ0.981 Ϫ2.609 Ϫ0.077 Ouranopithecus macedoniensis Ϫ4.465 0.749 Ϫ1.860 Ϫ0.514 0.349 0.045 Sivapithecus indicus Ϫ7.581 Ϫ3.490 1.281 1.675 0.255 Ϫ2.144 Turkanapithecus kalakolensis 2.351 0.948 Ϫ1.142 Ϫ1.004 Ϫ0.450 Ϫ1.899 Victoriapithecus macinnesi 1.573 Ϫ1.636 3.830 Ϫ2.987 Ϫ3.589 Ϫ2.354 Proconsul heseloni 3.400 0.757 0.690 Ϫ0.558 Ϫ2.790 Ϫ0.130 Pierolapithecus catalaunicus Ϫ0.947 3.489 2.773 Ϫ0.810 Ϫ0.079 0.023 Aegyptopithecus zeuxis 4.279 Ϫ0.764 0.868 Ϫ0.673 Ϫ2.931 Ϫ1.547 Ae. zeuxis 3.741 1.020 1.497 0.525 Ϫ2.845 Ϫ2.297 Ankarapithecus meteai Ϫ2.343 Ϫ0.334 1.222 Ϫ1.732 Ϫ0.289 Ϫ0.259

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 8 of 10 Table S5. Classification results of the canonical variate analysis and squared Mahalanobis distance of Anoiapithecus to extant centroids and fossil taxa Classification of fossil taxa

Squared Squared Mahalanobis Predicted group Mahalanobis Predicted group (first) distance to centroid (second) distance to centroid

Afropithecus turkanensis Macaca 10.932 Cercopithecus 34.6 Anoiapithecus brevirostris Colobinae 9.082 Hylobates s.l. 24.539 Hispanopithecus laietanus Pan 10.726 Gorilla 18.75 Ouranopithecus macedoniensis Gorilla 3.296 Pan 4.618 Sivapithecus indicus Pongo 25.611 Pan 32.928 Turkanapithecus kalakolensis Macaca 7.971 Cercopithecus 20.44 Victoriapithecus macinnesi Colobinae 37.176 Macaca 52.733 Proconsul heseloni Macaca 11.859 Cercopithecus 20.601 Pierolapithecus catalaunicus Macaca 17.577 Pan 32.397 Aegyptopithecus zeuxis Cercopithecus 15.613 Colobinae 17.98 Ae. zeuxis Macaca 19.838 Cercopithecus 22.766 Ankarapithecus meteai Pan 7.985 Gorilla 12.108

Classification of original cases (extant taxa) Cercopithecus Colobinae Gorilla Hylobates s.l. Pan Pongo Macaca Cercopithecus 14 (93.4%) 1 (6.7%) Colobinae 1 (4.0%) 24 (96.0%) Gorilla 15 (100%) Hylobates s.l. 1 (5.9%) 16 (94.1%) Pan 10 (15.6%) 54 (84.4%) Pongo 11 (100%) Macaca 1 (1.1%) 1 (1.1%) 1 (1.1%) 92 (96.8%)

Squared Mahalanobis distance of Anoiapithecus to extant centroids and fossil taxa

Cercopithecus Colobinae Gorilla Hylobates s.l. 27.77 9.08 49.13 24.54 Pan Pongo Macaca Afropithecus 48.01 35.91 42.17 59.43 Hispanopithecus Ouranopithecus Sivapithecus Turkanapithecus 83.29 67.92 87.15 40.13 Victoriapithecus Proconsul Pierolapithecus Aegyptoptihecus 34.76 44.60 63.48 38.75 Aegyptoptihecus Ankarapithecus 55.93 26.43

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 9 of 10 Table S6. Composition of the extant comparative sample employed in the morphometric analyses Genus N (craniofacial angle) N (geometric morphometrics)

Cercopithecus 16 15 Colobus 10 9 Gorilla 14 15 Homo 31 Hylobates s.l. 21 17 Macaca 55 95 Pan 63 64 Papio 13 Pongo 17 11 Presbytis 12 12 Procolobus 44

N, sample size.

Moya`-Sola`et al. www.pnas.org/cgi/content/short/0811730106 10 of 10