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Reassessment of the Phylogenetic Relationships of the Late Miocene Apes Hispanopithecus and Rudapithecus Based on Vestibular Morphology

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Reassessment of the Phylogenetic Relationships of the Late Miocene Apes Hispanopithecus and Rudapithecus Based on Vestibular Morphology Reassessment of the phylogenetic relationships of the late Miocene apes Hispanopithecus and Rudapithecus based on vestibular morphology Alessandro Urciuolia,1, Clément Zanollib, Sergio Almécijaa,c,d, Amélie Beaudeta,e,f,g, Jean Dumoncelh, Naoki Morimotoi, Masato Nakatsukasai, Salvador Moyà-Solàa,j,k, David R. Begunl, and David M. Albaa,1 aInstitut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, 08193 Barcelona, Spain; bUniv. Bordeaux, CNRS, MCC, PACEA, UMR 5199, F-33600 Pessac, France; cDivision of Anthropology, American Museum of Natural History, New York, NY 10024; dNew York Consortium in Evolutionary Primatology, New York, NY 10016; eDepartment of Archaeology, University of Cambridge, Cambridge CB2 1QH, United Kingdom; fSchool of Geography, Archaeology, and Environmental Studies, University of the Witwatersrand, Johannesburg, WITS 2050, South Africa; gDepartment of Anatomy, University of Pretoria, Pretoria 0001, South Africa; hLaboratoire Anthropology and Image Synthesis, UMR 5288 CNRS, Université de Toulouse, 31073 Toulouse, France; iLaboratory of Physical Anthropology, Graduate School of Science, Kyoto University, 606 8502 Kyoto, Japan; jInstitució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain; kUnitat d’Antropologia, Departament de Biologia Animal, Biologia Vegetal i Ecologia, Universitat Autònoma de Barcelona, 08193 Barcelona, Spain; and lDepartment of Anthropology, University of Toronto, Toronto, ON M5S 2S2, Canada Edited by Justin S. Sipla, University of Iowa, Iowa City, IA, and accepted by Editorial Board Member C. O. Lovejoy December 3, 2020 (received for review July 19, 2020) Late Miocene great apes are key to reconstructing the ancestral Dryopithecus and allied forms have long been debated. Until a morphotype from which earliest hominins evolved. Despite con- decade ago, several species of European apes from the middle sensus that the late Miocene dryopith great apes Hispanopithecus and late Miocene were included within this genus (9–16). laietanus (Spain) and Rudapithecus hungaricus (Hungary) are However, discoveries at the middle Miocene composite section closely related (Hominidae), ongoing debate on their phylogenetic of Abocador de Can Mata (6, 17–20) prompted the recognition relationships with extant apes (stem hominids, hominines, or pon- that the late Miocene species belong to one or more different gines) complicates our understanding of great ape and human genera distinct from Dryopithecus (2, 3, 6, 7, 18, 21–26): Hispa- evolution. To clarify this question, we rely on the morphology of nopithecus from Spain and Rudapithecus from Hungary, the the inner ear semicircular canals, which has been shown to be latter formerly considered a subgenus of the former by some ANTHROPOLOGY phylogenetically informative. Based on microcomputed tomogra- authors (6, 18, 22). phy scans, we describe the vestibular morphology of Hispanopi- Together with Dryopithecus and other middle to late Miocene thecus and Rudapithecus, and compare them with extant taxa (17, 19, 27), Hispanopithecus and Rudapithecus are currently hominoids using landmark-free deformation-based three- classified in a subfamily (Dryopithecinae) (6, 20, 26) or tribe dimensional geometric morphometric analyses. We also provide (Dryopithecini) (3, 7, 21) of their own, distinct from pongines. critical evidence about the evolutionary patterns of the vestibular Both taxa possess a hominid-like cranial morphology (6, 11–13, apparatus in living and fossil hominoids under different phyloge- 21, 25, 28, 29), as shown by the high zygomatic root, reduced netic assumptions for dryopiths. Our results are consistent with midfacial prognathism, lack of subarcuate fossa, deep glenoid the distinction of Rudapithecus and Hispanopithecus at the genus rank, and further support their allocation to the Hominidae based Significance on their derived semicircular canal volumetric proportions. Com- pared with extant hominids, the vestibular morphology of Hispa- Reconstructing the phylogenetic relationships of extinct apes is nopithecus and Rudapithecus most closely resembles that of challenging due to their fragmentary fossil record and the re- African apes, and differs from the derived condition of orangu- current independent evolution of morphological features. tans. However, the vestibular morphologies reconstructed for Given the relevance of the phylogenetic signal of the bony the last common ancestors of dryopiths, crown hominines, and labyrinth, here we assess the phylogenetic affinities of the late crown hominids are very similar, indicating that hominines are Miocene great apes Hispanopithecus and Rudapithecus by plesiomorphic in this regard. Therefore, our results do not conclu- studying their inner ear morphology. Our results are consistent sively favor a hominine or stem hominid status for the with the distinct generic status of these dryopiths, which fur- investigated dryopiths. ther differ from the derived condition of orangutans and most closely resemble African apes. However, the latter appear inner ear | semicircular canals | evolution | fossil apes | Hominidae largely primitive (similar to the last common ancestor of great apes and humans). Hence, our results do not conclusively favor ominoids (apes and humans) originated in Africa during the a closer relationship with African apes as opposed to great HOligocene (1) but subsequently dispersed into Eurasia, apes as a whole. giving rise to an impressive radiation during the middle and late Miocene (2, 3). Thus, while extant hominoids include only two Author contributions: A.U., S.M.-S., D.R.B., and D.M.A. designed research; A.U. and C.Z. moderately diverse families—hylobatids (gibbons and siamangs) performed research; A.U., C.Z., A.B., J.D., N.M., M.N., and D.R.B. contributed new re- — agents/analytic tools; A.U., C.Z., S.A., A.B., J.D., and D.M.A. analyzed data; and A.U., and hominids (great apes and humans) the panoply of extinct C.Z., and D.M.A. wrote the paper. genera recorded during the Miocene still defies classification The authors declare no competing interest. into a coherent systematic scheme. Other than the late Miocene — This article is a PNAS Direct Submission. J.S.S. is a guest editor invited by the Oreopithecus which might be a late-occurring stem hominoid Editorial Board. — (4, 5) there is consensus that most Eurasian large-bodied Published under the PNAS license. hominoids are members of the great-ape-and-human clade 1To whom correspondence may be addressed. Email: [email protected] or david. (Hominidae) (2, 3, 6). While most Asian extinct great apes, such [email protected]. as Sivapithecus, are considered to be more closely related to the This article contains supporting information online at https://www.pnas.org/lookup/suppl/ orangutan clade (Ponginae) than to African apes and humans doi:10.1073/pnas.2015215118/-/DCSupplemental. (Homininae) (2, 6–8), the phylogenetic affinities of European Published January 25, 2021. PNAS 2021 Vol. 118 No. 5 e2015215118 https://doi.org/10.1073/pnas.2015215118 | 1of12 Downloaded by guest on September 24, 2021 fossa, and prominent entoglenoid process. However, there is no favoring a European origin and subsequent back-to-Africa dis- consensus regarding the phylogenetic position of this group— persal for the African and human clade (2, 3, 15, 24, 25). Dis- being either considered stem hominids (6, 19, 30), stem homi- agreements and uncertainties about the phylogenetic position of nines (2, 3, 14, 16, 25), or even pongines (10, 28, 29)—which may extinct apes are persistent, and stem from a combination of be informally referred to as “dryopiths.” Resolving the phylo- factors, including the incomplete and fragmentary hominoid genetic position of dryopiths has important implications for the fossil record, the decimated current diversity of the group, and evolution of the great ape and human clade, since their pur- pervasive homoplasy coupled with mosaic evolution (6, 23, ported hominine status has led to paleobiogeographic scenarios 31–35). A Rudapithecus RUD 77L B Rudapithecus RUD 77R C Rudapithecus RUD 200 D Hispanopithecus IPS18000 E Oreopithecus F Nacholapithecus G Hoolock H Symphalangus I Hylobates J Pongo K Gorilla L Pan M Homo Fig. 1. The vestibular apparatus morphology of R. hungaricus (A–C), H. laietanus (D), fossil hominoids (E and F), and individuals from extant hominoid genera (G–M) as depicted by renderings of the 3D models. From left to right, in posterolateral, superior, and posteromedial views: (A) R. hungaricus (RUD 77L); (B) R. hungaricus (RUD 77R); (C) R. hungaricus (RUD 200); (D) H. laietanus (IPS18000); (E) Oreopithecus bambolii (BAC 208); (F) N. kerioi (BG 42744); (G) Hoolock hoolock (AMNH.M 83425); (H) Symphalangus syndactylus (AMNH.M 106583); (I) Hylobates lar (MCZ 41424); (J) Pongo sp.(IPS10647); (K) Gorilla gorilla (AMNH.M 167338); (I) Pan troglodytes (AMNH.M 51204); (M) Homo sapiens (F 04). (Scale bars, 5 mm.) 2of12 | PNAS Urciuoli et al. https://doi.org/10.1073/pnas.2015215118 Reassessment of the phylogenetic relationships of the late Miocene apes Hispanopithecus and Rudapithecus based on vestibular morphology Downloaded by guest on September 24, 2021 The morphology of the semicircular canals (SCs), which partly humans (Fig. 1M), while it is slightly more rounded in RUD 200 constitute the inner ear’s bony labyrinth, has been classically (Fig. 1C). In both RUD 77 and RUD 200, the posterior and related to locomotion (36–42). However, several studies have lateral canals approximately define a
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