Evidence for an Asian origin of stem anthropoids

Richard F. Kay1 Department of Evolutionary Anthropology, Duke University, Durham, NC 27708-03083

n PNAS, Chaimanee et al. (1) report Genetic, embryological, and anatomical We are not there yet. Recent comprehen- a previously undescribed species of evidence demonstrates that the sister sive phylogenetic analyses stemming from I primate, Afrasia, from the late Middle group of Anthropoidea is the south Asian virtually the same datasets yield somewhat Eocene of Burma. They identify tarsier, with the two forming the crown different cladograms that reflect sensitivity Afrasia as the sister taxon to the African group Haplorhini (6–8). The other clade of to which taxa are included in the analysis genus Afrotarsius but slightly more primitive extant primates is the lemurs and lorises, and which sets of analytical assumptions are than it and allied with stem Anthropoidea called Strepsirrhini. Eocene Holarctic selected. Pertinent to the biogeographic of south Asia. Anthropoidea is the taxo- Omomyoidea are generally considered as conclusions of Chaimanee et al. (1), Seiffert nomic group that today includes New and stem haplorhines, although the precise et al. (11) conclude that Afrotarsius cha- Old World monkeys, apes, and humans. If relationship of omomyoids to tarsiers and trathi [a younger species than the one that upheld, the biogeographic significance of anthropoids is uncertain (8). Tarsius often Chaimanee et al. (1) describe] is an African these results is profound: If Afrasia and is considered to be a relictual omomyoid tarsioid. If Seiffert et al. (11) are correct, Afrotarsius are as closely related as Chai- in south Asia. Afrasia could be a tarsier relative, and it manee et al. (1) propose, there must have may be that Afrasia documents a dispersal been a late Middle Eocene geographic An Asian origin for stem of Asian tarsioids to Africa. Topologies are connection between the primate faunas of unstable at the basal nodes of these phy- Asia and Africa. Further support for in- anthropoids is a plausible logenetic trees, as indicated by a Bremer tercontinental connections between south support of one or two steps at key nodes of Asia and Africa is found among other scenario based on the the reconstructed clades (Bremer support is the number of extra steps needed to contemporaneous mammalian groups, in- construct a tree where that clade is no cluding anomaluroid and hystricognathous present paleontological longer present). rodents (2). More provocatively, Chaima- The phylogenetic position of later nee et al. (1) consider the south Asian late evidence but is by no Eocene amphipithecids of Asia also is the Middle Eocene family Amphipithecidae means certain. subject of considerable debate. Mandibular to be a stem catarrhine clade and suggest and dental similarities (17) as well as the that Catarrhini (the group of Old World structure of an isolated talus (18) suggest anthropoids) also originated in south Asia It is generally held that stem anthro- amphipithecids are anthropoids. Others and dispersed to Africa. poids arose in Asia and that one or several allocate a strepsirrhine-like calcaneus A review of fossil evidence lends cre- anthropoid groups later migrated to Africa and humerus from Burmese sites to am- dence to the phylogenetic and biogeo- sometime in the Middle or Late Eocene phipithecids and conclude that amphipi- graphic scenario of Chaimanee et al. (1). (9). The weight of current fossil evidence thecids are strepsirrhines (19). Even At the same time, it must be acknowledged supports this Asian origin hypothesis. The accepting the specimen allocations (I do) that gaps in the Paleogene primate fossil earliest member of the tarsier family of Chaimanee et al. (1), the Bremer sup- record of south Asia and Africa allow for (Tarsiidae) come from the Middle Eocene port for a stem catarrhine placement of other plausible interpretations. Support for of Asia at about 45 Ma (Xanthorhysis) (10). amphipithecids is very weak, which per- their scenario is not made any stronger by Although African late Middle Eocene haps explains why the family has variously the fact that Afrasia djijidae and Afrotarsius and Early Oligocene Afrotarsius is said by been identified as stem anthropoids (11, libycus are known only from a few cheek some to be a tarsioid (11, 12), others 20) or placed in an unresolved trichotomy teeth. For that matter, key anatomical conclude that is an early anthropoid (13, with platyrrhines and catarrhines (16). evidence is lacking or incomplete for 14). Stem anthropoids called Eosimiidae In any case, in figure 3 in ref. 1, amphipi- other Asian stem anthropoids (e.g., in the first appear in the Asian Middle Eocene thecids are nested within an otherwise structure of the posterior wall of the orbit at ∼45 Ma, and larger-bodied late Middle African clade consisting of oligopithecids, and middle ear) that would make their Eocene Amphipithecidae also are Asian propliopithecids, parapithecids, and anthropoid status more certain. anthropoids and even possibly stem proteopithecids. Such a topology suggests catarrhines (15, 16). Although there are that amphipithecids migrated out of Africa Challenges of Early Anthropoid some hints, there is no convincing evi- rather than into it. If catarrhines originated Phylogeny dence for the existence of anthropoids in in Asia, their sister group, platyrrhines, The earliest undisputed anthropoids, Africa before the late Middle Eocene, must also have done so, which seems Proteopithecidae, Parapithecidae, Oligo- ∼38Ma.However,doesthe(debated) unlikely for geographic reasons. pithecidae, and Propliopithecidae, come restriction of tarsioids to Asia and the Several other fragmentary fossil remains from the later Eocene and Early Oligo- finding that eosimiids first appear in the (isolated teeth) suggest a considerably cene of North Africa. They had nearly all Middle Eocene of Asia, and only later deeper history for anthropoids in Africa the anatomical hallmarks of extant an- in Africa, indicate an Asian origin for or Asia. Some analyses support the hy- thropoids, especially resembling living stem Anthropoidea? Likewise, are pothesis that Altiatlasius from the late New World monkeys in size, morphology, amphipithecids stem catarrhines, and if and reconstructions of their behavior, so, did catarrhines have an Asian origin being frugivorous above-branch arboreal as well? Author contributions: R.F.K. wrote the paper. quadrupeds that were highly social and To evaluate these biogeographic The author declares no conflict of interest. daytime-active with significant reliance on hypotheses, we must first have a highly See companion article on page 10293. the sense of vision (3–5). resolved phylogeny of Eocene primates. 1E-mail: [email protected].

10132–10133 | PNAS | June 26, 2012 | vol. 109 | no. 26 www.pnas.org/cgi/doi/10.1073/pnas.1207933109 Downloaded by guest on September 29, 2021 COMMENTARY

Paleocene of North Africa is a stem an- tarsiers was early Paleocene or even late conclusion that the two are sister taxa thropoid (11, 20, 21), whereas others Cretaceous (6, 25). and indicates a cross-Tethian dispersal consider it to be an omomyoid (22) or event in the late Middle Eocene. On the a plesiadapoid (23). Bajpai et al. (20) Biogeographic Hypotheses other hand, 20 or more million years proposed that Anthrasimias from India is An Asian origin for stem anthropoids is may separate Asian Middle Eocene stem an eosimiid anthropoid extending the a plausible scenario based on the present anthropoids from the date of the last Asian fossil record of anthropoids back to paleontological evidence but is by no common ancestor of anthropoids and the Early Eocene. However, Rose et al. means certain. Whether anthropoid pri- tarsiers. In addition, if either Altiatlasius (24) suggested that these isolated teeth mates first differentiated in Africa or or Anthrasimias is a stem anthropoid, could belong to the adapoid Marcgodino- Asia remains uncertain because the fossil repeated primate trans-Tethian tius, although admitting that some of the record of the Paleogene of south Asia and dispersal events could have occurred in characters of the hypodigm of Anthrasimias Africa is poorly known and because the either direction. and also some isolated ankle bones from Tethys seaway between the two continents Finally, even if amphipithecids are the same fossil site resemble eosimiids in was breached by many small mammals catarrhines, an Asian origin for Catarrhini some respects. Neither Altiatlasius nor during the Paleogene. Irrespective of seems unlikely because they are nested Anthrasimias can be ruled out of conten- whether the afrotarsiids Afrasia and within an otherwise African clade. Is it not tion as a stem anthropoid on the basis of Afrotarsius are related to eosimiids or to more parsimonious to assume that amphi- geological age because the proposed date tarsioids, the close correspondence pithecids, if they are catarrhines, had an of cladogenesis between anthropoids and between the two genera supports the African origin?

1. Chaimanee Y, et al. (2012) Late Middle Eocene primate 10. Beard KC (1998) A new genus of Tarsiidae (Mammalia: Anthropoid Origins: New Visions, eds Ross CF, Kay RF from Myanmar and the initial anthropoid colonization of Primates) from the middle Eocene of Shanxi Province, (Kluwer/, Plenum, New York), pp 91–135. Africa. Proc Natl Acad Sci USA 109:10293–10297. China, with notes on the historical biogeography of 18. Marivaux L, et al. (2003) The anthropoid status of a pri- 2. Jaeger J-J, et al. (2010) New rodent assemblages from tarsiers. Bulletin of the Carnegie Museum of Natural mate from the late middle Eocene Pondaung Forma- the Eocene Dur At-Talah escarpment (Sahara of central History 34:260–277. tion (Central Myanmar): Tarsal evidence. Proc Natl – Libya): Systematic, biochronological, and palaeobiogeo- 11. Seiffert ER, et al. (2005) Basal anthropoids from Egypt Acad Sci USA 100:13173 13178. graphical implications. Zool J Linn Soc 160(1):195–213. and the antiquity of Africa’s higher primate radiation. 19. Ciochon RL, Gingerich PD, Gunnell GF, Simons EL (2001) 3. Kay RF, Simons EL (1980) The ecology of Oligocene Science 310:300–304. Primate postcrania from the late middle Eocene of – African Anthropoidea. Int J Primatol 1(1):21–37. 12. Simons EL, Bown TM (1985) Afrotarsius chatrathi, first Myanmar. Proc Natl Acad Sci USA 98:7672 7677. 20. Bajpai S, et al. (2008) The oldest Asian record of Anthro- 4. Fleagle JG, Kay RF, Simons EL (1980) Sexual dimor- tarsiiform primate (?Tarsiidae) from Africa. Nature poidea. Proc Natl Acad Sci USA 105:11093–11098. phism in early anthropoids. Nature 287:328–330. 313:475–477. 21. Beard KC (2006) Mammalian biogeography and anthro- 5. Kirk EC, Kay RF (2004) The evolution of high visual 13. Jaeger J-J, et al. (2010) Late middle Eocene epoch of poid origins. Primate Biogeography, eds Lehman SM, acuity in the Anthropoidea. Anthropoid Origins: New Libya yields earliest known radiation of African Fleagle JG (Springer, New York), pp 439–467. Visions, eds Ross CF, Kay RF (Kluwer/Plenum, New anthropoids. Nature 467:1095–1098. 22. Sigé B, Jaeger J-J, Sudre J, Vianey-Liaud M (1990) Al- York), pp 539–602. 14. Fleagle JG, Kay RF (1987) The phyletic position of the tiatlasius koulchii n. gen. et sp., primate omomyidé du 6. Perelman P, et al. (2011) A molecular phylogeny of Parapithecidae. J Hum Evol 16:483–532. Paléocène supérieur du Moroc, et les origines des Eu- 15. Beard KC, Wang B, Dawson M, Huang X, Tong Y (1996) living primates. PLoS Genet 7:e1001342. primates. Paleontographica 212:1–24. 7. Martin RD (1990) Primate Origins and Evolution, a Earliest complete dentition of an anthropoid primate 23. Hooker JJ, Russell DE, Phélizon A (1999) A new family Phylogenetic Reconstruction (Princeton Univ Press, from the late middle Eocene of Shanxi Province, China. of Plesiadapiformes (Mammalia) from the Old World – Princeton). Science 272:82 85. lower Paleogene. Palaeontology 42:377–407. 8. Williams BA, Kay RF, Kirk EC (2010) New perspectives 16. Beard KC, et al. (2009) A new primate from the Eocene 24. Rose KD, et al. (2009) Early Eocene primates from Gu- on anthropoid origins. Proc Natl Acad Sci USA 107: Pondaung Formation of Myanmar and the monophyly jarat, India. J Hum Evol 56:366–404. 4797–4804. of Burmese amphipithecids. Proc Biol Sci 276: 25. Steiper ME, Seiffert ER (2012) Evidence for a conver- 9. Beard KC (2002) Basal anthropoids. The Primate Fossil 3285–3294. gent slowdown in primate molecular rates and Record, ed Hartwig WC (Cambridge Univ Press, Cam- 17. Kay RF, Williams BA, Ross CF, Takai M, Shigehara N its implications for the timing of early primate evo- bridge, UK), pp 133–150. (2004) Anthropoid origins: a phylogenetic analysis. lution. Proc Natl Acad Sci USA 109:6006–6011.

Kay PNAS | June 26, 2012 | vol. 109 | no. 26 | 10133 Downloaded by guest on September 29, 2021