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Science Journals — AAAS RESEARCH ◥ differ from those of Wailekia and Kyitchaungia RESEARCH ARTICLES in having lingually open trigonids with proto- conid and metaconid more closely approximated and talonids bearing more trenchant cristids. PRIMATE EVOLUTION UppermolarsdifferfromthoseofGuangxilemur in having more prominent parastyles and pre- and postprotocristae joining the bases of the Oligocene primates from China reveal paracone and metacone, respectively, rather than merging with the pre- and postcingula. Upper molars with weaker buccal cingulum and incom- divergence between African and plete mesostyle, in contrast to Guangxilemur tongi. Lower molars differ from those of Guang- Asian primate evolution xilemur singsilai in having lingually open trig- onids and deeper, more extensive valley separating Xijun Ni,1,2* Qiang Li,1,2 Lüzhou Li,1 K. Christopher Beard3,4 entoconid and hypoconulid. Differs from Miocene 4 sivaladapids in lacking fully molariform P4 and P Profound environmental and faunal changes are associated with climatic deterioration and having upper molars with distinct pericone during the Eocene-Oligocene transition (EOT) roughly 34 million years ago. Reconstructing and hypocone cusps and pre- and postprotocris- how Asian primates responded to the EOT has been hindered by a sparse record of tae joining bases of paracone and metacone. Oligocene primates on that continent. Here, we report the discovery of a diverse primate Etymology: Generic name recognizes the geo- fauna from the early Oligocene of southern China. In marked contrast to Afro-Arabian graphic provenance of this taxon and its adapi- Downloaded from Oligocene primate faunas, this Asian fauna is dominated by strepsirhines. There appears to form affinities. be a strong break between Paleogene and Neogene Asian anthropoid assemblages. Asian Yunnanadapis folivorus sp. nov. Holotype: and Afro-Arabian primate faunas responded differently to EOT climatic deterioration, IVPP V22702, left dentary fragment preserving indicating that the EOT functioned as a critical evolutionary filter constraining the the crowns of C1-M3 (Fig. 1A and supplementary subsequent course of primate evolution across the Old World. materials). Horizon and locality:EarlyOligo- cene Lijiawa fossil site, upper part of Caijiachong Formation, Yuezhou Basin, Yunnan Province, China. http://science.sciencemag.org/ rimates are among the most thermophilic primates has been hindered by geographic and Diagnosis: Smaller than Yunnanadapis impera- and hence environmentally sensitive of all temporal biases in the Asian fossil record. Eocene tor.P3 without buccal cingulid, in contrast to Y. mammals. As a result, both the geographic primates have been sporadically reported from imperator.P4 differs from that of Y. imperator in P distribution and macroevolutionary pat- northern China and Mongolia (10–12), but Eocene having much weaker buccal cingulid and hypo- terns shown by fossil primates are strongly primatesaremorediverseandabundantinsouth- conidandcristidobliquamorelingualinposition, mediated by shifting climatic conditions during ern Asia, where the Oligocene record is generally yielding deeper hypoflexid and narrower talonid the Cenozoic. Dramatic range expansions, such absent (13, 14). With the sole exception of the late basin. Etymology: Trivial name reflects the likely as the dispersal of the earliest primates from early Oligocene Paali Nala locality in the Bugti dietary adaptations of this species. their Asian birthplace into North America and Hills of Pakistan (15–17), Oligocene primates are Yunnanadapis imperator sp. nov. Holotype: Europe during the Paleocene-Eocene Thermal unknown in Asia. This very limited record of IVPP V22706, right P (Fig. 1B and supplemen- 4 Maximum, coincided with intervals of extreme Asian Oligocene primates has made it difficult to tary materials). Horizon and locality:Early on October 25, 2017 global warmth (1, 2). In contrast, episodes of assess the impact of EOT environmental changes Oligocene Lijiawa fossil site, upper part of Cai- cooler, drier climatic conditions such as that on Asian primate evolution. Here, we describe a jiachong Formation, Yuezhou Basin, Yunnan characterizing the Eocene-Oligocene transition diverseassemblageoffossilprimatesfromthe Province, China. Diagnosis:LargerthanYun- (EOT) resulted in continental-scale extinction of early Oligocene of Yunnan Province in southern nanadapis folivorus.P3 with strong buccal cin- primates on landmasses that lacked direct geo- China that helps to fill this gap in the record of gulid, in contrast to Y. folivorus.P4 differs from graphic access to low-latitude refugia (3). Pri- Asian primate evolution. that of Y. folivorus in having much stronger mates were extirpated at or near the EOT in North We collected the primate fossils reported here buccal cingulid and hypoconid and cristid obli- America and Europe, but Afro-Arabian primate via careful excavation and screen-washing at the qua more buccal in position, yielding shallower faunas dominated by anthropoids continued to Lijiawa fossil site in Yunnan, which has yielded hypoflexid and wider talonid basin. Etymology: radiateduringtheOligoceneandNeogene(4–7). more than 10 mammal taxa that indicate an early Latin “imperator” (commander), in allusion to In northern China and Mongolia, mammalian Oligocene age (supplementary materials) (18). the large size of this species. faunal turnover across the EOT was pervasive Primates Linnaeus, 1758; Strepsirhini Geoffroy, Laomaki yunnanensis gen. et sp. nov. Holo- enough to be compared with the European Grande 1812; Adapiformes Hoffstetter, 1977; Sivaladapi- type:IVPPV22708,rightmaxillafragmentpre- Coupure, and this abrupt change in Asian mam- dae Thomas and Verma, 1979; Yunnanadapis serving M1-3 (Fig. 1C and supplementary materials). mal faunas has been designated the Mongolian gen. nov. Type species: Yunnanadapis folivorus Horizon and locality: Early Oligocene Lijiawa Remodeling (8, 9). However, assessing the im- sp. nov. Included species:Thetypespeciesand fossil site, upper part of Caijiachong Formation, pact of EOT climatic deterioration on early Asian Yunnanadapis imperator sp. nov. Diagnosis: Yuezhou Basin, Yunnan Province, China. Diag- Differs from Paukkaungia, Hoanghonius,and nosis: Differs from all sivaladapids aside from Rencunius in having more nearly molariform P4 Rencunius in having strongly developed conules 1 4 4 4 Key Laboratory of Vertebrate Evolution and Human Origins, and P (P remains unknown in Paukkaungia). on upper molars. P4 and P lack substantial mo- Institute of Vertebrate Paleontology and Paleoanthropology Lower molars further differ from those of Pauk- larization, in contrast to Yunnanadapis and Mio- (IVPP), Chinese Academy of Sciences, 142 Xi Zhi Men Wai kaungia, Hoanghonius,andRencunius in having cene sivaladapids. Upper and lower molars differ Street, Beijing, 100044, China. 2Chinese Academy of Sciences (CAS) Center for Excellence in Tibetan Plateau less cuspidate paraconids and more angular hy- from those of Rencunius and Paukkaungia in Earth Sciences, Beijing, 100101, China. 3Biodiversity Institute, poconids that are relatively mesial in position, having highly crenulated enamel, taller and more University of Kansas, 1345 Jayhawk Boulevard, Lawrence, KS so that the cristid obliqua is shorter than the pyramidal cusps/cuspids, and more trenchant 4 66045-7561, USA. Department of Ecology and Evolutionary postcristid. Upper molars further differ from crests/cristids. Upper molars are more transverse Biology, University of Kansas, 1345 Jayhawk Boulevard, Lawrence, KS 66045-7561, USA. those of Hoanghonius and (especially) Rencu- than those of Rencunius, and upper molar con- 4 *Corresponding author. Email: [email protected] nius in lacking distinct conules. Lower molars ules are pyramidal rather than bulbous. P bears SCIENCE sciencemag.org 6MAY2016• VOL 352 ISSUE 6286 673 RESEARCH | RESEARCH ARTICLES a tiny hypocone, in contrast to that of Rencunius. to those of Bugtilemur and Muangthanhinius,in from Eocene Tarsius eocaenus and modern Tar- Etymology: Generic name derives from the which these structures are obliquely oriented so sius pumilus. Differs from extant tarsiids and Mandarin “lao” (old) and the Malagasy “maky” that metaconid is located distolingual to proto- Miocene Hesperotarsius in having well-developed (lemur). Trivial name reflects the geographic prov- conid. Upper molars differ from those of Bugtilemur conules and distobuccally oriented postmetacrista enance of this species. in having more inflated (rather than buccolingually on M1. Postprotocrista of M1 continuous with Ekgmowechashalidae Szalay, 1976; Gatanthro- compressed) paracone and metacone, broader postmetaconule crista, rather than merging with pus micros gen. et sp. nov. Holotype: IVPP V22717, buccal cingulum, and stronger and more exten- hypometacrista to form distal margin of trigon, as isolated left M1 (Fig. 1D and supplementary sive postprotocingulum. Etymology: In allusion in extant tarsiids. M1 differs from that of Eocene materials). Horizon and locality:EarlyOligo- to the ekgmowechashalid affinities of this taxon, Xanthorhysis in being relatively shorter, broader, cene Lijiawa fossil site, upper part of Caijiachong its generic name derives from the Greek “gata” and higher-crowned, with entoconid located far- Formation, Yuezhou Basin, Yunnan Province, (cat) and “anthropus” (man), and its trivial name ther mesially. Lacks hypoparacrista and hypome- China. Diagnosis: Differs from other ekgmowe- derives from the Greek “micros” (small). Ekgmo-
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