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Full-Text PDF (Final Published Version) Bai, B., Meng, J., Janis, C. M., Zhang, Z-Q., & Wang, Y-Q. (2020). Perissodactyl diversities and responses to climate changes as reflected by dental homogeneity during the Cenozoic in Asia. Ecology and Evolution, 10(13), 1-23. [6363]. https://doi.org/10.1002/ece3.6363 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.1002/ece3.6363 Link to publication record in Explore Bristol Research PDF-document This is the final published version of the article (version of record). It first appeared online via Wiley at https://doi.org/10.1002/ece3.6363 . Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/red/research-policy/pure/user-guides/ebr-terms/ Received: 22 January 2020 | Revised: 20 April 2020 | Accepted: 21 April 2020 DOI: 10.1002/ece3.6363 ORIGINAL RESEARCH Perissodactyl diversities and responses to climate changes as reflected by dental homogeneity during the Cenozoic in Asia Bin Bai1,2 | Jin Meng1,3,4 | Christine M. Janis5,6 | Zhao-Qun Zhang1,2,7 | Yuan-Qing Wang1,2,7 1Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China 2CAS Center for Excellence in Life and Paleoenvironment, Beijing, China 3Division of Paleontology, American Museum of Natural History, New York, NY, USA 4Earth and Environmental Sciences, Graduate Center, City University of New York, New York, NY, USA 5School of Earth Sciences, University of Bristol, Bristol, UK 6Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA 7College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing, China Correspondence Bin Bai, Key Laboratory of Vertebrate Abstract Evolution and Human Origins of Chinese Cenozoic mammal evolution and faunal turnover are considered to have been influ- Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, enced and triggered by global climate change. Teeth of large terrestrial ungulates are Chinese Academy of Sciences, Beijing reliable proxies to trace long-term climatic changes due to their morphological and 100044, China. Email: [email protected] physicochemical properties; however, the role of premolar molarization in ungulate evolution and related climatic change has rarely been investigated. Recently, three Funding information China Scholarship Council, Grant/Award patterns of premolar molarization among perissodactyls have been recognized: en- Number: 201204910062; National Natural doprotocrista-derived hypocone (type I); paraconule–protocone separation (type II); Science Foundation of China, Grant/Award Number: 41672014; the Strategic Priority and metaconule-derived pseudohypocone (type III). These three patterns of premo- Research Program of Chinese Academy lar molarization play an important role in perissodactyl diversity coupled with global of Sciences, Grant/Award Number: XDB26000000; Geological Investigation climate change during the Cenozoic in Asia. Those groups with a relatively higher Project of the China Geological Survey, degree of premolar molarization, initiated by the formation of the hypocone, survived Grant/Award Number: DD20190009; the Frick Fund from the Division of into Neogene, whereas those with a lesser degree of molarization, initiated by the Paleontology, American Museum of Natural deformation of existing ridges and cusps, went extinct by the end of the Oligocene. History; Youth Innovation Promotion Association of the Chinese Academy of In addition, the hypothesis of the “Ulan Gochu Decline” is proposed here to designate Sciences, Grant/Award Number: 2017101 the most conspicuous decrease of perissodactyl diversity that occurred in the latest middle Eocene rather than at the Eocene–Oligocene transition in Asia, as convention- ally thought; this event was likely comparable to the contemporaneous post-Uintan decline of the North American land fauna. KEYWORDS Asian perissodactyl diversity, Cenozoic, premolar molarization, Ulan Gochu Decline This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd Ecology and Evolution. 2020;10:6333–6355. www.ecolevol.org | 6333 6334 | BAI ET AL. 1 | INTRODUCTION Fortelius, 1996; Mihlbachler et al., 2011; Secord et al., 2012), but lit- tle attention has been paid to the evolutionary patterns of premolar Living perissodactyls (odd-toed ungulates) represent the rem- molarization in perissodactyls (Butler, 1952; Holbrook, 2015). nants of a major evolutionary sequence and comprise only six gen- Molarization of the premolars generally results in dental ho- era and 17 species with many in danger of extinction (Nowak & mogeneity and increases the grinding area of the dentition; this is Walker, 1999). However, perissodactyls had a rich, diverse fossil re- especially important for hindgut fermenting ungulates such as peris- cord spanning 56 Myr, and have not only long been used as a strong sodactyls as they are highly reliant on oral processing of the food evidence for evolution since Huxley (e.g., horses), but also for infer- before its initial ingestion (Clauss, Nunn, Fritz, & Hummel, 2009; ring climatic and environmental changes, and their coevolution with Fletcher, Janis, & Rayfield, 2010). In contrast, the foregut ferment- such changes (Franzen, 2010; MacFadden, 1992; Mihlbachler, Rivals, ing artiodactyls, ruminants and camelids, are less reliant on oral Solounias, & Semprebon, 2011; Secord et al., 2012; Simpson, 1951). processing: they only have partially molarized premolars, and their The most conspicuous fauna turnover during the Paleogene in Asia premolar complexity decreases from P4 to P2 (P1 is usually lost). is considered to have occurred during the Eocene–Oligocene transi- However, it is unclear what the role of premolar molarization is in tion, and the Eocene perissodactyl-dominant faunas were abruptly perissodactyl evolution and diversity, how perissodactyl diversity replaced by the Oligocene rodent/lagomorph-dominant fau- and premolar molariform changed through the Cenozoic in Asia, nas (Meng & McKenna, 1998). This major faunal turnover, known as and whether perissodactyl diversity tracked the Cenozoic climatic “Mongolian Remodelling,” is attributed to climatic changes from the changes. Here, we show that three recently proposed patterns of warm, humid Eocene to the cooler and more arid Oligocene (Meng premolar molarization in perissodactyls may have played an import- & McKenna, 1998; Zachos, Pagani, Sloan, Thomas, & Billups, 2001). ant role in their response to climatic and environmental changes However, there is controversy as to whether this faunal turnover during the Cenozoic. Further, based on analysis of perissodactyl either predates (Wasiljeff, Kaakinen, Salminen, & Zhang, 2020), co- diversity with an updated Cenozoic timescale of China in Asia, we incides with (Sun et al., 2014; Zhang, Kravchinsky, & Yue, 2012), or note that the most distinct change occurred during the latest middle postdates (Kraatz & Geisler, 2010) the Eocene–Oligocene boundary. Eocene, rather than at Eocene–Oligocene transition as convention- Perissodactyls have been considered to have originated from ally considered, and is likely comparable to the contemporaneous within the radiation of phenacodont condylarths (Radinsky, 1966; post-Uintan decline of North American land fauna (Prothero, 1994). Thewissen & Domning, 1992) or to be a sister group to Radinskya from the middle Paleocene of China (Holbrook, 2014; McKenna, Chow, Ting, & Luo, 1989), while more recent work has shown cam- 2 | METHODS baytheres from the early Eocene of Indian subcontinent to be more closely related to perissodactyls than either of these previously 2.1 | Premolar molarization considered taxa (Rose et al., 2014). Recent research on ancient proteins suggests that crown perissodactyls are the sister group to Five categories of premolar molarization, initially used for rhinocer- some extinct South American ungulates among more recent mam- oses, were assigned to the P2-4 of perissodactyls: nonmolariform, mals (Welker et al., 2015). Teeth, composed of the hardest verte- premolariform, submolariform, semimolariform, and molariform (Qiu brate tissues, are the best preserved material in perissodactyls as in & Wang, 2007) (Figure 1). In the premolariform morphology, the hy- other mammal fossils, and the most sensitive proxy to environmen- pocone is united with the protoloph, but the metaloph is not com- tal changes (Mihlbachler et al., 2011; Secord et al., 2012). Previous pletely formed (i.e., is separate from the hypocone) (Figure 1a). In studies on the dentition of extinct perissodactyls (and other ungu- the submolariform morphology, the metaloph is completely formed lates) have focused on molar crown height, enamel stable isotopes, (connected to the hypocone) and united with the protoloph on the micro-mesowear, and overall morphology through the Cenozoic lingual side (Figure 1b). In the semimolariform morphology, the pro- (Ackermans, 2020; Evans & Pineda-Munoz,
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