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Mammalia, Perissodactyla ARTICLE https://doi.org/10.1038/s42003-020-01205-8 OPEN The origin of Rhinocerotoidea and phylogeny of Ceratomorpha (Mammalia, Perissodactyla) ✉ ✉ Bin Bai 1,2 , Jin Meng 1,3,4, Chi Zhang 1,2, Yan-Xin Gong1,2,5 & Yuan-Qing Wang 1,2,5 1234567890():,; Rhinoceroses have been considered to have originated from tapiroids in the middle Eocene; however, the transition remains controversial, and the first unequivocal rhinocerotoids appeared about 4 Ma later than the earliest tapiroids of the Early Eocene. Here we describe 5 genera and 6 new species of rhinoceroses recently discovered from the early Eocene to the early middle Eocene deposits of the Erlian Basin of Inner Mongolia, China. These new materials represent the earliest members of rhinocerotoids, forstercooperiids, and/or hyr- achyids, and bridge the evolutionary gap between the early Eocene ceratomorphs and middle Eocene rhinocerotoids. The phylogenetic analyses using parsimony and Bayesian inference methods support their affinities with rhinocerotoids, and also illuminate the phylogenetic relationships and biogeography of Ceratomorpha, although some discrepancies are present between the two criteria. The nearly contemporary occurrence of various rhinocerotoids indicates that the divergence of different rhinocerotoid groups occurred no later than the late early Eocene, which is soon after the split between the rhinocerotoids and the tapiroids in the early early Eocene. However, the Bayesian tip-dating estimate suggests that the divergence of different ceratomorph groups occurred in the middle Paleocene. 1 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China. 2 CAS Center for Excellence in Life and Paleoenvironment, Beijing 100044, China. 3 Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA. 4 Earth and Environmental Sciences, Graduate Center, City University of New York, New York, NY 10016, USA. 5 College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing 100049, China. ✉ email: [email protected]; [email protected] COMMUNICATIONS BIOLOGY | (2020) 3:509 | https://doi.org/10.1038/s42003-020-01205-8 | www.nature.com/commsbio 1 analyses have eitherCeratomorpha focused still on remainnumerous tapiroids contentious. fossils, Previousextinction. the phylogenetic Furthermore, phylogeny despite and a evolutionary long history research of history and Rhinocerotoidea. controversial rhinocerotoids) known from Asiadistributions and of North new America. rhinocerotoids Abbreviations: from A. the Amynodontidae, Erlian Br. Basin. Bridgerian, The Forst. light Forstercooperiidae, blue, R gray, and green bars represent previously described early rhinocerotoid Chaganboerhe; 10, Bayan Ulan; 11,the Nom Erlian Khong. Basin. The 1, red dots Houldjin; refer 2, to Arshanto; the 3, localities Irdin where Manha; new 4, materials Daoteyin were found. Obo; 5, Duheminboerhe; 6, Nuhetingboerhe; 7, Wulanboerhe; 8, Huheboerhe; 9, and unequivocal rhinocerotoids and new material from the early Eocene and early remained atomorpha were not well resolved and many controversies still atomorphs arediverse reduced fossil to records in the Cenozoic; however, extant cer- Amynodontidae, and Rhinocerotidae Hyracodontidae (giant rhinos) recently treated as a separated family derived from 2 Fig. 1 Fossil localities and distributions of early rhinocerotoids. a taxa and character selection contained both tapiroidswithout and the rhinocerotoids are combination still of limited both in groups. Analyses that have B ARTICLE America in the middle Eocene, and has usually been considered to achyus Rhinocerotoidea conventionally comprises Hyracodontidae, group Ceratomorpha that Rhinocerotoidea and Tapiroideaoth form morphological a and monophyletic molecular studies support the idea ’ (or Hyrachyidae), which spr 1 c , 4 a , 5 , 8 13.2 m 22.6 m 12.6 m 9.8 m – 13 11 . Rhinocerotoids probably originated from . Section China AS-3 AS-6 NM-3 NM-4 AS-1 AS-2 AS-4 AS-5 IM-2 IM-2 COMMUNICATIONS BIOLOGY 1 – 1 3 , fi 7 . The ceratomorphs have abundant, , so that relationships within Cer- ve genera and on the brink of Nomogen F. Arshanto Formation IM Mongolia Yimengia magna ead from Eurasia to North Yimengia chaganses 10 “Rhinocerotoidea” , 12 * , with paraceratheres Triplopus? youjingensis 4 , 5 * or rhinocerotoids Hyrachyus? tumidus Erlian 500 km | (2020) 3:509 | https://doi.org/10.1038/s42003-020-01205-8 | www.nature.com/commsbio Inner Mongolia * Ephyrachyus woodi Beijing Hyrachyus crista Asia The location of the Erlian Basin of Inner Mongolia, China; Triplopus? proficiens * ‘ Forst. Gobioceras wan Hyr- gi COMMUNICATIONS BIOLOGY | https://doi.org/10.1038/s42003-020-01205-8 Pappaceras 6 b skeleton for fast running Recently, Wang et al. However, the postcranial skeleton of ‘ and could not be an ancestor of cerotoids have not been reported from the early Eocene or the early Uintan as represented by its sister group otoid Arshantan ALMA (Fig. rhinos. But known rhinocerotoids and considered to be ancestral to later giant these two families amynodontid characters, suggesti and possesses a combination o Mammal Age (ALMA) be a transitional form from the tapiroids to rhinocerotoids Land Mammal Age (NALMA) triamynodon Forstercooperia dontids areall rhinocerotoid represented groups. The by earliest hyracodontids and amyno- Hyrachyus – A. middle Eocene in the Erlian Basin. The dark blue bars and stars show the Rostriamynodon Rhodopagus Pappaceras meiomenus Rhino.? Fouchia ’ Pappaceras arose from tapiroids more primitive than , respectively, from the early Uintan North American Dilophodon North America Hyrachyus rachyus 11 Epihy , 20 11 .Exceptfor Triplopus 18 Rhino. 1 reported the earliest u is already more derived than 14 c), which is slightly earlier than any other (Fig. Epitriplopus .So Uintaceras 17 Hyrachyus 1 from the early Triplopus Amynodon ). Rhinocerotidae also appeared in and/or Irdin Manhan Asian Land Triplopus ng a close relationship between c Pappaceras Distributions of early controversial Bumbanian Arshantan ALMA f both paraceratheriid and Br1b Br1a Br2 Br3 Uintan1 MA b Wasatchian NAL , which bears a specialized Hyrachyus 47.8 Paleogene fossil localities in 56.0 could not be ancestry to Ypresian Lutetian (Stage) Epoch/Age and ,unequivocalrhino- nequivocal rhinocer- – Early Eocene Middle Eocene middleEoceneof Amynodon suggests that Uintaceras 50 55 56 47 45 ‘ Hyrachyus Heptodon 6 s (or hino. , 14 / Ros- – 19 16 ’ . , , COMMUNICATIONS BIOLOGY | https://doi.org/10.1038/s42003-020-01205-8 ARTICLE Fig. 2 Specimens of Yimengia magna sp. nov. from the upper part of the Nomogen Formation of the Erlian Basin. a, b Right mandible with dp4-m1 (a), m3 (b) (IVPP V 26234, holotype) in occlusal (a1, b1), buccal (a2, b2), and lingual (a3, c3) views; c right mandible with dp3–m1 (IVPP V 26235) in occlusal (c1), buccal (c2), and lingual (c3) views; d partial left P4 (IVPP V 26238.1) in occlusal (d1) and lingual (d2) views; e right M3 (IVPP V 26238.2) in occlusal (e1), buccal (e2), and lingual (e3) views; f right maxilla with M1–2 (IVPP V 26241) in occlusal (f1), buccal (f2), and lingual (f3) views. early–middle Eocene in either North America or Asia, although Locality and horizon. Early–middle Eocene; Guanzhuang some relatively small ceratomorphs have been argued to be rhino- Formation, Laiwu and Xintai county, Shandong Province; cerotoids, such as Fouchia, Dilophodon, Rhodopagus,andYimen- Nomogen and Arshanto formation, Erlian Basin, Inner Mongolia. gia21–23 (Fig. 1c). Diagnosis. Differs from Rhodopagus in having P4 metaconule Here on the basis of new, diverse rhinocerotoid materials from contacting the base of the protocone, M1–2 metacone less the early Eocene to the early–middle Eocene in the Erlian Basin of lingually appressed and more elongated without bulges at the base Inner Mongolia, China (Fig. 1a, b), we describe five genera of the buccal side, M3 with a more distinct metacone, and (including a new genus) and six new species that represent ear- centrocrista not confluent with the metaloph, p3–4 paraconid and liest members of rhinocerotoids, forstercooperiids, and/or hyr- hypoconid relatively lower, cristid obliqua more lingually slanted, achyids (Fig. 1c). We further resurrect the genus Ephyrachyus, p3 metaconid separated from the protoconid, p4 entoconid less and erect a new species of Ephyrachyus. These new materials are distinct, and the lower molars with relatively longer trigonid, unearthed from the upper part of the Nomogen Formation and more transversely extended protoloph, and more lingually the Arshanto Formation, which are considered to be the early extended cristid obliqua with a relatively higher contact with Eocene Bumbanian and the early–middle Eocene Arshantan the protolophid. Differs from Minchenoletes in having a more ALMA24, respectively. The Bumbanian is normally comparable lingually placed metacone on M1–3, metaloph of M1–3 joining with Wasatchian NALMA, and the Arshantan is comparable with the ectoloph less forward, M3 metacone more reduced, and less Bridgerian plus the early Uintan NALMA based on the mammal distinct hypoconulids on lower molars. Differs from Triplopus (as fauna correlation and the recent paleomagnetic analyses25,26. represented by T. cubitalus) in having the metaconule not These new diverse rhinocerotoids bridge the evolutionary gap forming a loop with the protoloph on P3–4, a shorter metacone
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