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On the Origin of the Order Artiodactyla (Arctocyonidae/Paleocene/Eocene) KENNETH D

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On the Origin of the Order Artiodactyla (Arctocyonidae/Paleocene/Eocene) KENNETH D Proc. Natl. Acad. Sci. USA Vol. 93, pp. 1705-1709, February 1996 Evolution On the origin of the order Artiodactyla (Arctocyonidae/Paleocene/Eocene) KENNETH D. ROSE Department of Cell Biology and Anatomy, The Johns Hopkins University School of Medicine, Baltimore, MD 21205 Communicated by Edwin H. Colbert, Museum of Northern Arizona, Flagstaff AZ, February 27, 1995 ABSTRACT The first known members of the order Ar- (i.e., euprimates: lemurs, tarsiers, monkeys, and apes) and suddenly throughout the Holarctic region Perissodactyla (odd-toed ungulates such as horses, tapirs, and tiodactyla appeared in early at the beginning of the Eocene. They are characterized by rhinos)-also appeared abruptly and in abundance distinctive cursorial skeletal specializations. Owing to their Eocene Holarctic deposits, with little indication of their an- and the lack of transitional forms, the cestry. This situation has given rise to speculation that these abrupt appearance or South origin of the order is problematic. Descent from a "condy- orders originated in isolation, perhaps in Central has been sug- America, Africa, or India, and that warming climates or larth," specifically the arctocyonid Chriacus, dispersal into gested based on dental resemblances, but until now postcra- breakdown of physical barriers allowed their nial anatomy seemed to preclude close relationship between Holarctica (3, 31-33). Artiodactyla. A middle Paleocene specimen Fueling this speculation have been several recent fossil Arctocyonidae and an apparent true primate, of a small arctocyonid (?Chriacus) reported here is much more discoveries. These include teeth of derived older than any other, from the late Paleocene of north Africa similar to the oldest artiodactyl, Diacodexis, in the late reviving the possibility that Artio- (34), and the skull of a primitive phenacolophid from the condition of the hindlimb, which appears to be more closely dactyla evolved from an arctocyonid. Paleocene of southern China, related to Perissodactyla than the long-held sister group, North American Paleocene Phenacodonta (35-37). More pertinent Artiodactyla, the even-toed ungulates (pigs, camels, deer, of Diacodexis in land to the origin of artiodactyls is the discovery cattle, and their relatives), are the predominant large late early-middle Eocene strata of Pakistan and India (29, 30). mammals of today. The oldest fossil artiodactyls come from Though possibly more primitive than the oldest North Amer- early Eocene strata of North America, Europe, and Asia. Their ican and European Diacodexis, Diacodexis pakistanensis is initial appearance seems to coincide with what is increasingly geologically younger. This evidence, while tantalizing, is still regarded, at least among vertebrate paleontologists, as the circumstantial, and significant stages in the transition to these beginning of the Eocene on these continents-i.e., the base of modern orders are missing. In short, the geographic source of the Wasatchian, Sparnacian, or Bumbanian land-mammal Artiodactyla remains unresolved. ages, respectively (1-6). There is general agreement that the beginning of these land-mammal ages was essentially isochro- Condylarths and Artiodactyla nous. The earliest artiodactyls are instantly recognizable from For more than 50 years, the phylogenetic source of Artiodac- their diagnostic double-pulley astragalus, but much of the tyla has been considered to lie among the Condylarthra, a skeleton also bears the hallmarks of the order, including diverse, paraphyletic assemblage that also probably includes strongly paraxonic feet and other specializations for cursorial the basal stock of other ungulates, including perissodactyls, locomotion (7-14). The skull and its bunodont dentition, on hyracoids, sirenians, proboscideans, and cetaceans, as well as the other hand, are relatively conservative in these early forms, several extinct orders (36, 38). Derivation from a hyopsodontid exhibiting few if any diagnostic artiodactyl traits. condylarth was long believed probable (refs. 39 and 40; see ref. Early Eocene records of Artiodactyla are referable to Dia- 41 for historical review) but now seems unlikely. Although codexis and closely allied genera variously allocated to Di- there is a general dental resemblance between Paleocene hyops- chobunidae sensu lato or Diacodexeidae (for oldest North odontids (e.g., Promioclaenus, Litomylus) and Wasatchian American records, see refs. 3 and 15-18; for Europe, refs. artiodactyls, hyopsodontid postcranial anatomy-primarily 19-26; for Asia, refs. 1 and 27-30). About the size of a rabbit, based on Bridgerian Hyopsodus (42-44)-indicates that they these oldest artiodactyls were much smaller than most modern were short-limbed, pentadactyl, clawed mammals of quite members of the order. The relative abundance, widespread disparate adaptation (fossorial or perhaps scansorial) from all occurrence, and abrupt appearance of artiodactyls at the base early artiodactyls. of the Eocene make them among the strongest fossil evidence Van Valen (41) put forth the most plausible proposal for the that this boundary has been crossed. phylogenetic source of Artiodactyla, their possible descent The sudden appearance of artiodactyls in early Eocene from small arctocyonid condylarths near Metachriacus, which Holarctic faunas presents one of the great enigmas of mam- he then considered to be included in the genus Tricentes. This malian history: how and where did Artiodactyla originate? inference was based primarily on dental resemblance (which is They are usually considered to have evolved from "condy- closer than that to hyopsodontids), since at that time practi- larths" (a rather heterogeneous grade of primitive, mostly cally nothing was known of the postcranial skeletons of either herbivorous placental mammals often characterized as archaic small arctocyonids or the most primitive artiodactyls. Later, ungulates even though many bore claws), but no transitional Van Valen (45) transferred these and several other species of forms have been found-though, admittedly, we still know small arctocyonids previously placed in Tricentes, Metachria- comparatively little about Paleocene faunas, especially outside cus, and Spanoxyodon, to Chriacus, which he portrayed as the of western North America. Two other extant orders-Primates direct ancestor ofArtiodactyla. Subsequent discovery of nearly The publication costs of this article were defrayed in part by page charge Abbreviations: USGS, Geological Survey, Denver; USNM, National payment. This article must therefore be hereby marked "advertisement" in Museum of Natural History, Smithsonian Institution, Washington, accordance with 18 U.S.C. §1734 solely to indicate this fact. DC. 1705 Downloaded by guest on September 28, 2021 1706 Evolution: Rose Proc. Natl. Acad. Sci. USA 93 (1996) complete skeletons of Wasatchian Chriacus (sensu stricto) and the the (e.g., condylarths Hyopsodus, Phenacodus, and Menisco- primitive artiodactyl Diacodexis revealed profound differ- therium, as well as is indeed ences between them and led to perissodactyls) large and com- the conclusion that Chriacus paratively distal in position, this process differs markedly in was not particularly close to Artiodactyla (7, 46). Other size or in others arctocyonids for position (e.g., uintatheres, Arsinoitherium, which postcrania are known either resemble anisonchine periptychid condylarths). It is smaller and rela- Chriacus in their skeletal anatomy or differ from early artio- more in dactyls in tively proximal arctocyonids than in phenacodontid other ways (47-51). condylarths and In Diacodexis the third Rejection of Chriacus as the ancestor of perissodactyls (48). Artiodactyla as- trochanter is very small and slightly more distal than in sumes that Diacodexis approximates the artiodactyl morpho- all other type. Although it has arctocyonids (7, 8). Nearly artiodactyls lack a third widely been considered to be the most trochanter, hence its reduction and loss is inferred to be primitive known artiodactyl (8, 9, 23, 41), some of its postcra- derived in Therefore, both the reduced nial specializations for cursorial-saltatorial locomotion Artiodactyla. (artio- seem dactyl) and hypertrophied (perissodactyl) states are probably to exceed those in certain other primitive artiodactyls. For this derived relative to that in arctocyonids. reason, Diacodexis has sometimes been viewed as closer to selenodont artiodactyls (camels, ruminants, and their kin, New Fossil Evidence whose teeth are characterized by crescentic crests) and there- fore unlikely to represent the stem artiodactyl (7, 52). No older The probability of a close or even sister-group relationship or demonstrably more primitive artiodactyl genus is known, between and is however, and the Arctocyonidae Artiodactyla resurrected by a relatively uniform postcranial anatomy of previously undescribed specimen of a small arctocyonid from dichobunids suggests that Diacodexis does in fact approach the the middle Paleocene ofNew Mexico. USNM 407522 (USNM, primitive condition for the order. Dental anatomy also sup- National Museum of Natural History, Smithsonian Institution, ports the basal position of Diacodexis (18). consists of both dentaries Prothero et al. (38) Washington, DC) and associated considered Artiodactyla to be the sister bone fragments including a distal left femur, proximal left group of all other Ungulata (including Arctocyonidae, the next tibia, and two vertebrae. The dentaries contain left P4 and M2, most primitive group), citing addition of a
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