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A New Genus of Horse from Pleistocene North America

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A New Genus of Horse from Pleistocene North America bioRxiv preprint doi: https://doi.org/10.1101/154963; this version posted June 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 A new genus of horse from Pleistocene North America 2 3 Peter D. Heintzmana,b*, Grant D. Zazulac, Ross D.E. MacPheed, Eric Scotte, James A. Cahilla, 4 Brianna K. McHorsef, Joshua D. Kappa, Mathias Stillera,g, Matthew J. Woollerh,i, Ludovic 5 Orlandoj,k, John R. Southonl, Duane G. Froesem, Beth Shapiroa,n* 6 7 a Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA 8 95064 9 b Tromsø University Museum, UiT - The Arctic University of Norway, 9037 Tromsø, Norway 10 c Yukon Palaeontology Program, Government of Yukon, Whitehorse, YT Y1A 2C6, Canada 11 d Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History, 12 New York, NY 10024 13 e Dr. John D. Cooper Archaeological and Palaeontological Center, California State University Fullerton, 14 Fullerton, CA 92831 15 f Department of Organismal and Evolutionary Biology, Harvard University, Cambridge, MA 16 g Department of Translational Skin Cancer Research, German Consortium for Translational Cancer 17 Research, D-45141 Essen, Germany 18 h College of Fisheries and Ocean Sciences, University of Alaska Fairbanks, 905 N. Koyukuk Dr., 19 Fairbanks AK 99775 USA 20 i Alaska Stable Isotope Facility, Water and Environmental Research Center, University of Alaska 21 Fairbanks, 306 Tanana Loop, Fairbanks AK 99775 USA 22 j Centre for GeoGenetics, Natural History Museum of Denmark, Øster Voldgad 5-7, 1350K Copenhagen, 23 Denmark 1 bioRxiv preprint doi: https://doi.org/10.1101/154963; this version posted June 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 24 k Université de Toulouse, Université Paul Sabatier (UPS), Laboratoire AMIS, CNRS UMR 5288, 25 Toulouse, France 26 l Keck-CCAMS Group, Earth System Science Department, University of California, Irvine, CA 92697 27 m Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB T6G 2E3, 28 Canada 29 n UCSC Genomics Institute, University of California Santa Cruz, Santa Cruz, CA 95064 30 31 *Corresponding authors: Peter D. Heintzman: [email protected]; Beth Shapiro: 32 [email protected] 33 2 bioRxiv preprint doi: https://doi.org/10.1101/154963; this version posted June 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 34 Abstract 35 The extinct “New World stilt-legged”, or NWSL, equids constitute a perplexing group of 36 Pleistocene horses endemic to North America. Their slender distal limb bones resemble those of 37 Asiatic asses, such as the Persian onager. Previous palaeogenetic studies, however, have 38 suggested a closer relationship to caballine horses than to Asiatic asses. Here, we report complete 39 mitochondrial and partial nuclear genomes from NWSL equids from across their geographic 40 range. Although multiple NWSL equid species have been named, our palaeogenomic and 41 morphometric analyses support the idea that there was only a single species of middle to late 42 Pleistocene NWSL equid, and demonstrate that it falls outside of crown group Equus. We 43 therefore propose a new genus, Haringtonhippus, for the sole species H. francisci. Our combined 44 genomic and phenomic approach to resolving the systematics of extinct megafauna will allow for 45 an improved understanding of the full extent of the terminal Pleistocene extinction event. 46 3 bioRxiv preprint doi: https://doi.org/10.1101/154963; this version posted June 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 47 Introduction 48 The family that includes modern horses, asses, and zebras, the Equidae, is a classic model of 49 macroevolution. The excellent fossil record of this family clearly documents its ~55 million year 50 evolution from dog-sized hyracotheres through many intermediate forms and extinct offshoots to 51 present-day Equus, which comprises all living equid species (MacFadden, 1992). The downside 52 of this excellent fossil record is that many dubious fossil equid taxa have been erected, a problem 53 especially acute within Pleistocene Equus of North America (Macdonald & Toohey, 1992). 54 While numerous species are described from the fossil record, molecular data suggest that most 55 belonged to, or were closely related to, a single, highly variable stout-legged caballine species 56 that includes the domestic horse, E. caballus (Weinstock et al., 2005). The enigmatic and extinct 57 “New World stilt-legged” (NWSL) forms, however, exhibit a perplexing mix of morphological 58 characters, including slender, stilt-like distal limb bones with narrow hooves reminiscent of 59 extant Eurasian hemionines, the Asiatic wild asses (E. hemionus, E. kiang) (Eisenmann, 1992; 60 Eisenmann et al., 2008; Harington & Clulow, 1973; Lundelius & Stevens, 1970; Scott, 2004), 61 and dentitions that have been interpreted as more consistent with either caballine horses 62 (Lundelius & Stevens, 1970) or hemionines (MacFadden, 1992). 63 On the basis of their slender distal limb bones, the NWSL equids have traditionally been 64 considered as allied to hemionines (e.g. (Eisenmann et al., 2008; Guthrie, 2003; Scott, 2004; 65 Skinner & Hibbard, 1972)). Palaeogenetic analyses based on mitochondrial DNA (mtDNA) 66 have, however, consistently placed NWSL equids closer to caballine horses (Der Sarkissian et 67 al., 2015; Orlando et al., 2008, 2009; Vilstrup et al., 2013; Weinstock et al., 2005). The current 68 mtDNA-based phylogenetic model therefore suggests that the stilt-legged morphology arose 69 independently in the New and Old Worlds (Weinstock et al., 2005), and may represent 4 bioRxiv preprint doi: https://doi.org/10.1101/154963; this version posted June 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 70 convergent adaptations to arid climates and habitats (Eisenmann, 1985). However, these models 71 have been based on two questionable sources. The first is based on 4 short control region 72 sequences (<1000 base pairs, bp; (Weinstock et al., 2005)), a data type that can be unreliable for 73 resolving the placement of major equid groups (Der Sarkissian et al., 2015; Orlando et al., 2009). 74 The second consist of 2 mitochondrial genome sequences (Vilstrup et al., 2013) that are either 75 incomplete or otherwise problematic (see Results). Given continuing uncertainty regarding the 76 phylogenetic placement of NWSL equids—which impedes our understanding of Pleistocene 77 equid evolution in general—we therefore sought to resolve their position using multiple 78 mitochondrial and partial nuclear genomes from specimens representing as many parts of late 79 Pleistocene North America as possible. 80 The earliest recognized NWSL equid fossils date to the late Pliocene/early Pleistocene 81 (~2-3 million years ago, Ma) of New Mexico (Azzaroli & Voorhies, 1993; Eisenmann, 2003; 82 Eisenmann et al., 2008)). Middle and late Pleistocene forms tended to be smaller in stature than 83 their early Pleistocene kin, and ranged across southern and extreme northwestern North America 84 (i.e., eastern Beringia, which includes Alaska, USA and Yukon Territory, Canada). NWSL 85 equids have been assigned to several named species, such as E. tau Owen 1869, E. francisci Hay 86 1915, E. calobatus Troxell 1915, and E. (Asinus) cf. kiang, but there is considerable confusion 87 and disagreement regarding their taxonomy. Consequently, some researchers have chosen to 88 refer to them collectively as Equus (Hemionus) spp. (Guthrie, 2003; Scott, 2004), or avoid a 89 formal taxonomic designation altogether (Der Sarkissian et al., 2015; Vilstrup et al., 2013; 90 Weinstock et al., 2005). Using our phylogenetic framework and comparisons between specimens 91 identified by palaeogenomics and/or morphology, we attempted to determine the taxonomy of 92 middle-late Pleistocene NWSL equids. 5 bioRxiv preprint doi: https://doi.org/10.1101/154963; this version posted June 24, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 93 Radiocarbon (14C) dates from Gypsum Cave, Nevada, confirm that NWSL equids 94 persisted in areas south of the continental ice sheets during the last glacial maximum (LGM; 95 ~26-19 thousand radiocarbon years before present (ka BP; (Clark et al., 2009)) until near the 96 terminal Pleistocene, ~13 thousand radiocarbon years before present (14C ka BP) (Weinstock et 97 al., 2005), soon after which they became extinct, along with their caballine counterparts and 98 most other coeval species of megafauna (Koch & Barnosky, 2006). This contrasts with dates 99 from unglaciated eastern Beringia, where NWSL equids were seemingly extirpated locally 100 during a relatively mild interstadial interval centered on ~31 14C ka BP (Guthrie, 2003), thus 101 prior to the LGM (Clark et al., 2009), final loss of caballine horses (Guthrie, 2003, 2006), and 102 arrival of humans in the region (Guthrie,
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