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Species-Specific Responses of Late Quaternary Megafauna to Climate and Humans

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Species-Specific Responses of Late Quaternary Megafauna to Climate and Humans Species-specific responses of Late Quaternary megafauna to climate and humans Eline D. Lorenzen1*, David Nogue´s-Bravo2*, Ludovic Orlando1*, Jaco Weinstock1*, Jonas Binladen1*, Katharine A. Marske2*, Andrew Ugan3,42,43, Michael K. Borregaard2, M. Thomas P. Gilbert1, Rasmus Nielsen4,5, Simon Y. W. Ho6, Ted Goebel7, Kelly E. Graf7, David Byers8, Jesper T. Stenderup1, Morten Rasmussen1, Paula F. Campos1, Jennifer A. Leonard9,10, Klaus-Peter Koepfli11,12, Duane Froese13, Grant Zazula14, Thomas W. Stafford Jr1,15, Kim Aaris-Sørensen1, Persaram Batra16, Alan M. Haywood17, Joy S. Singarayer18, Paul J. Valdes18, Gennady Boeskorov19, James A. Burns20,21, Sergey P. Davydov22, James Haile1, Dennis L. Jenkins23, Pavel Kosintsev24, Tatyana Kuznetsova25, Xulong Lai26, Larry D. Martin27, H. Gregory McDonald28, Dick Mol29, Morten Meldgaard1, Kasper Munch30, Elisabeth Stephan31, Mikhail Sablin32, Robert S. Sommer33, Taras Sipko34, Eric Scott35, Marc A. Suchard36,37, Alexei Tikhonov32, Rane Willerslev38, Robert K. Wayne11, 39 40 34 41 2 1 Alan Cooper , Michael Hofreiter , Andrei Sher {, Beth Shapiro , Carsten Rahbek & Eske Willerslev Despite decades of research, the roles of climate and humans in driving the dramatic extinctions of large-bodied mammals during the Late Quaternary period remain contentious. Here we use ancient DNA, species distribution models and the human fossil record to elucidate how climate and humans shaped the demographic history of woolly rhinoceros, woolly mammoth, wild horse, reindeer, bison and musk ox. We show that climate has been a major driver of population change over the past 50,000 years. However, each species responds differently to the effects of climatic shifts, habitat redistribution and human encroachment. Although climate change alone can explain the extinction of some species, such as Eurasian musk ox and woolly rhinoceros, a combination of climatic and anthropogenic effects appears to be responsible for the extinction of others, including Eurasian steppe bison and wild horse. We find no genetic signature or any distinctive range dynamics distinguishing extinct from surviving species, emphasizing the challenges associated with predicting future responses of extant mammals to climate and human-mediated habitat change. Towards the end of the Late Quaternary, beginning around 50,000 was greatest on continents that experienced the most dramatic climatic years ago, Eurasia and North America lost approximately 36% and changes6, implying a major role of climate in species loss. However, the 72% of their large-bodied mammalian genera (megafauna), respec- continental pattern of megafaunal extinctions in North America and tively1. The debate surrounding the potential causes of these extinc- Australia approximately coincides with the first appearance of tions has focused primarily on the relative roles of climate and humans, suggesting a potential anthropogenic contribution to species humans2–5. In general, the proportion of species that went extinct extinctions3,5. 1Centre for GeoGenetics, University of Copenhagen, Øster Voldgade 5–7, DK-1350 Copenhagen K, Denmark. 2Center for Macroecology, Evolution and Climate, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark. 3Smithsonian Tropical Research Institute, Tupper Building, 401 Balboa, Anco´ n, Punama´ , Repu´ blica de Panama´ . 4Departments of Integrative Biology and Statistics, University of California, Berkeley, 4098 VLSB, Berkeley, California 94720, USA. 5Department of Biology, University of Copenhagen, Ole Maaloes Vej 5, DK-2200, Denmark. 6School of Biological Sciences, University of Sydney, New South Wales 2006, Australia. 7Center for the Study of the First Americans, Department of Anthropology, Texas A&M University, College Station, Texas 77843, USA. 8Department of Sociology and Anthropology, Missouri State University, 901 South National, Springfield, Missouri 65807, USA. 9Department of Evolutionary Biology, Uppsala University, 75236 Uppsala, Sweden. 10Conservation and Evolutionary Genetics Group, Estacio´ n Biolo´ gica de Don˜ ana (EBD-CSIC), Avenida Ame´ rico Vespucio, 41092 Seville, Spain. 11Department of Ecology and Evolutionary Biology, University of California, Los Angeles, California 90095, USA. 12Laboratory of Genomic Diversity, National Cancer Institute, Building 560, Room 11-33, Frederick, Maryland 21702, USA. 13Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada. 14Government of Yukon, Department of Tourism and Culture, Yukon Palaeontology Program, PO Box 2703 L2A, Whitehorse, Yukon Territory Y1A 2C6, Canada. 15Stafford Research Inc., 200 Acadia Avenue, Lafayette, Colorado 80026, USA. 16Department of Earth and Environment, Mount Holyoke College, 50 College Street, South Hadley, Massachusetts 01075, USA. 17School of Earth and Environment, University of Leeds, Woodhouse Lane, Leeds, West Yorkshire LS2 9JT, UK. 18School of Geographical Sciences, University of Bristol, University Road, Bristol BS8 1SS, UK. 19Diamond and Precious Metals Geology Institute, Siberian Branch of Russian Academy of Sciences, 39 Prospect Lenina, 677891 Yakutsk, Russia. 20Royal Alberta Museum, Edmonton, Alberta T5N 0M6, Canada. 21The Manitoba Museum, Winnipeg, Manitoba R3B 0N2, Canada. 22North-East Science Station, Pacific Institute for Geography, Far East Branch of Russian Academy of Sciences, 2 Malinovy Yar Street, 678830 Chersky, Russia. 23Museum of Natural and Cultural History, 1224 University of Oregon, Eugene, Oregon 97403- 1224, USA. 24Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences, 8 Marta Street, 202, 620144 Ekaterinburg, Russia. 25Moscow State University, Vorob’evy Gory, 119899 Moscow, Russia. 26State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, Hubei 430074, China. 27University of Kansas Museum of Natural History, University of Kansas, Lawrence, Kansas 66045, USA. 28Park Museum Management Program, National Park Service, 1201 Oakridge Drive, Suite 150, Fort Collins, Colorado 80525, USA. 29Natural History Museum, Rotterdam, c/o Gudumholm 41, 2133 HG Hoofddorp, Netherlands. 30Bioinformatics Research Centre (BiRC), Aarhus University, C.F. Møllers Alle´ 8, DK-8000 Aarhus C, Denmark. 31Regierungspra¨ sidium Stuttgart, Landesamt fu¨ r Denkmalpflege, Stromeyersdorfstrasse 3, D-78467 Konstanz, Germany. 32Zoological Institute of Russian Academy of Sciences, Universitetskaya nab. 1, 199034 Saint-Petersburg, Russia. 33Christian-Albrechts-University of Kiel, Institute for Nature and Resource Conservation, Department of Landscape Ecology, Olshausenstrasse 40, 24098 Kiel, Germany. 34Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky Prospect, 119071 Moscow, Russia. 35San Bernardino County Museum, Division of Geological Sciences, 2024 Orange Tree Lane, Redlands, California 92374, USA. 36Departments of Biomathematics and Human Genetics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California 90095, USA. 37Department of Biostatistics, UCLA School of Public Health, University of California, Los Angeles, Los Angeles, California 90095, USA. 38Museum of Cultural History, University of Oslo, St. Olavsgate 29, Postboks 6762 St. Olavsplass, 0130 Oslo, Norway. 39Australian Centre for Ancient DNA, The University of Adelaide, South Australia 5005, Australia. 40Department of Biology (Area 2), The University of York, Wentworth Way, Heslington, York YO10 5DD, UK. 41Department of Biology, The Pennsylvania State University, 326 Mueller Laboratory, University Park, Pennsylvania 16802, USA. 42Department of Anthropology, University of Utah, 271N1400E, Salt Lake City, Utah 84112-0060, USA. 43Museo de Historia Natural de San Rafael, (5600) Parque Mariano Moveno, San Rafael, Mendoza, Argentina. *These authors contributed equally to this work. {Deceased. 1 RESEAH Demographic trajectories of different taxa vary widely and depend 42 kyr BP 30 kyr BP 21 kyr BP 6 kyr BP 3,5,7 on the geographic scale and methodological approaches used . For Woolly example, genetic diversity in bison8,9, musk ox10 and European cave rhinoceros 11 bear declines gradually from approximately 50,000–30,000 calendar Extinct years ago (kyr BP). In contrast, sudden losses of genetic diversity are observed in woolly mammoth12,13 and cave lion14 long before their extinction, followed by genetic stability until the extinction events. It Woolly remains unresolved whether the Late Quaternary extinctions were a mammoth cross-taxa response to widespread climatic or anthropogenic stressors, NA or were a species-specific response to one or both factors15,16. Additionally, it is unclear whether distinctive genetic signatures or geographical range-size dynamics characterize extinct or surviving species—questions of particular importance to the conservation of Horse extant species. To disentangle the processes underlying population dynamics and extinction, we investigate the demographic histories of six megafauna herbivores of the Late Quaternary: woolly rhinoceros (Coelodonta antiquitatis), woolly mammoth (Mammuthus primigenius), horse Reindeer (wild Equus ferus and living domestic Equus caballus), reindeer/ caribou (Rangifer tarandus), bison (Bison priscus/Bison bison) and musk ox (Ovibos moschatus). These taxa were characteristic of Late Quaternary Eurasia and/or North America and represent both extinct and extant species. Our analyses are based on 846 radiocarbon-dated Bison mitochondrial
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