ARTICLE doi:10.1038/nature10574 Species-specific responses of Late Quaternary megafauna to climate and humans Eline D. Lorenzen1*, David Nogues-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, Alan Cooper39, Michael Hofreiter40, Andrei Sher34{, Beth Shapiro41, Carsten Rahbek2 & Eske Willerslev1 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 muskox. We show that climatehas been a major driverof populationchangeoverthepast50,000years.However,eachspeciesrespondsdifferentlytotheeffectsofclimaticshifts, habitat redistribution and human encroachment. Although climate change alone can explain the extinction of some species, such as Eurasian muskox 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 years ago, Eurasia and North America lost approximately 36% and 72% of their large-bodied mammalian genera (megafauna), respec- tively1. The debate surrounding the potential causes of these extinc- tions has focused primarily on the relative roles of climate and humans2–5. In general, the proportion of species that went extinct wasgreatest on continents that experienced the most dramatic climatic changes6, implying a major role of climate in species loss. However, the continental pattern of megafaunal extinctions in North America and Australia approximately coincides with the first appearance of humans, suggesting a potential anthropogenic contribution to species extinctions3,5. *These authors contributed equally to this work. {Deceased. 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. 3 Smithsonian Tropical Research Institute, Tupper Building, 401 Balboa, Ancon, ´ Punama, ´ Republica ´ de Panama. ´ 4 Departments 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. 6 School of Biological Sciences, University of Sydney, New South Wales 2006, Australia. 7 Center 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. 10 Conservation and Evolutionary Genetics Group, Estacion ´ Biologica ´ de Donana ˜ (EBD-CSIC), Avenida Americo ´ Vespucio, 41092 Seville, Spain. 11 Department of Ecology and Evolutionary Biology, Universityof California, Los Angeles, California 90095,USA. 12Laboratory of Genomic Diversity, National Cancer Institute, Building 560,Room 11-33,Frederick, Maryland 21702,USA. 13 Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada. 14 Government of Yukon, Department of Tourism and Culture, Yukon Palaeontology Program, PO Box 2703 L2A, Whitehorse, Yukon Territory Y1A 2C6, Canada. 15 Stafford Research Inc., 200 Acadia Avenue, Lafayette, Colorado 80026, USA. 16 Department of Earth and Environment, Mount Holyoke College, 50 College Street, South Hadley, Massachusetts 01075, USA. 17 School of Earth and Environment, University of Leeds, Woodhouse Lane, Leeds, West Yorkshire LS2 9JT, UK. 18 School of Geographical Sciences, University of Bristol, University Road, Bristol BS8 1SS, UK. 19 Diamond and Precious Metals Geology Institute, Siberian Branch of Russian Academy of Sciences, 39 Prospect Lenina, 677891Yakutsk,Russia. 20 Royal AlbertaMuseum,Edmonton,Alberta T5N0M6,Canada. 21 TheManitobaMuseum,Winnipeg,ManitobaR3B 0N2,Canada. 22 North-EastScienceStation,PacificInstitutefor Geography, Far East Branch of Russian Academy of Sciences, 2 Malinovy Yar Street, 678830 Chersky, Russia. 23 Museum 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. 26 State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, Hubei 430074, China. 27 University 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. 30 Bioinformatics Research Centre (BiRC), Aarhus University, C.F. Møllers Alle ´ 8, DK-8000 Aarhus C, Denmark. 31Regierungsprasidium ¨ Stuttgart, Landesamt fur ¨ Denkmalpflege, Stromeyersdorfstrasse 3, D-78467 Konstanz, Germany. 32Zoological Institute of Russian Academy of Sciences, Universitetskaya nab. 1, 199034 Saint-Petersburg, Russia. 33 Christian-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. 36 Departments 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. 39 Australian Centre for Ancient DNA, The University of Adelaide, South Australia 5005, Australia. 40 Department 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. 43 Museo de Historia Natural de San Rafael, (5600) Parque Mariano Moveno, San Rafael, Mendoza, Argentina. 1 7 N O V E M B E R 2 0 1 1 | V O L 4 7 9 | N A T U R E | 3 5 9 Macmillan Publishers Limited. 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Demographic trajectories of different taxa vary widely and depend on the geographic scale and methodological approaches used3,5,7. For example, genetic diversity in bison8,9, musk ox10 and European cave bear11 declines gradually from approximately 50,000–30,000 calendar 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 remains unresolved whether the Late Quaternary extinctions were a cross-taxa response to widespread climatic or anthropogenic stressors, 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 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 (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 mitochondrial DNA (mtDNA) control region sequences, 1,439 directly dated megafaunal remains and 6,291 radiocarbon determina- tions associated with Upper Palaeolithic human occupations in Eurasia. We reconstruct the demographic histories of the megafauna herbivores from ancient DNA data, model past species distribu- tions and determine the geographical overlap between humans and megafauna over the past 50,000 years. We use these data to investigate how climate change and anthropogenic impacts affected species dynamics at continental and global scales, and contributed to the extinction of some species and the survival of others. Responses differ among species and continents The direct link between climate change, population size and species extinctions is difficult to document10. However, population size is probably controlled by the amount of available habitat and is indi- cated by the geographical range of a species17,18. We assessed the role of climate using species distribution models, dated megafauna fossil remains and palaeoclimatic data on temperature and precipitation. We estimated species range sizes at the time periods of 42, 30, 21 and 6 kyr BP as a proxy for habitat availability (Fig. 1 and Supplementary Information section 1). Range size dynamics were then compared with demographic histories inferred from ancient DNA using three dis- tinct analyses (Supplementary Information section 3): (1) coalescent- based estimation of changes in effective population size through time (Bayesian skyride19), which allows detection of changes in global gen- etic diversity (2) serial coalescent simulation followed by approximate Bayesian computation, which selects among different models describ- ing continental population dynamics and (3) isolation-by-distance analysis, which estimates potential population structure and connec- tivity within continents. If climate was a major factor driving species population sizes, we would expect expansion and contraction of a species’ geographical range to mirror population increase and decline, respectively. Wefindapositivecorrelationbetweenchangesinthesizeofavailable habitat and genetic diversity for the four species—horse, reindeer, bison and musk ox—for which we have range estimates spanning all four time-points (the correlation is not statistically significant for rein- deer: P 5 0.101) (Fig. 2 and Supplementary Information section 4). Hence, species distribution modelling based on fossil distributions and climate data are congruent with estimates of effective population size basedon ancient DNA data, even in species with very differentlife- history traits. We conclude that climate has been a major driving force in megafauna population changes over the past 50,000 years. It is noteworthy that both estimated modelled ranges and genetic data are derived from a subset of the entire fossil record (Supplementary Information sections 1 and 3). Thus, changes in effective population size and range size might change with the addition of more data, especiallyfrom outside the geographical regionscoveredbythepresent study. However, we expect that the reported positive correlation will prevail when congruent data are compared. The best-supported models of changes in effective population size in North America and Eurasia during periods of dramatic climatic change over the past 50,000 years are those in which populations increase in size (Fig. 3 and Supplementary Information section 3). This is true for all taxa except bison. However, the timing is not synchronous across populations. Specifically, we find highest support for population increase beginning approximately 34kyr BP in Eurasian horse, reindeer and musk ox (Fig. 3a). Eurasian woolly mammoth and North American horse increase before the Last Glacial Maximum (LGM) approximately 26kyr BP. Models of population increase in woolly rhinoceros and North American woolly mammoth fit equally well before and after the LGM, and North American reindeer popula- tions increase later still. Only North American bison shows a popu- lation decline (Fig. 3b), the intensity of which probably swamps the signal of global population increase starting at approximately 35kyr BP identified in the skyride plot (Fig. 2a). These increases in effective population size probably reflect res- ponses to climate change. By 34 kyr BP, the relatively warmer Marine Isotope Stage (MIS) 3 interstadial marked the transition to cold, arid full-glacial conditions of MIS 2, which began approximately Reindeer Horse Woolly mammoth Bison Musk ox Woolly rhinoceros Extinct 42 kyr BP 30 kyr BP 21 kyr BP 6 kyr BP NA Figure 1 | Modelled potential ranges of megafauna species at 42, 30, 21 and 6 kyr BP. Ranges were modelled using the megafauna fossil record and palaeoclimatic data for temperature and precipitation ice sheet extent was not included as a co-variable. Range measurements were restricted to the regions for which fossils were used to build the models, rather than all potentially suitable Holarctic area. NA, not available. RESEARCH ARTICLE 3 6 0 | N A T U R E | V O L 4 7 9 | 1 7 N O V E M B E R 2 0 1 1 Macmillan Publishers Limited. All rights reserved ©2011