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Species-specific responses of Late Quaternary megafauna to climate and humans

Naturevolume 479, pages359–364 (2011)Cite this article

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Abstract

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.

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Figure 1:Modelled potential ranges of megafauna species at 42, 30, 21 and 6 kyrbp.
Figure 2:Temporal changes in global genetic diversity and range size in horse, bison, reindeer and musk ox.
Figure 3:Best-supported demographic models inferred by approximate Bayesian computation model-selection.
Figure 4:Spatial and temporal association between megafauna and Upper Palaeolithic humans.

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Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Mitochondrial DNA sequences are deposited in GenBank under accession numbersJN570760–JN571033.

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Acknowledgements

This paper is in memory of our friend and colleague Andrei Sher, who was a contributor to this study. Dr Sher died unexpectedly, but his major contributions to the field of Quaternary science will be remembered and appreciated for many years. We are grateful to A. Lister and T. Stuart for guidance and discussions. We thank T. B. Brandt, B. Hockett and A. Telka for laboratory help and samples, and L. M. R. Thrane for his work on the megafauna locality database. Data taken from the Stage 3 project were partly funded by grant F/757/A from the Leverhulme Trust, and a grant from the McDonald Grants and Awards Fund. B.S. was supported by NSF ARC-0909456. We acknowledge the Danish National Research Foundation, the Lundbeck Foundation, the Danish Council for Independent Research and the US National Science Foundation for financial support.

Author information

Author notes

  1. Eline D. Lorenzen, David Nogués-Bravo, Ludovic Orlando, Jaco Weinstock, Jonas Binladen and Katharine A. Marske: These authors contributed equally to this work.

  2. Andrei Sher: Deceased.

Authors and Affiliations

  1. Centre for GeoGenetics, University of Copenhagen, Øster Voldgade 5–7, DK-1350 Copenhagen K, Denmark ,

    Eline D. Lorenzen, Ludovic Orlando, Jaco Weinstock, Jonas Binladen, M. Thomas P. Gilbert, Jesper T. Stenderup, Morten Rasmussen, Paula F. Campos, Thomas W. Stafford, Kim Aaris-Sørensen, James Haile, Morten Meldgaard & Eske Willerslev

  2. Department of Biology, Center for Macroecology, Evolution and Climate, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark,

    David Nogués-Bravo, Katharine A. Marske, Michael K. Borregaard & Carsten Rahbek

  3. Smithsonian Tropical Research Institute, Tupper Building, 401 Balboa, Ancón, Punamá, República de Panamá ,

    Andrew Ugan

  4. Departments of Integrative Biology and Statistics, University of California, Berkeley, 4098 VLSB, Berkeley, California 94720, USA,

    Rasmus Nielsen

  5. Department of Biology, University of Copenhagen, Ole Maaloes Vej 5, DK-2200, Denmark,

    Rasmus Nielsen

  6. School of Biological Sciences, University of Sydney, New South Wales 2006, Australia ,

    Simon Y. W. Ho

  7. Department of Anthropology, Center for the Study of the First Americans, Texas A&M University, College Station, 77843, Texas, USA

    Ted Goebel & Kelly E. Graf

  8. Department of Sociology and Anthropology, Missouri State University, 901 South National, Springfield, Missouri 65807, USA,

    David Byers

  9. Department of Evolutionary Biology, Uppsala University, 75236 Uppsala, Sweden,

    Jennifer A. Leonard

  10. Conservation and Evolutionary Genetics Group, Estación Biológica de Doñana (EBD-CSIC), Avenida Américo Vespucio, 41092 Seville, Spain ,

    Jennifer A. Leonard

  11. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 90095, California, USA

    Klaus-Peter Koepfli & Robert K. Wayne

  12. Laboratory of Genomic Diversity, National Cancer Institute, Building 560, Room 11-33, Frederick, Maryland 21702, USA ,

    Klaus-Peter Koepfli

  13. Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta T6G 2E3, Canada,

    Duane Froese

  14. Department of Tourism and Culture, Government of Yukon, Yukon Palaeontology Program, PO Box 2703 L2A, Whitehorse, Yukon Territory Y1A 2C6, Canada,

    Grant Zazula

  15. Stafford Research Inc., 200 Acadia Avenue, Lafayette, 80026, Colorado, USA

    Thomas W. Stafford

  16. Department of Earth and Environment, Mount Holyoke College, 50 College Street, South Hadley, 01075, Massachusetts, USA

    Persaram Batra

  17. School of Earth and Environment, University of Leeds, Woodhouse Lane, Leeds, West Yorkshire LS2 9JT, UK ,

    Alan M. Haywood

  18. School of Geographical Sciences, University of Bristol, University Road, Bristol BS8 1SS, UK ,

    Joy S. Singarayer & Paul J. Valdes

  19. Diamond and Precious Metals Geology Institute, Siberian Branch of Russian Academy of Sciences, 39 Prospect Lenina, 677891 Yakutsk, Russia ,

    Gennady Boeskorov

  20. Royal Alberta Museum, Edmonton, T5N 0M6, Alberta, Canada

    James A. Burns

  21. The Manitoba Museum, Winnipeg, R3B 0N2, Manitoba, Canada

    James A. Burns

  22. North-East Science Station, Pacific Institute for Geography, Far East Branch of Russian Academy of Sciences, 2 Malinovy Yar Street, 678830 Chersky, Russia ,

    Sergey P. Davydov

  23. Museum of Natural and Cultural History, 1224 University of Oregon, Eugene, 97403-1224, Oregon, USA

    Dennis L. Jenkins

  24. Institute of Plant and Animal Ecology, Ural Branch of the Russian Academy of Sciences, 8 Marta Street, 202, 620144 Ekaterinburg, Russia ,

    Pavel Kosintsev

  25. Moscow State University, Vorob’evy Gory, 119899 Moscow, Russia ,

    Tatyana Kuznetsova

  26. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan, 430074, Hubei, China

    Xulong Lai

  27. University of Kansas Museum of Natural History, University of Kansas, Lawrence, 66045, Kansas, USA

    Larry D. Martin

  28. Park Museum Management Program, National Park Service, 1201 Oakridge Drive, Suite 150, Fort Collins, Colorado 80525, USA ,

    H. Gregory McDonald

  29. Natural History Museum, Rotterdam, c/o Gudumholm 41, 2133 HG Hoofddorp, Netherlands ,

    Dick Mol

  30. Bioinformatics Research Centre (BiRC), Aarhus University, C.F. Møllers Allé 8, DK-8000 Aarhus C, Denmark ,

    Kasper Munch

  31. Regierungspräsidium Stuttgart, Landesamt für Denkmalpflege, Stromeyersdorfstrasse 3, D-78467 Konstanz, Germany ,

    Elisabeth Stephan

  32. Zoological Institute of Russian Academy of Sciences, Universitetskaya nab. 1, 199034 Saint-Petersburg, Russia ,

    Mikhail Sablin & Alexei Tikhonov

  33. Department of Landscape Ecology, Christian-Albrechts-University of Kiel, Institute for Nature and Resource Conservation, Olshausenstrasse 40, 24098 Kiel, Germany,

    Robert S. Sommer

  34. Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky Prospect, 119071 Moscow, Russia ,

    Taras Sipko & Andrei Sher

  35. Division of Geological Sciences, San Bernardino County Museum, 2024 Orange Tree Lane, Redlands, California 92374, USA,

    Eric Scott

  36. Departments of Biomathematics and Human Genetics, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, California 90095, USA,

    Marc A. Suchard

  37. Department of Biostatistics, UCLA School of Public Health, University of California, Los Angeles, Los Angeles, California 90095, USA,

    Marc A. Suchard

  38. Museum of Cultural History, University of Oslo, St. Olavsgate 29, Postboks 6762 St. Olavsplass, 0130 Oslo, Norway ,

    Rane Willerslev

  39. Australian Centre for Ancient DNA, The University of Adelaide, South Australia 5005, Australia ,

    Alan Cooper

  40. Department of Biology (Area 2), The University of York, Wentworth Way, Heslington, York YO10 5DD, UK,

    Michael Hofreiter

  41. Department of Biology, The Pennsylvania State University, 326 Mueller Laboratory, University Park, 16802, Pennsylvania, USA

    Beth Shapiro

  42. Department of Anthropology, University of Utah, 271N1400E, Salt Lake City, 84112-0060, Utah, USA

    Andrew Ugan

  43. Museo de Historia Natural de San Rafael, (5600) Parque Mariano Moveno, San Rafael, Mendoza, Argentina

    Andrew Ugan

Authors
  1. Eline D. Lorenzen
  2. David Nogués-Bravo
  3. Ludovic Orlando
  4. Jaco Weinstock
  5. Jonas Binladen
  6. Katharine A. Marske
  7. Andrew Ugan
  8. Michael K. Borregaard
  9. M. Thomas P. Gilbert
  10. Rasmus Nielsen
  11. Simon Y. W. Ho
  12. Ted Goebel
  13. Kelly E. Graf
  14. David Byers
  15. Jesper T. Stenderup
  16. Morten Rasmussen
  17. Paula F. Campos
  18. Jennifer A. Leonard
  19. Klaus-Peter Koepfli
  20. Duane Froese
  21. Grant Zazula
  22. Thomas W. Stafford
  23. Kim Aaris-Sørensen
  24. Persaram Batra
  25. Alan M. Haywood
  26. Joy S. Singarayer
  27. Paul J. Valdes
  28. Gennady Boeskorov
  29. James A. Burns
  30. Sergey P. Davydov
  31. James Haile
  32. Dennis L. Jenkins
  33. Pavel Kosintsev
  34. Tatyana Kuznetsova
  35. Xulong Lai
  36. Larry D. Martin
  37. H. Gregory McDonald
  38. Dick Mol
  39. Morten Meldgaard
  40. Kasper Munch
  41. Elisabeth Stephan
  42. Mikhail Sablin
  43. Robert S. Sommer
  44. Taras Sipko
  45. Eric Scott
  46. Marc A. Suchard
  47. Alexei Tikhonov
  48. Rane Willerslev
  49. Robert K. Wayne
  50. Alan Cooper
  51. Michael Hofreiter
  52. Andrei Sher
  53. Beth Shapiro
  54. Carsten Rahbek
  55. Eske Willerslev

Contributions

E.W. conceived and headed the overall project. C.R. headed the species distribution modelling and range measurements. E.D.L. and J.T.S. extracted, amplified and sequenced the reindeer DNA sequences. J.B. extracted, amplified and sequenced the woolly rhinoceros DNA sequences; M.H. generated part of the woolly rhinoceros data. J.W., K.-P.K., J.L. and R.K.W. generated the horse DNA sequences; A.C. generated part of the horse data. L.O., E.D.L. and B.S. analysed the genetic data, with input from R.N., K.M., M.A.S. and S.Y.W.H. Palaeoclimate simulations were provided by P.B., A.M.H, J.S.S. and P.J.V. The directly dated spatial latitudinal/longitudinal megafauna locality information was collected by E.D.L., K.A.M., D.N.-B., D.B. and A.U.; K.A.M. and D.N.-B. performed the species distribution modelling and range measurements. M.B. carried out the gene–climate correlation. A.U. and D.B. assembled the human Upper Palaeolithic sites from Eurasia. T.G. and K.E.G. assembled the archaeofaunal assemblages from Siberia. A.U. analysed the spatial overlap of humans and megafauna and the archaeofaunal assemblages. E.D.L., L.O., B.S., K.A.M., D.N.-B., M.K.B., A.U., T.G. and K.E.G. wrote theSupplementary Information. D.F., G.Z., T.W.S., K.A.-S., G.B., J.A.B., D.L.J., P.K., T.K., X.L., L.D.M., H.G.M., D.M., M.M., E.S., M.S., R.S.S., T.S., E.S., A.T., R.W. and A.C. provided the megafauna samples used for ancient DNA analysis. E.D.L. produced the figures. E.D.L, L.O. and E.W. wrote most of the manuscript, with input from B.S., M.H., D.N.-B., K.A.M., M.T.P.G., C.R., R.K.W, A.U. and the remaining authors.

Corresponding author

Correspondence toEske Willerslev.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Sections 1-6 (see page 1 for details), Supplementary Figures with legends, Supplementary Tables and additional references. (PDF 18259 kb)

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Lorenzen, E., Nogués-Bravo, D., Orlando, L.et al. Species-specific responses of Late Quaternary megafauna to climate and humans.Nature479, 359–364 (2011). https://doi.org/10.1038/nature10574

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Editorial Summary

Ice Age exits

The charismatic megafauna of the Ice Age are either extinct or much restricted in range. Was their fate sealed by climate change or overhunting by humans? A detailed survey of the last days of mammoths and woolly rhinos, as well as horses, bison, reindeer and musk oxen, based on radiocarbon dating and ancient DNA, shows that the response of each creature to its oncoming fate was idiosyncratic. The mass extinction of megafauna at the close of the Pleistocene epoch cannot be attributed either solely to climate change or to overhunting, but to a combination of many factors that are unique to each species.

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