Letter | Published:

Genomic analyses inform on migration events during the peopling of Eurasia

Nature volume 538, pages 238242 (13 October 2016) | Download Citation

Abstract

High-coverage whole-genome sequence studies have so far focused on a limited number1 of geographically restricted populations2,3,4,5, or been targeted at specific diseases, such as cancer6. Nevertheless, the availability of high-resolution genomic data has led to the development of new methodologies for inferring population history7,8,9 and refuelled the debate on the mutation rate in humans10. Here we present the Estonian Biocentre Human Genome Diversity Panel (EGDP), a dataset of 483 high-coverage human genomes from 148 populations worldwide, including 379 new genomes from 125 populations, which we group into diversity and selection sets. We analyse this dataset to refine estimates of continent-wide patterns of heterozygosity, long- and short-distance gene flow, archaic admixture, and changes in effective population size through time as well as for signals of positive or balancing selection. We find a genetic signature in present-day Papuans that suggests that at least 2% of their genome originates from an early and largely extinct expansion of anatomically modern humans (AMHs) out of Africa. Together with evidence from the western Asian fossil record11, and admixture between AMHs and Neanderthals predating the main Eurasian expansion12, our results contribute to the mounting evidence for the presence of AMHs out of Africa earlier than 75,000 years ago.

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Accessions

Primary accessions

European Nucleotide Archive

Data deposits

The newly sequenced genomes are part of the Estonian Biocentre human Genome Diversity Panel (EGDP) and were deposited in the ENA archive under accession number PRJEB12437 and are also freely available through the Estonian Biocentre website (www.ebc.ee/free_data)

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Acknowledgements

Support was provided by: Estonian Research Infrastructure Roadmap grant no 3.2.0304.11-0312; Australian Research Council Discovery grants (DP110102635 and DP140101405) (D.M.L., M.W. and E.W.); Danish National Research Foundation; the Lundbeck Foundation and KU2016 (E.W.); ERC Starting Investigator grant (FP7 - 261213) (T.K.); Estonian Research Council grant PUT766 (G.C. and M.K.); EU European Regional Development Fund through the Centre of Excellence in Genomics to Estonian Biocentre (R.V.; M.Me. and A.Me.), and Centre of Excellence for Genomics and Translational Medicine Project No. 2014-2020.4.01.15-0012 to EGC of UT (A.Me.) and EBC (M.Me.); Estonian Institutional Research grant IUT24-1 (L.S., M.J., A.K., B.Y., K.T., C.B.M., Le.S., H.Sa., S.L., D.M.B., E.M., R.V., G.H., M.K., G.C., T.K. and M.Me.) and IUT20-60 (A.Me.); French Ministry of Foreign and European Affairs and French ANR grant number ANR-14-CE31-0013-01 (F.-X.R.); Gates Cambridge Trust Funding (E.J.); ICG SB RAS (No. VI.58.1.1) (D.V.L.); Leverhulme Programme grant no. RP2011-R-045 (A.B.M., P.G. and M.G.T.); Ministry of Education and Science of Russia; Project 6.656.2014/K (S.A.F.); NEFREX grant funded by the European Union (People Marie Curie Actions; International Research Staff Exchange Scheme; call FP7-PEOPLE-2012-IRSES-number 318979) (M.Me., G.H. and M.K.); NIH grants 5DP1ES022577 05, 1R01DK104339-01, and 1R01GM113657-01 (S.Tis.); Russian Foundation for Basic Research (grant N 14-06-00180a) (M.G.); Russian Foundation for Basic Research; grant 16-04-00890 (O.B. and E.B); Russian Science Foundation grant 14-14-00827 (O.B.); The Russian Foundation for Basic Research (14-04-00725-a), The Russian Humanitarian Scientific Foundation (13-11-02014) and the Program of the Basic Research of the RAS Presidium “Biological diversity” (E.K.K.); Wellcome Trust and Royal Society grant WT104125AIA & the Bristol Advanced Computing Research Centre (http://www.bris.ac.uk/acrc/) (D.J.L.); Wellcome Trust grant 098051 (Q.A.; C.T.-S. and Y.X.); Wellcome Trust Senior Research Fellowship grant 100719/Z/12/Z (M.G.T.); Young Explorers Grant from the National Geographic Society (8900-11) (C.A.E.); ERC Consolidator Grant 647787 ‘LocalAdaptatio’ (A.Ma.); Program of the RAS Presidium “Basic research for the development of the Russian Arctic” (B.M.); Russian Foundation for Basic Research grant 16-06-00303 (E.B.); a Rutherford Fellowship (RDF-10-MAU-001) from the Royal Society of New Zealand (M.P.C.).

Author information

Author notes

    • Luca Pagani
    • , Daniel John Lawson
    • , Evelyn Jagoda
    • , Alexander Mörseburg
    • , Anders Eriksson
    • , Richard Villems
    • , Eske Willerslev
    • , Toomas Kivisild
    •  & Mait Metspalu

    These authors contributed equally to this work.

Affiliations

  1. Estonian Biocentre, 51010 Tartu, Estonia

    • Luca Pagani
    • , Georgi Hudjashov
    • , Lauri Saag
    • , Mari Järve
    • , Monika Karmin
    • , Alena Kushniarevich
    • , Bayazit Yunusbayev
    • , Kristiina Tambets
    • , Chandana Basu Mallick
    • , Hovhannes Sahakyan
    • , Gyaneshwer Chaubey
    • , Sergei Litvinov
    • , Doron M. Behar
    • , Ene Metspalu
    • , Richard Villems
    • , Toomas Kivisild
    •  & Mait Metspalu
  2. Department of Archaeology and Anthropology, University of Cambridge, Cambridge CB2 1QH, UK

    • Luca Pagani
    • , Evelyn Jagoda
    • , Alexander Mörseburg
    • , Florian Clemente
    • , Alexia Cardona
    • , Sarah Kaewert
    • , Charlotte Inchley
    • , Christiana L. Scheib
    • , Florin Mircea Iliescu
    • , Christina A. Eichstaedt
    •  & Toomas Kivisild
  3. Department of Biological, Geological and Environmental Sciences, University of Bologna, Via Selmi 3, 40126 Bologna, Italy

    • Luca Pagani
  4. Integrative Epidemiology Unit, School of Social and Community Medicine, University of Bristol, Bristol BS8 2BN, UK

    • Daniel John Lawson
  5. Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Evelyn Jagoda
  6. Integrative Systems Biology Lab, Division of Biological and Environmental Sciences & Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia

    • Anders Eriksson
  7. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK

    • Anders Eriksson
    •  & Andrea Manica
  8. Estonian Genome Center, University of Tartu, 51010 Tartu, Estonia

    • Mario Mitt
    • , Reedik Mägi
    • , Evelin Mihailov
    •  & Andres Metspalu
  9. Department of Biotechnology, Institute of Molecular and Cell Biology, University of Tartu, 51010 Tartu, Estonia

    • Mario Mitt
    •  & Andres Metspalu
  10. Institut de Biologie Computationnelle, Université Montpellier 2, 34095 Montpellier, France

    • Florian Clemente
  11. Department of Psychology, University of Auckland, Auckland 1142, New Zealand

    • Georgi Hudjashov
    •  & Monika Karmin
  12. Statistics and Bioinformatics Group, Institute of Fundamental Sciences, Massey University, 4442 Palmerston North, New Zealand

    • Georgi Hudjashov
    •  & Murray P. Cox
  13. Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802, USA

    • Michael DeGiorgio
  14. Institute for Human Genetics, University of California, San Francisco, California 94143, USA

    • Jeffrey D. Wall
  15. MRC Epidemiology Unit, University of Cambridge, Institute of Metabolic Science, Box 285, Addenbrooke’s Hospital, Hills Road, Cambridge CB2 0QQ, UK

    • Alexia Cardona
  16. School of Life Sciences, Arizona State University, Tempe, Arizona 85287, USA

    • Melissa A. Wilson Sayres
  17. Center for Evolution and Medicine, The Biodesign Institute, Tempe, Arizona 85287, USA

    • Melissa A. Wilson Sayres
  18. Department of Evolutionary Biology, Institute of Molecular and Cell Biology, University of Tartu, 51010 Tartu, Estonia

    • Monika Karmin
    • , Lehti Saag
    • , Ene Metspalu
    •  & Richard Villems
  19. Mathematical Sciences, University of Southampton, Southampton SO17 1BJ, UK

    • Guy S. Jacobs
  20. Institute for Complex Systems Simulation, University of Southampton, Southampton SO17 1BJ, UK

    • Guy S. Jacobs
  21. Division of Biological Sciences, University of Montana, Missoula, Montana 59812, USA

    • Tiago Antao
  22. Institute of Genetics and Cytology, National Academy of Sciences, BY-220072 Minsk, Belarus

    • Alena Kushniarevich
  23. The Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK

    • Qasim Ayub
    • , Chris Tyler-Smith
    •  & Yali Xue
  24. Institute of Biochemistry and Genetics, Ufa Scientific Center of RAS, 450054 Ufa, Russia

    • Bayazit Yunusbayev
    • , Alexandra Karunas
    • , Sergei Litvinov
    • , Rita Khusainova
    • , Vita Akhmetova
    • , Irina Khidiyatova
    •  & Elza K. Khusnutdinova
  25. Kuban State Medical University, 350040 Krasnodar, Russia

    • Elvira Pocheshkhova
  26. Scientific Research Center of the Caucasian Ethnic Groups, St. Andrews Georgian University, 0162 Tbilisi, Georgia

    • George Andriadze
  27. Center for GeoGenetics, University of Copenhagen, 1350 Copenhagen, Denmark

    • Craig Muller
    • , Rasmus Nielsen
    •  & Eske Willerslev
  28. Research Centre for Human Evolution, Environmental Futures Research Institute, Griffith University, Nathan, Queensland 4111, Australia

    • Michael C. Westaway
    •  & David M. Lambert
  29. Center of Molecular Diagnosis and Genetic Research, University Hospital of Obstetrics and Gynecology, 1000 Tirana, Albania

    • Grigor Zoraqi
  30. Center of High Technology, Academy of Sciences, 100047 Tashkent, Uzbekistan

    • Shahlo Turdikulova
  31. Institute of Bioorganic Chemistry Academy of Science, 100047 Tashkent, Uzbekistan

    • Dilbar Dalimova
  32. L.N. Gumilyov Eurasian National University, 010008 Astana, Kazakhstan

    • Zhaxylyk Sabitov
  33. Centre for Advanced Research in Sciences (CARS), DNA Sequencing Research Laboratory, University of Dhaka, Dhaka-1000, Bangladesh

    • Gazi Nurun Nahar Sultana
  34. Department of Genetics, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6145, USA

    • Joseph Lachance
  35. School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia 30332, USA

    • Joseph Lachance
  36. Departments of Genetics and Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6313, USA

    • Sarah Tishkoff
  37. DNcode laboratories, 117623 Moscow, Russia

    • Kuvat Momynaliev
  38. Institute of Molecular Biology and Medicine, 720040 Bishkek, Kyrgyzstan

    • Jainagul Isakova
  39. Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, 630090 Novosibirsk, Russia

    • Larisa D. Damba
    • , Marina Gubina
    • , Daria V. Lichman
    • , Mikhail Voevoda
    •  & Ludmila P. Osipova
  40. Mongolian Academy of Medical Sciences, 210620 Ulaanbaatar, Mongolia

    • Pagbajabyn Nymadawa
  41. Northern State Medical University, 163000 Arkhangelsk, Russia

    • Irina Evseeva
  42. Anthony Nolan, The Royal Free Hospital, Pond Street, London NW3 2QG, UK

    • Irina Evseeva
  43. V. N. Karazin Kharkiv National University, 61022 Kharkiv, Ukraine

    • Lubov Atramentova
    •  & Olga Utevska
  44. Evolutionary Medicine group, Laboratoire d’Anthropologie Moléculaire et Imagerie de Synthèse, UMR 5288, Centre National de la Recherche Scientifique, Université de Toulouse 3, Toulouse 31073, France

    • François-Xavier Ricaut
    • , Nicolas Brucato
    •  & Thierry Letellier
  45. Genome Diversity and Diseases Laboratory, Eijkman Institute for Molecular Biology, 10430 Jakarta, Indonesia

    • Herawati Sudoyo
  46. Department of Molecular Genetics, Yakut Scientific Centre of Complex Medical Problems, 677027 Yakutsk, Russia

    • Nikolay A. Barashkov
    •  & Sardana A. Fedorova
  47. Laboratory of Molecular Biology, Institute of Natural Sciences, M.K. Ammosov North-Eastern Federal University, 677027 Yakutsk, Russia

    • Nikolay A. Barashkov
    •  & Sardana A. Fedorova
  48. Genos DNA laboratory, 10000 Zagreb, Croatia

    • Vedrana Škaro
  49. University of Osijek, Medical School, 31000 Osijek, Croatia

    • Vedrana Škaro
    •  & Dragan Primorac
  50. Center for Genomics and Transcriptomics, CeGaT, GmbH, D-72076 Tübingen, Germany

    • Lejla Mulahasanovic´
  51. St. Catherine Specialty Hospital, 49210 Zabok and 10000 Zagreb, Croatia

    • Dragan Primorac
  52. Eberly College of Science, The Pennsylvania State University, University Park, Pennsylvania 16802, USA

    • Dragan Primorac
  53. University of Split, Medical School, 21000 Split, Croatia

    • Dragan Primorac
  54. Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences, Republic of Armenia, 7 Hasratyan Street, 0014 Yerevan, Armenia

    • Hovhannes Sahakyan
    •  & Levon Yepiskoposyan
  55. Department of Applied Social Sciences, University of Winchester, Sparkford Road, Winchester SO22 4NR, UK

    • Maru Mormina
  56. Thoraxklinik Heidelberg, University Hospital Heidelberg, 69120 Heidelberg, Germany

    • Christina A. Eichstaedt
  57. Novosibirsk State University, 630090 Novosibirsk, Russia

    • Daria V. Lichman
    • , Mikhail Voevoda
    •  & Ludmila P. Osipova
  58. RIPAS Hospital, Bandar Seri Begawan, BE1518 Brunei

    • Syafiq Abdullah
  59. National Cancer Centre Singapore, 169610 Singapore

    • Joseph T. S. Wee
  60. Department of Genetics and Fundamental Medicine, Bashkir State University, 450000 Ufa, Russia

    • Alexandra Karunas
    • , Sergei Litvinov
    • , Rita Khusainova
    • , Natalya Ekomasova
    • , Irina Khidiyatova
    •  & Elza K. Khusnutdinova
  61. Department of Genetics and Bioengineering. Faculty of Engineering and Information Technologies, International Burch University, 71000 Sarajevo, Bosnia and Herzegovina

    • Damir Marjanović
  62. Institute for Anthropological Researches, 10000 Zagreb, Croatia

    • Damir Marjanović
  63. Research Centre for Medical Genetics, Russian Academy of Sciences, Moscow 115478, Russia

    • Elena Balanovska
    •  & Oleg Balanovsky
  64. Genetics Laboratory, Institute of Biological Problems of the North, Russian Academy of Sciences, 685000 Magadan, Russia

    • Miroslava Derenko
    •  & Boris Malyarchuk
  65. Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, 630009 Novosibirsk, Russia

    • Mikhail Voevoda
  66. Leverhulme Centre for Human Evolutionary Studies, Department of Archaeology and Anthropology, University of Cambridge, Cambridge CB2 1QH, UK

    • Marta Mirazón Lahr
  67. Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK

    • Pascale Gerbault
    •  & Mark G. Thomas
  68. Department of Archaeology, University of Papua New Guinea, University PO Box 320, 134 NCD, Papua New Guinea

    • Matthew Leavesley
  69. College of Arts, Society and Education, James Cook University, PO Box 6811, Cairns, Queensland 4870, Australia

    • Matthew Leavesley
  70. Department of Anthropology, University College London, London WC1H 0BW, UK

    • Andrea Bamberg Migliano
  71. Max Planck Institute for the Science of Human History, Kahlaische Strasse 10, D-07743 Jena, Germany

    • Michael Petraglia
  72. Vavilov Institute for General Genetics, Russian Academy of Sciences, 119333 Moscow, Russia

    • Oleg Balanovsky
  73. Department of Integrative Biology, University of California Berkeley, Berkeley 94720, California, USA

    • Rasmus Nielsen
  74. Estonian Academy of Sciences, 6 Kohtu Street, Tallinn 10130, Estonia

    • Richard Villems

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  98. Search for Mait Metspalu in:

Contributions

R.V., E.W., T.K. and M.Me. conceived the study. A.K., K.T., C.B.M., Le.S., E.P., G.A., C.M., M.W., D.L., G.Z., S.T., D.D., Z.S., G.N.N.S., K.M., J.I., L.D.D., M.G., P.N., I.E., L.At., O.U., F.-X.R., N.B., H.S., T.L., M.P.C., N.A.B., V.S., L.A., D.Pr., H.Sa., M.Mo., C.A.E., D.V.L., S.A., G.C., J.T.S.W., E.Mi., A.Ka., S.L., R.K., N.T., V.A., I.K., D.M., L.Y., D.M.B., E.B., A.Me., M.D., B.M., M.V., S.A.F., L.P.O., M.Mi., M.L., A.B.M., O.B., E.K.K, E.M., M.G.T. and E.W. conducted anthropological research and/or sample collection and management. J.L. and S.Ti. provided access to data. L.P., D.J.L, E.J., A.Mo., A.E., M.Mi., F.C., G.H., M.D., L.S., J.W., A.C., R.M., M.A.W.S., S.K., C.I., C.L.S., M.J., M.K., G.S.J., T.A., F.M.I., A.K., Q.A., C.T.-S., Y.X., B.Y., C.B.M., T.K. and M.Me. analysed data. L.P., D.J.L., E.J., A.Mo., L.S., M.K., K.T., C.B.M., Le.S., G.C., M.Mi., P.G., M.L., A.B.M., M.P., E.M., M.G.T., A.Ma., R.N., R.V., E.W., T.K. and M.Me. contributed to the interpretation of results. L.P., D.J.L., E.J., A.Mo., A.E., F.C., G.H., M.D., A.C., M.A.W.S., B.Y., J.L., S.Ti., M.Mi., P.G., M.L., A.B.M., M.P., M.G.T., A.Ma., R.N., R.V., E.W., T.K. and M.Me. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Luca Pagani or Toomas Kivisild or Mait Metspalu.

Reviewer Information Nature thanks R. Dennell and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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