Letter | Published:

Ancient human genomes suggest three ancestral populations for present-day Europeans

Nature 513, 409–413 (18 September 2014) | Download Citation

Subjects

Abstract

We sequenced the genomes of a ∼7,000-year-old farmer from Germany and eight ∼8,000-year-old hunter-gatherers from Luxembourg and Sweden. We analysed these and other ancient genomes1,2,3,4 with 2,345 contemporary humans to show that most present-day Europeans derive from at least three highly differentiated populations: west European hunter-gatherers, who contributed ancestry to all Europeans but not to Near Easterners; ancient north Eurasians related to Upper Palaeolithic Siberians3, who contributed to both Europeans and Near Easterners; and early European farmers, who were mainly of Near Eastern origin but also harboured west European hunter-gatherer related ancestry. We model these populations’ deep relationships and show that early European farmers had ∼44% ancestry from a ‘basal Eurasian’ population that split before the diversification of other non-African lineages.

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Accessions

Primary accessions

European Nucleotide Archive

Data deposits

The aligned sequences are available through the European Nucleotide Archive under accession number PRJEB6272. The fully public version of the Human Origins dataset can be found at (http://genetics.med.harvard.edu/reichlab/Reich_Lab/Datasets.html). The full version of the dataset (including additional samples) is available to researchers who send a signed letter to D.R. indicating that they will abide by specified usage conditions (Supplementary Information section 9).

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Acknowledgements

We thank the 1,615 volunteers from 147 diverse populations who donated DNA samples and whose genetic data are newly reported in this study. We are grateful to C. Beall, N. Bradman, A. Gebremedhin, D. Labuda, M. Nelis and A. Di Rienzo for sharing DNA samples; to D. Weigel, C. Lanz, V. Schünemann, P. Bauer and O. Riess for support and access to DNA sequencing facilities; to P. Johnson for advice on contamination estimation; to G. Hellenthal for help with the ChromoPainter software; and to P. Skoglund for sharing graphics software. We thank K. Nordtvedt for alerting us to newly discovered Y-chromosome SNPs. We downloaded the POPRES data from dbGaP at (http://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/study.cgi?study_id=phs000145.v4.p2) through dbGaP accession number phs000145.v1.p2. We thank all the volunteers who donated DNA. We thank the staff of the Unità Operativa Complessa di Medicina Trasfusionale, Azienda Ospedaliera Umberto I, Siracusa, Italy for assistance in sample collection; and The National Laboratory for the Genetics of Israeli Populations for facilitating access to DNA. We thank colleagues at the Applied Genomics at the Children’s Hospital of Philadelphia, especially H. Hakonarson, C. Kim, K. Thomas, and C. Hou, for genotyping samples on the Human Origins array. J.Kr., A.M. and C.P. are grateful for support from DFG grant number KR 4015/1-1, the Carl-Zeiss Foundation and the Baden Württemberg Foundation. S.P., G.R., Q.F., C.F., K.P., S.C. and J.Ke. acknowledge support from the Presidential Innovation Fund of the Max Planck Society. G.R. was supported by an NSERC fellowship. J.G.S. acknowledges use of the Extreme Science and Engineering Discovery Environment (XSEDE), which is supported by NSF grant number OCI-1053575. E.B. and O.B. were supported by RFBR grants 13-06-00670, 13-04-01711, 13-04-90420 and by the Molecular and Cell Biology Program of the Presidium, Russian Academy of Sciences. B.M. was supported by grants OTKA 73430 and 103983. A.Saj. was supported by a Finnish Professorpool (Paulo Foundation) Grant. The Lithuanian sampling was supported by the LITGEN project (VP1-3.1-ŠMM-07-K-01-013), funded by the European Social Fund under the Global Grant Measure. A.S. was supported by Spanish grants SAF2011-26983 and EM 2012/045. O.U. was supported by Ukrainian SFFS grant F53.4/071. S.A.T. was supported by NIH Pioneer Award 8DP1ES022577-04 and NSF HOMINID award BCS-0827436. K.T. was supported by an Indian CSIR Network Project (GENESIS: BSC0121). L.S. was supported by an Indian CSIR Bhatnagar Fellowship. R.V., M.M., J.P. and E.M. were supported by the European Union Regional Development Fund through the Centre of Excellence in Genomics to the Estonian Biocentre and University of Tartu and by an Estonian Basic Research grant SF0270177As08. M.M. was additionally supported by Estonian Science Foundation grant number 8973. J.G.S. and M.S. were supported by NIH grant GM40282. P.H.S. and E.E.E. were supported by NIH grants HG004120 and HG002385. D.R. and N.P. were supported by NSF HOMINID award BCS-1032255 and NIH grant GM100233. D.R. and E.E.E. are Howard Hughes Medical Institute investigators. This project has been funded in part with federal funds from the National Cancer Institute, National Institutes of Health, under contract HHSN26120080001E. The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government. This Research was supported in part by the Intramural Research Program of the NIH, National Cancer Institute, Center for Cancer Research.

Author information

    • Theologos Loukidis
    •  & Lalji Singh

    Present addresses: Amgen, 33 Kazantzaki Str, Ilioupolis 16342, Athens, Greece (T.L.); Banaras Hindu University, Varanasi 221 005, India (L.S.).

    • Ruslan Ruizbakiev

    Deceased.

Affiliations

  1. Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA.

    • Iosif Lazaridis
    • , Swapan Mallick
    • , Qiaomei Fu
    • , Susanne Nordenfelt
    • , Heng Li
    • , Nadin Rohland
    •  & David Reich

  2. Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA.

    • Iosif Lazaridis
    • , Nick Patterson
    • , Swapan Mallick
    • , Bonnie Berger
    • , Susanne Nordenfelt
    • , Heng Li
    • , Nadin Rohland
    •  & David Reich

  3. Institute for Archaeological Sciences, University of Tübingen, Tübingen 72074, Germany.

    • Alissa Mittnik
    • , Kirsten I. Bos
    • , Cosimo Posth
    •  & Johannes Krause

  4. Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany.

    • Gabriel Renaud
    • , Sergi Castellano
    • , Qiaomei Fu
    • , Cesare de Filippo
    • , Kay Prüfer
    • , Susanna Sawyer
    • , Matthias Meyer
    • , Svante Pääbo
    •  & Janet Kelso

  5. Institute of Anthropology, Johannes Gutenberg University Mainz, Mainz D-55128, Germany.

    • Karola Kirsanow
    • , Ruth Bollongino
    •  & Joachim Burger

  6. Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA.

    • Peter H. Sudmant
    • , Joshua G. Schraiber
    •  & Evan E. Eichler

  7. Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA.

    • Joshua G. Schraiber
    • , William Klitz
    •  & Montgomery Slatkin

  8. Department of Mathematics and Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.

    • Mark Lipson
    •  & Bonnie Berger

  9. Archaeological Research Laboratory, Stockholm University, 114 18, Sweden.

    • Christos Economou

  10. Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, IVPP, CAS, Beijing 100049, China.

    • Qiaomei Fu

  11. Australian Centre for Ancient DNA and Environment Institute, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia.

    • Wolfgang Haak
    •  & Alan Cooper

  12. The Cultural Heritage Foundation, Västerås 722 12, Sweden.

    • Fredrik Hallgren
    •  & Elin Fornander

  13. National Museum of Natural History, L-2160, Luxembourg.

    • Dominique Delsate
    •  & Jean-Michel Guinet

  14. National Center of Archaeological Research, National Museum of History and Art, L-2345, Luxembourg.

    • Dominique Delsate

  15. Department of Paleoanthropology, Senckenberg Center for Human Evolution and Paleoenvironment, University of Tübingen, Tübingen D-72070, Germany.

    • Michael Francken

  16. State Office for Cultural Heritage Management Baden-Württemberg, Osteology, Konstanz D-78467, Germany.

    • Joachim Wahl

  17. Center for Global Health and Child Development, Kisumu 40100, Kenya.

    • George Ayodo

  18. Institutes of Evolution, Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, UK.

    • Hamza A. Babiker

  19. Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alkhod, Muscat 123, Oman.

    • Hamza A. Babiker

  20. Laboratorio de Genética Molecular Poblacional, Instituto Multidisciplinario de Biología Celular (IMBICE), CCT-CONICET & CICPBA, La Plata, B1906APO, Argentina.

    • Graciela Bailliet
    •  & Claudio M. Bravi

  21. Research Centre for Medical Genetics, Moscow 115478, Russia.

    • Elena Balanovska
    •  & Oleg Balanovsky

  22. Vavilov Institute for General Genetics, Moscow 119991, Russia.

    • Oleg Balanovsky

  23. Escuela de Biología, Universidad de Costa Rica, San José 2060, Costa Rica.

    • Ramiro Barrantes

  24. Institute of Biology, Research group GENMOL, Universidad de Antioquia, Medellín, Colombia.

    • Gabriel Bedoya

  25. Rambam Health Care Campus, Haifa 31096, Israel.

    • Haim Ben-Ami

  26. Department of Medical Genetics and Szentagothai Research Center, University of Pécs, Pécs H-7624, Hungary.

    • Judit Bene
    •  & Béla Melegh

  27. Al Akhawayn University in Ifrane (AUI), School of Science and Engineering, Ifrane 53000, Morocco.

    • Fouad Berrada

  28. Forensic Genetics Laboratory, Institute of Legal Medicine, Università Cattolica del Sacro Cuore, Rome 00168, Italy.

    • Francesca Brisighelli

  29. Department of Zoology, University of Oxford, Oxford OX1 3PS, UK.

    • George B. J. Busby
    •  & Cristian Capelli

  30. Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, UK.

    • George B. J. Busby

  31. Laboratorio di Genetica Molecolare, IRCCS Associazione Oasi Maria SS, Troina 94018, Italy.

    • Francesco Cali

  32. Belgorod State University, Belgorod 308015, Russia.

    • Mikhail Churnosov

  33. Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario M5G 1L5, Canada.

    • David E. C. Cole

  34. Servicio de Huellas Digitales Genéticas, School of Pharmacy and Biochemistry, Universidad de Buenos Aires, 1113 CABA, Argentina.

    • Daniel Corach

  35. Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia.

    • Larissa Damba
    • , Marina Gubina
    • , Ludmila Osipova
    • , Olga Posukh
    •  & Mikhail Voevoda

  36. Institute of Linguistics, University of Bern, Bern CH-3012, Switzerland.

    • George van Driem

  37. Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk 630090, Russia.

    • Stanislav Dryomov
    • , Elena B. Starikovskaya
    •  & Rem Sukernik

  38. Anthropologie Moléculaire et Imagerie de Synthèse, CNRS UMR 5288, Université Paul Sabatier Toulouse III, Toulouse 31000, France.

    • Jean-Michel Dugoujon

  39. North-Eastern Federal University and Yakut Research Center of Complex Medical Problems, Yakutsk 677013, Russia.

    • Sardana A. Fedorova

  40. Department of Human Genetics, University of Chicago, Chicago, Illinois 60637, USA.

    • Irene Gallego Romero
    •  & Aashish R. Jha

  41. ARL Division of Biotechnology, University of Arizona, Tucson, Arizona 85721, USA.

    • Michael Hammer

  42. Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York 11794, USA.

    • Brenna M. Henn

  43. Department of Clinical Science, University of Bergen, Bergen 5021, Norway.

    • Tor Hervig

  44. NextBio, Illumina, Santa Clara, California 95050, USA.

    • Ugur Hodoglugil

  45. Department of Medical Genetics, National Human Genome Center, Medical University Sofia, Sofia 1431, Bulgaria.

    • Sena Karachanak-Yankova
    • , Desislava Nesheva
    •  & Draga Toncheva

  46. Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa 450054, Russia.

    • Rita Khusainova
    • , Elza Khusnutdinova
    •  & Sergey Litvinov

  47. Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa 450074, Russia.

    • Rita Khusainova
    • , Elza Khusnutdinova
    •  & Sergey Litvinov

  48. College of Medicine, University of Arizona, Tucson, Arizona 85724, USA.

    • Rick Kittles

  49. Division of Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK.

    • Toomas Kivisild

  50. Department of Human and Medical Genetics, Vilnius University, Vilnius LT-08661, Lithuania.

    • Vaidutis Kučinskas
    •  & Ingrida Uktveryte

  51. Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia.

    • Alena Kushniarevich
    • , Sergey Litvinov
    • , Hovhannes Sahakyan
    • , Richard Villems
    •  & Mait Metspalu

  52. Translational Medicine and Neurogenetics, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch 67404, France.

    • Leila Laredj

  53. Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK.

    • Theologos Loukidis
    • , Mark G. Thomas
    •  & Andres Ruiz-Linares

  54. Gladstone Institutes, San Francisco, California 94158, USA.

    • Robert W. Mahley

  55. Department of Evolutionary Biology, University of Tartu, Tartu 51010, Estonia.

    • Ene Metspalu
    • , Jüri Parik
    •  & Richard Villems

  56. Centro de Investigaciones Biomédicas de Guatemala, Ciudad de Guatemala, Guatemala.

    • Julio Molina

  57. Research Department, 23andMe, Mountain View, California 94043, USA.

    • Joanna Mountain

  58. Cultural Anthropology Program, University of Oulu, Oulu 90014, Finland.

    • Klemetti Näkkäläjärvi

  59. Department of Biochemistry, Muhimbili University of Health and Allied Sciences, Dar es Salaam 65001, Tanzania.

    • Thomas Nyambo

  60. Research Institute of Health, North-Eastern Federal University, Yakutsk 677000, Russia.

    • Fedor Platonov

  61. Dipartimento di Fisica e Chimica, Università di Palermo, Palermo 90128, Italy.

    • Valentino Romano

  62. Instituto de Alta Investigación, Universidad de Tarapacá, Arica 1000000, Chile.

    • Francisco Rothhammer

  63. Programa de Genética Humana ICBM Facultad de Medicina Universidad de Chile, Santiago 8320000, Chile.

    • Francisco Rothhammer

  64. Centro de Investigaciones del Hombre en el Desierto, Arica 1000000, Chile.

    • Francisco Rothhammer

  65. Centre for Population Health Sciences, The University of Edinburgh Medical School, Edinburgh EH8 9AG, UK.

    • Igor Rudan

  66. Institute of Immunology, Academy of Science, Tashkent 70000, Uzbekistan.

    • Ruslan Ruizbakiev

  67. Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan 0014, Armenia.

    • Hovhannes Sahakyan
    •  & Levon Yepiskoposyan

  68. Department of Forensic Medicine, Hjelt Institute, University of Helsinki, Helsinki 00014, Finland.

    • Antti Sajantila

  69. Institute of Applied Genetics, Department of Molecular and Medical Genetics, University of North Texas Health Science Center, Fort Worth, Texas 76107, USA.

    • Antti Sajantila

  70. Unidade de Xenética, Departamento de Anatomía Patolóxica e Ciencias Forenses, and Instituto de Ciencias Forenses, Grupo de Medicina Xenómica (GMX), Facultade de Medicina, Universidade de Santiago de Compostela, Galcia 15872, Spain.

    • Antonio Salas

  71. Research Fellow, Henry Stewart Group, Russell House, London WC1A 2HN, UK.

    • Ayele Tarekegn

  72. Institute of Bioorganic Chemistry Academy of Sciences Republic of Uzbekistan, Tashkent 100125, Uzbekistan.

    • Shahlo Turdikulova

  73. Department of Genetics and Cytology, V. N. Karazin Kharkiv National University, Kharkiv 61077, Ukraine.

    • Olga Utevska

  74. Instituto Boliviano de Biología de la Altura, Universidad Mayor de San Andrés, 591 2 La Paz, Bolivia.

    • René Vasquez
    •  & Mercedes Villena

  75. UniversidadAutonoma Tomás Frías, Potosí, Bolivia.

    • René Vasquez
    •  & Mercedes Villena

  76. Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, Novosibirsk 630089, Russia.

    • Mikhail Voevoda

  77. Novosibirsk State University, Novosibirsk 630090, Russia.

    • Mikhail Voevoda

  78. Basic Research Laboratory, NCI, NIH, Frederick National Laboratory, Leidos Biomedical, Frederick, Maryland 21702, USA.

    • Cheryl A. Winkler

  79. Lebanese American University, School of Medicine, Beirut 13-5053, Lebanon.

    • Pierre Zalloua

  80. Harvard School of Public Health, Boston, Massachusetts 02115, USA.

    • Pierre Zalloua

  81. Department of Medical Biology, University of Split, School of Medicine, Split 21000, Croatia.

    • Tatijana Zemunik

  82. Department of Biology and Genetics, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.

    • Sarah A. Tishkoff

  83. CSIR-Centre for Cellular and Molecular Biology, Hyderabad 500 007, India.

    • Lalji Singh
    •  & Kumarasamy Thangaraj

  84. Estonian Academy of Sciences, Tallinn 10130, Estonia.

    • Richard Villems

  85. Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona 08003, Spain.

    • David Comas

  86. Howard Hughes Medical Institute, University of Washington, Seattle, Washington 98195, USA.

    • Evan E. Eichler

  87. Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02115, USA.

    • David Reich

  88. Senckenberg Centre for Human Evolution and Palaeoenvironment, University of Tübingen, 72070 Tübingen, Germany.

    • Johannes Krause

  89. Max Planck Institut für Geschichte und Naturwissenschaften, Jena 07745, Germany.

    • Johannes Krause

Authors

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Contributions

B.B., E.E.E., J.Bu., M.S., S.P., J.Ke., D.R. and J.Kr. supervised the study. I.L., N.P., A.M., G.R., S.M., K.K., P.H.S., J.G.S., S.C., M.L., Q.F., H.L., C.dF., K.P., W.H., M.Met., M.Mey. and D.R. analysed genetic data. F.H., E.F., D.D., M.F., J.-M.G., J.W., A.C. and J.Kr. obtained human remains. A.M., C.E., R.Bo., K.I.B., S.S., C.P., N.R. and J.Kr. processed ancient DNA. I.L., N.P., S.N., N.R., G.A., H.A.B., G.Ba., E.B., O.B., R.Ba., G.Be., H.B.-A., J.Be., F.Be., C.M.B., F.Br., G.B.J.B., F.C., M.C., D.E.C.C., D.Cor., L.D., G.vD., S.D., J.-M.D., S.A.F., I.G.R., M.G., M.H., B.M.H., T.H., U.H., A.R.J., S.K.-Y., R.Kh., E.K., R.Ki., T.K., W.K., V.K., A.K., L.L., S.L., T.L., R.W.M., B.M., E.M., J.Mol., J.Mou., K.N., D.N., T.N., L.O., J.P., F.P., O. P., V.R., F.R., I.R., R.R., H.S., A.Saj., A.Sal., E.B.S., A.Tar., D.T., S.T., I.U., O.U., R.Va., M.Vi., M.Vo., C.A.W., L.Y., P.Z., T.Z., C.C., M.G.T., A.R.-L., S.A.T., L.S., K.T., R.Vi., D.Com., R.S., M.Met., S.P. and D.R. assembled the genotyping dataset. I.L., N.P., D.R. and J.Kr. wrote the manuscript with help from all co-authors.

Competing interests

U.H. is an employee of Illumina, T.L. is an employee of Amgen, and J.M. is an employee of 23andMe.

Corresponding authors

Correspondence to David Reich or Johannes Krause.

Extended data

Extended data figures

  1. 1.

    Photographs of analysed ancient samples.

  2. 2.

    Pairwise sequential Markovian coalescent (PSMC) analysis.

  3. 3.

    ADMIXTURE analysis (K = 2 to K = 20).

  4. 4.

    ANE ancestry is present in both Europe and the Near East but WHG ancestry is restricted to Europe, which cannot be due to a single admixture event.

  5. 5.

    MA1 is the best surrogate for ANE for which we have data.

  6. 6.

    The differential relatedness of west Eurasians to Stuttgart (EEF), Loschbour (WHG), and MA1 (ANE) cannot be explained by two-way mixture.

  7. 7.

    Evidence for Siberian gene flow into far north-eastern Europe.

Extended data tables

  1. 1.

    West Eurasians genotyped on the Human Origins array and key f statistics

  2. 2.

    Confirmation of key findings on transversions and on whole-genome sequence data

  3. 3.

    Admixture proportions for European populations

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Information Parts 1-19 – see Supplementary Contents for details.This file contains Supplementary Information Parts 1-19 – see Supplementary Contents for details.

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Publication history

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DOI

https://doi.org/10.1038/nature13673

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