Letter | Published:

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

Nature volume 513, pages 409413 (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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.

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).

References

  1. 1.

    et al. New insights into the Tyrolean Iceman’s origin and phenotype as inferred by whole-genome sequencing. Nature Commun. 3, 698 (2012)

  2. 2.

    et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014)

  3. 3.

    et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505, 87–91 (2014)

  4. 4.

    et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336, 466–469 (2012)

  5. 5.

    et al. Genetic discontinuity between local hunter-gatherers and Central Europe’s first farmers. Science 326, 137–140 (2009)

  6. 6.

    et al. Ancient DNA from European early Neolithic farmers reveals their Near Eastern affinities. PLoS Biol. 8, e1000536 (2010)

  7. 7.

    et al. Efficient moment-based inference of admixture parameters and sources of gene flow. Mol. Biol. Evol. 30, 1788–1802 (2013)

  8. 8.

    et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012)

  9. 9.

    et al. A complete mtDNA genome of an early modern human from Kostenki, Russia. Curr. Biol. 20, 231–236 (2010)

  10. 10.

    , , , & Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS ONE 7, e34131 (2012)

  11. 11.

    et al. Ancient DNA from the first European farmers in 7500-year-old Neolithic sites. Science 310, 1016–1018 (2005)

  12. 12.

    et al. Diet and the evolution of human amylase gene copy number variation. Nature Genet. 39, 1256–1260 (2007)

  13. 13.

    , & Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009)

  14. 14.

    , & Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006)

  15. 15.

    , , , & Reconstructing Indian population history. Nature 461, 489–494 (2009)

  16. 16.

    et al. Genetic evidence for recent population mixture in India. Am. J. Hum. Genet. 93, 422–438 (2013)

  17. 17.

    et al. Reconstructing Native American population history. Nature 488, 370–374 (2012)

  18. 18.

    et al. Gene flow from North Africa contributes to differential human genetic diversity in southern Europe. Proc. Natl Acad. Sci. USA. 110, 11791–11796 (2013)

  19. 19.

    et al. Reconstructing ancient mitochondrial DNA links between Africa and Europe. Genome Res. 22, 821–826 (2012)

  20. 20.

    et al. The history of African gene flow into southern Europeans, Levantines, and Jews. PLoS Genet. 7, e1001373 (2011)

  21. 21.

    & Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8, e1002967 (2012)

  22. 22.

    et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl Acad. Sci. USA 110, 2223–2227 (2013)

  23. 23.

    The Chronology of the Middle Paleolithic of the Levant 39–56 (Plenum Press, 1998)

  24. 24.

    et al. The southern route “out of Africa”: evidence for an early expansion of modern humans into Arabia. Science 331, 453–456 (2011)

  25. 25.

    et al. The Nubian Complex of Dhofar, Oman: an African middle stone age industry in Southern Arabia. PLoS ONE 6, e28239 (2011)

  26. 26.

    et al. The questionable contribution of the Neolithic and the Bronze Age to European craniofacial form. Proc. Natl Acad. Sci. USA 103, 242–247 (2006)

  27. 27.

    & Improving the accuracy and efficiency of identity-by-descent detection in population data. Genetics 194, 459–471 (2013)

  28. 28.

    & The geography of recent genetic ancestry across Europe. PLoS Biol. 11, e1001555 (2013)

  29. 29.

    , , & Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012)

  30. 30.

    et al. Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342, 257–261 (2013)

  31. 31.

    , & De l’ocre sur le crâne mésolithique (haplogroupe U5a) de Reuland-Loschbour (Grand-Duché de Luxembourg)? Bull. Soc. Préhist. Luxembourgeoise 31, 7–30 (2009)

  32. 32.

    & Ancient DNA extraction from bones and teeth. Nature Protocols 2, 1756–1762 (2007)

  33. 33.

    et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl Acad. Sci. USA 110, 15758–15763 (2013)

  34. 34.

    Häuser und absolute Datierung der Ältesten Bandkeramik (Habelt, 2005)

  35. 35.

    , , , & Improved DNA extraction from ancient bones using silica-based spin columns. Am. J. Phys. Anthropol. 105, 539–543 (1998)

  36. 36.

    & Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc.. (2010)

  37. 37.

    et al. A high-coverage genome sequence from an Archaic Denisovan individual. Science 338, 222–226 (2012)

  38. 38.

    et al. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res. 38, e87 (2010)

  39. 39.

    Analysis of high-throughput ancient DNA sequencing data. Methods Mol. Biol. 480, 197–228 (2012)

  40. 40.

    & Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009)

  41. 41.

    et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010)

  42. 42.

    , & Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS ONE 5, e14004 (2010)

  43. 43.

    et al. A Copernican reassessment of the human mitochondrial DNA tree from its root. Am. J. Hum. Genet. 90, 675–684 (2012)

  44. 44.

    et al. A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing. Cell 134, 416–426 (2008)

  45. 45.

    et al. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr. Biol. 23, 553–559 (2013)

  46. 46.

    et al. The complete genome sequence of a 45,000-year-old modern human from western Siberia. Nature (in the press)

  47. 47.

    et al. An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334, 94–98 (2011)

  48. 48.

    et al. HAPLOFIND: a new method for high-throughput mtDNA haplogroup assignment. Hum. Mutat. 34, 1189–1194 (2013)

  49. 49.

    et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739 (2011)

  50. 50.

    , , & Accurate sex identification of ancient human remains using DNA shotgun sequencing. J. Archaeol. Sci. 40, 4477–4482 (2013)

  51. 51.

    & BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214 (2007)

  52. 52.

    et al. Human paternal and maternal demographic histories: insights from high-resolution Y chromosome and mtDNA sequences. Preprint at bioRxiv, (2014)

  53. 53.

    et al. A draft sequence of the Neandertal genome. Science 328, 710–722 (2010)

  54. 54.

    et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053–1060 (2010)

  55. 55.

    et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43–49 (2014)

  56. 56.

    & Inference of human population history from individual whole-genome sequences. Nature 475, 493–496 (2011)

  57. 57.

    et al. mrsFAST: a cache-oblivious algorithm for short-read mapping. Nature Methods 7, 576–577 (2010)

  58. 58.

    An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56–65 (2012)

  59. 59.

    et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011)

  60. 60.

    The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25, 2078–2079 (2009)

  61. 61.

    , , & Measurement of the human allele frequency spectrum demonstrates greater genetic drift in East Asians than in Europeans. Nature Genet. 39, 1251–1255 (2007)

  62. 62.

    et al. Principal components analysis corrects for stratification in genome-wide association studies. Nature Genet. 38, 904–909 (2006)

  63. 63.

    et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007)

  64. 64.

    & Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12, 246 (2011)

  65. 65.

    & CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806 (2007)

  66. 66.

    , , & New approaches to population stratification in genome-wide association studies. Nature Rev. Genet. 11, 459–463 (2010)

  67. 67.

    , & Delete-m Jackknife for Unequal m. Stat. Comput. 9, 3–8 (1999)

  68. 68.

    et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193, 1233–1254 (2013)

  69. 69.

    et al. The population reference sample, POPRES: a resource for population, disease, and pharmacological genetics research. Am. J. Hum. Genet. 83, 347–358 (2008)

Download references

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

Author notes

    • 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

  1. Search for Iosif Lazaridis in:

  2. Search for Nick Patterson in:

  3. Search for Alissa Mittnik in:

  4. Search for Gabriel Renaud in:

  5. Search for Swapan Mallick in:

  6. Search for Karola Kirsanow in:

  7. Search for Peter H. Sudmant in:

  8. Search for Joshua G. Schraiber in:

  9. Search for Sergi Castellano in:

  10. Search for Mark Lipson in:

  11. Search for Bonnie Berger in:

  12. Search for Christos Economou in:

  13. Search for Ruth Bollongino in:

  14. Search for Qiaomei Fu in:

  15. Search for Kirsten I. Bos in:

  16. Search for Susanne Nordenfelt in:

  17. Search for Heng Li in:

  18. Search for Cesare de Filippo in:

  19. Search for Kay Prüfer in:

  20. Search for Susanna Sawyer in:

  21. Search for Cosimo Posth in:

  22. Search for Wolfgang Haak in:

  23. Search for Fredrik Hallgren in:

  24. Search for Elin Fornander in:

  25. Search for Nadin Rohland in:

  26. Search for Dominique Delsate in:

  27. Search for Michael Francken in:

  28. Search for Jean-Michel Guinet in:

  29. Search for Joachim Wahl in:

  30. Search for George Ayodo in:

  31. Search for Hamza A. Babiker in:

  32. Search for Graciela Bailliet in:

  33. Search for Elena Balanovska in:

  34. Search for Oleg Balanovsky in:

  35. Search for Ramiro Barrantes in:

  36. Search for Gabriel Bedoya in:

  37. Search for Haim Ben-Ami in:

  38. Search for Judit Bene in:

  39. Search for Fouad Berrada in:

  40. Search for Claudio M. Bravi in:

  41. Search for Francesca Brisighelli in:

  42. Search for George B. J. Busby in:

  43. Search for Francesco Cali in:

  44. Search for Mikhail Churnosov in:

  45. Search for David E. C. Cole in:

  46. Search for Daniel Corach in:

  47. Search for Larissa Damba in:

  48. Search for George van Driem in:

  49. Search for Stanislav Dryomov in:

  50. Search for Jean-Michel Dugoujon in:

  51. Search for Sardana A. Fedorova in:

  52. Search for Irene Gallego Romero in:

  53. Search for Marina Gubina in:

  54. Search for Michael Hammer in:

  55. Search for Brenna M. Henn in:

  56. Search for Tor Hervig in:

  57. Search for Ugur Hodoglugil in:

  58. Search for Aashish R. Jha in:

  59. Search for Sena Karachanak-Yankova in:

  60. Search for Rita Khusainova in:

  61. Search for Elza Khusnutdinova in:

  62. Search for Rick Kittles in:

  63. Search for Toomas Kivisild in:

  64. Search for William Klitz in:

  65. Search for Vaidutis Kučinskas in:

  66. Search for Alena Kushniarevich in:

  67. Search for Leila Laredj in:

  68. Search for Sergey Litvinov in:

  69. Search for Theologos Loukidis in:

  70. Search for Robert W. Mahley in:

  71. Search for Béla Melegh in:

  72. Search for Ene Metspalu in:

  73. Search for Julio Molina in:

  74. Search for Joanna Mountain in:

  75. Search for Klemetti Näkkäläjärvi in:

  76. Search for Desislava Nesheva in:

  77. Search for Thomas Nyambo in:

  78. Search for Ludmila Osipova in:

  79. Search for Jüri Parik in:

  80. Search for Fedor Platonov in:

  81. Search for Olga Posukh in:

  82. Search for Valentino Romano in:

  83. Search for Francisco Rothhammer in:

  84. Search for Igor Rudan in:

  85. Search for Ruslan Ruizbakiev in:

  86. Search for Hovhannes Sahakyan in:

  87. Search for Antti Sajantila in:

  88. Search for Antonio Salas in:

  89. Search for Elena B. Starikovskaya in:

  90. Search for Ayele Tarekegn in:

  91. Search for Draga Toncheva in:

  92. Search for Shahlo Turdikulova in:

  93. Search for Ingrida Uktveryte in:

  94. Search for Olga Utevska in:

  95. Search for René Vasquez in:

  96. Search for Mercedes Villena in:

  97. Search for Mikhail Voevoda in:

  98. Search for Cheryl A. Winkler in:

  99. Search for Levon Yepiskoposyan in:

  100. Search for Pierre Zalloua in:

  101. Search for Tatijana Zemunik in:

  102. Search for Alan Cooper in:

  103. Search for Cristian Capelli in:

  104. Search for Mark G. Thomas in:

  105. Search for Andres Ruiz-Linares in:

  106. Search for Sarah A. Tishkoff in:

  107. Search for Lalji Singh in:

  108. Search for Kumarasamy Thangaraj in:

  109. Search for Richard Villems in:

  110. Search for David Comas in:

  111. Search for Rem Sukernik in:

  112. Search for Mait Metspalu in:

  113. Search for Matthias Meyer in:

  114. Search for Evan E. Eichler in:

  115. Search for Joachim Burger in:

  116. Search for Montgomery Slatkin in:

  117. Search for Svante Pääbo in:

  118. Search for Janet Kelso in:

  119. Search for David Reich in:

  120. Search for Johannes Krause in:

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

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.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature13673

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.