Article

Population genomics of Bronze Age Eurasia

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Abstract

The Bronze Age of Eurasia (around 3000–1000 BC) was a period of major cultural changes. However, there is debate about whether these changes resulted from the circulation of ideas or from human migrations, potentially also facilitating the spread of languages and certain phenotypic traits. We investigated this by using new, improved methods to sequence low-coverage genomes from 101 ancient humans from across Eurasia. We show that the Bronze Age was a highly dynamic period involving large-scale population migrations and replacements, responsible for shaping major parts of present-day demographic structure in both Europe and Asia. Our findings are consistent with the hypothesized spread of Indo-European languages during the Early Bronze Age. We also demonstrate that light skin pigmentation in Europeans was already present at high frequency in the Bronze Age, but not lactose tolerance, indicating a more recent onset of positive selection on lactose tolerance than previously thought.

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Accessions

Primary accessions

European Nucleotide Archive

Data deposits

DNA sequence alignments are available from the European Nucleotide Archive (http://www.ebi.ac.uk/ena) under accession number PRJEB9021.

References

  1. 1.

    et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445–449 (2014)

  2. 2.

    et al. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113–1118 (2014)

  3. 3.

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

  4. 4.

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

  5. 5.

    et al. The genetic prehistory of the New World Arctic. Science 345, 1255832 (2014)

  6. 6.

    et al. The genome of a Late Pleistocene human from a Clovis burial site in western Montana. Nature 506, 225–229 (2014)

  7. 7.

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

  8. 8.

    et al. Ancient DNA reveals lack of continuity between Neolithic hunter-gatherers and contemporary Scandinavians. Curr. Biol. 19, 1758–1762 (2009)

  9. 9.

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

  10. 10.

    et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014)

  11. 11.

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

  12. 12.

    et al. Genome flux and stasis in a five millennium transect of European prehistory. Nature Commun. 5, 5257 (2014)

  13. 13.

    in The World System and the Earth System. Global Socioenvironmental Change and Sustainability Since the Neolithic (eds Hornborg, B. & Crumley, C.) (Left Coast Press, 2007)

  14. 14.

    Reconstruction of the Bronze Age of the Caspian Steppes. Life Styles and Life Ways of Pastoral Nomads. Vol. 1876 (Archaeopress, 2008)

  15. 15.

    The Horse, The Wheel and Language. How Bronze-Age Riders from the Eurasian Steppes Shaped the Modern World (Princeton Univ. Press, 2007)

  16. 16.

    & The Transformation of Europe in the third millennium BC: the example of ‘Le Petit-Chasseur I + III’ (Sion, Valais, Switzerland). Praehistorische Zeitschrift. 82, 129–214 (2007)

  17. 17.

    Culture and Change in the Central European Prehistory, 6th to 1st millennium BC (Aarhus Univ. Press, 2007)

  18. 18.

    & The Rise of Bronze Age Society. Travels, Transmissions and Transformations (Cambridge Univ. Press, 2005)

  19. 19.

    , & Towards a refined chronology for the Bronze Age of the southern Urals, Russia. Antiquity 81, 353–367 (2007)

  20. 20.

    The emergence of Bronze Age chariots in Eastern Europe. Antiquity 80, 638–645 (2006)

  21. 21.

    & The Urals and Western Siberia in the Bronze and Iron Ages (Cambridge Univ. Press, 2007)

  22. 22.

    et al. Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463, 757–762 (2010)

  23. 23.

    et al. Pulling out the 1%: whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am. J. Hum. Genet. 93, 852–864 (2013)

  24. 24.

    et al. Improving access to endogenous DNA in ancient bones and teeth. Preprint at bioRxiv (2015)

  25. 25.

    , , , & Survival and recovery of DNA from ancient teeth and bones. J. Archaeol. Sci. 38, 956–964 (2011)

  26. 26.

    et al. True single-molecule DNA sequencing of a Pleistocene horse bone. Genome Res. 21, 1705–1719 (2011)

  27. 27.

    & Modern humans’ paleogenomics and the new evidences on the European prehistory. Science and Technology of Archaeological Research 1, (2015)

  28. 28.

    Ancient Indo-Europeans (Charoid, 2002)

  29. 29.

    De l’Âge du Bronze et lÂge du Fer au Kazakkstan, gestes funéraires et paramètres biologiques. Identités culturelles des population Andronovo et Saka (De Boccard, 2007)

  30. 30.

    , & Collateral relatives of American Indians among the Bronze Age populations of Siberia? Am. J. Phys. Anthropol. 108, 193–204 (1999)

  31. 31.

    in Becoming European. The transformation of third millennium Northern and Western Europe (eds Prescott, C. & Glørstad, H.) (Oxbow Books, 2012)

  32. 32.

    et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature (this issue)

  33. 33.

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

  34. 34.

    , , , & The origins of lactase persistence in Europe. PLoS Computational Biol. 5, e1000491 (2009)

  35. 35.

    In Search of the Indo-Europeans. Language, Archaeology and Myth (Thames & Hudson, 1987)

  36. 36.

    Archaeology and Language. The Puzzle of Indo-European Origins (Penguin, 1987)

  37. 37.

    & The Tarim Mummies. Ancient China and the Mystery of the Earliest People from the West (Thames & Hudson, 2000)

  38. 38.

    et al. Ancient DNA provides new insights into the history of south Siberian Kurgan people. Hum. Genet. 126, 395–410 (2009)

  39. 39.

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

  40. 40.

    et al. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74–78 (2013)

  41. 41.

    et al. Two ancient human genomes reveal Polynesian ancestry among the indigenous Botocudos of Brazil. Curr. Biol. 24, R1035–R1037 (2014)

  42. 42.

    & Ancient DNA. Proc. Royal Soc. B 272, 3–16 (2005)

  43. 43.

    et al. Patterns of damage in genomic DNA sequences from a Neandertal. Proc. Natl Acad. Sci. USA 104, 14616–14621 (2007)

  44. 44.

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

  45. 45.

    et al. Improving ancient DNA read mapping against modern reference genomes. BMC Genomics 13, 178 (2012)

  46. 46.

    et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009)

  47. 47.

    & BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010)

  48. 48.

    , , , & mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics (2013)

  49. 49.

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

  50. 50.

    , & ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, (2014)

  51. 51.

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

  52. 52.

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

  53. 53.

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

  54. 54.

    & Estimating F-statistics. Annu. Rev. Genet. 36, 721–750 (2002)

  55. 55.

    et al. Microsatellite genotyping reveals end-Pleistocene decline in mammoth autosomal genetic variation. Mol. Ecol. 21, 3391–3402 (2012)

  56. 56.

    & Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084–1097 (2007)

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Acknowledgements

We thank K. Magnussen, L. A. Petersen, C. D. Mortensen and A. Seguin-Orlando at the Danish National Sequencing Centre for help with the sequencing. We thank C. G. Zacho for technical assistance. The project was funded by The European Research Council (FP/2007-2013, grant no. 269442, The Rise), The University of Copenhagen (KU2016 programme), Marie Curie Actions of the European Union (FP7/2007-2013, grant no. 300554), The Villum Foundation (Young Investigator Programme, grant no. 10120), Frederik Paulsen, The Miller Institute, University of California, Berkeley, The Lundbeck Foundation, and The Danish National Research Foundation.

Author information

Author notes

    • Morten E. Allentoft
    •  & Martin Sikora

    These authors contributed equally to this work.

Affiliations

  1. Centre for GeoGenetics, Natural History Museum, University of Copenhagen, Øster Voldgade 5-7, 1350 Copenhagen K, Denmark

    • Morten E. Allentoft
    • , Martin Sikora
    • , Morten Rasmussen
    • , Jesper Stenderup
    • , Peter B. Damgaard
    • , Hannes Schroeder
    • , Lasse Vinner
    • , Anna-Sapfo Malaspinas
    • , Ashot Margaryan
    • , Ludovic Orlando
    •  & Eske Willerslev
  2. Department of Historical Studies, University of Gothenburg, 405 30 Gothenburg, Sweden

    • Karl-Göran Sjögren
    • , Dalia Pokutta
    •  & Kristian Kristiansen
  3. Center for Biological Sequence Analysis, Department of Systems Biology, Technical University of Denmark, 2800 Kgs Lyngby, Denmark

    • Simon Rasmussen
    • , Thomas Sicheritz-Pontén
    •  & Søren Brunak
  4. Faculty of Archaeology, Leiden University, 2300 Leiden, The Netherlands

    • Hannes Schroeder
  5. Department of Archaeology and Ancient History, Lund University, 221 00 Lund, Sweden

    • Torbjörn Ahlström
  6. Oxford Radiocarbon Accelerator Unit, University of Oxford, Oxford OX1 3QY, UK

    • Tom Higham
    •  & David Chivall
  7. Unit of Forensic Anthropology, Department of Forensic Medicine, University of Copenhagen, 2100 Copenhagen, Denmark

    • Niels Lynnerup
    •  & Lise Harvig
  8. Institute of Archaeology, University of Wrocław, 50-139 Wrocław, Poland

    • Justyna Baron
    • , Mirosław Furmanek
    • , Tomasz Gralak
    •  & Irena Lasak
  9. Archaeological Institute, University of Zurich, CH-8006, Zurich, Switzerland

    • Philippe Della Casa
  10. Department of Anatomy, Wrocław Medical University, 50-368 Wrocław, Poland

    • Paweł Dąbrowski
  11. Department of Anthropology, University of Toronto, Toronto ONM5S 2S2, Canada

    • Paul R. Duffy
  12. Department of Archeology and General History, Gorno-Altaisk State University, 649000 Gorno-Altaisk, Russia

    • Alexander V. Ebel
  13. Institute of History and Archaeology RAS (South Ural Department), South Ural State University, 454080 Chelyabinsk, Russia

    • Andrey Epimakhov
  14. Environmental Research and Material Science and Centre for Textile Research, The National Museum of Denmark, 1471 Copenhagen K, Denmark

    • Karin Frei
  15. Peter the Great Museum of Anthropology and Ethnography (Kunstkamera) RAS, 199034 St Petersburg, Russia

    • Andrey Gromov
    • , Valeri Khartanovich
    •  & Vyacheslav Moiseyev
  16. Department of Anthropology, Polish Academy of Sciences, 50–449 Wrocław, Poland

    • Stanisław Gronkiewicz
  17. Biocentre of the Ludwig-Maximilian-University München, 82152 Munich, Germany

    • Gisela Grupe
    •  & George McGlynn
  18. Department of Biological Anthropology, Institute of Biology, Eötvös Loránd University, H-1117 Budapest, Hungary

    • Tamás Hajdu
  19. Department of Anthropology, Hungarian Natural History Museum, H-1083 Budapest, Hungary

    • Tamás Hajdu
  20. The Archaeological Museum of Wrocław, 50-077 Wrocław, Poland

    • Radosław Jarysz
  21. Samara State Academy of Social Science and Humanities, 443099 Samara, Russia

    • Alexandr Khokhlov
  22. Institute of Archaeology of the Hungarian Academy of Sciences, Research Center for the Humanities, H-1250 Budapest, Hungary

    • Viktória Kiss
    •  & Vajk Szeverényi
  23. Institute of Archaeology and Museology, Faculty of Arts, Masaryk University, CZ-602 00 Brno, Czech Republic

    • Jan Kolář
  24. Department of Vegetation Ecology, Institute of Botany of the Czech Academy of Sciences, CZ-602 00 Brno, Czech Republic

    • Jan Kolář
  25. Department of Archaeology, University of Tartu, 51003 Tartu, Estonia

    • Aivar Kriiska
    •  & Liivi Varul
  26. Archaeological Superintendence of Lombardy, 20123 Milano, Italy

    • Cristina Longhi
  27. Department of Archaeology, University of Vilnius, LT-01513 Vilnius, Lithuania

    • Algimantas Merkevicius
  28. The SAXO Institute, University of Copenhagen, 2300 Copenhagen S, Denmark

    • Inga Merkyte
  29. Department of Evolutionary Biology, Estonian Biocentre and University of Tartu, 51010 Tartu, Estonia

    • Mait Metspalu
    •  & Lehti Saag
  30. Department of History, Yerevan State University, 0025 Yerevan, Armenia

    • Ruzan Mkrtchyan
  31. Hungarian National Museum, H-1083 Budapest, Hungary

    • László Paja
  32. Department of Biological Anthropology, University of Szeged, H-6726 Szeged, Hungary

    • László Paja
    •  & György Pálfi
  33. Institute of Archaeology and Ethnology of the Polish Academy of Sciences, 61-612 Poznań, Poland

    • Łukasz Pospieszny
  34. Laboratory for Archaeological Chemistry, University of Wisconsin-Madison, Madison, Wisconsin 53706, USA

    • T. Douglas Price
  35. Zoological Institute of the Russian Academy of Sciences, 199034 St Petersburg, Russia

    • Mikhail Sablin
  36. Department of Archaeology, State Historical Museum, 109012 Moscow, Russia

    • Natalia Shishlina
  37. Institute for History of Medicine and Foreign Languages of the First Faculty of Medicine, Charles University, 121 08 Prague, Czech Republic

    • Václav Smrčka
  38. Research Center for the History and Culture of the Turkic Peoples, Gorno-Altaisk State University, 649000 Gorno-Altaisk, Russia

    • Vasilii I. Soenov
    •  & Synaru V. Trifanova
  39. Department of Pre- and Early History, Institute of Archaeological Sciences, Faculty of Humanities, Eötvös Loránd University, H-1088 Budapest, Hungary

    • Gusztáv Tóth
  40. Matrica Museum, 2440 Százhalombatta, Hungary

    • Magdolna Vicze
  41. Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences, 0014 Yerevan, Armenia

    • Levon Yepiskoposyan
  42. Department of Archaeology, Faculty of History, Moscow State University, 119991 Moscow, Russia

    • Vladislav Zhitenev
  43. Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, 2200 Copenhagen, Denmark

    • Søren Brunak
  44. Center for Theoretical Evolutionary Genetics, University of California, Berkeley, California 94720-3140, USA

    • Rasmus Nielsen

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Contributions

E.W. and K.K. initiated and led the study. M.E.A., J.S., L.V., H.S., P.B.D., A.M., M.R., L.S. performed the DNA laboratory work. M.Si., S.R., M.E.A., A.-S.M., P.B.D., A.M. analysed the genetic data. K.-G.S., T.A., N.L., L.H., J.B., P.D.C., P.D., P.R.D., A.E., A.V.E., K.F., M.F., G.G., T.G., A.G., S.G., T.H., R.J., J.K., V.K., A.K., V.K., A.K., I.L., C.L., A.M., G.M., I.M., M.M., R.M., V.M., D.Po., G.P., L.P., D.Pr., L.P., M.Sa., N.S., V.Sm., V.Sz., V.I.S., G.T., S.V.T., L.V., M.V., L.Y., V.Z. collected the samples and/or provided input to the archaeological interpretations. T.H. and D.C. conducted radiocarbon dating. T.S.-P., L.O., S.B., R.N. provided input to the genetic analyses. E.W., K.K., M.E.A., M.Si., K.-G.S. wrote the paper with input from all co-authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Eske Willerslev.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Information sections 1-6. Section 1: An introduction to the sampled cultures and their dating. Section 2: Brief description of the samples (including Supplementary Tables 1-3). Section 3: Laboratory work and sample selection (including Supplementary Tables 4-5, and Supplementary Figure 1). Section 4: Radiocarbon dating. Section 5: Bioinformatics and DNA authentication. Section 6: Population genomics (including Supplementary Table 9 and Supplementary Figures 2-6).

Excel files

  1. 1.

    Supplementary Table 6

    This table contains sequencing summary statistics.

  2. 2.

    Supplementary Table 7

    This table contains an overview of aDNA damage statistics.

  3. 3.

    Supplementary Table 8

    This table contains results of DNA contamination tests.

  4. 4.

    Supplementary Table 10

    This table contains D-test for all combinations D(Outgroup,Ancient1)(Ancient2)(Ancient3); 1000 Genomes dataset.

  5. 5.

    Supplementary Table 11

    This table contains “Outgroup” f3-statistics for all combinations of ancient and modern groups; Human Origins dataset.

  6. 6.

    Supplementary Table 12

    This table contains all-pair “admixture” f3-statistics; 1000 Genomes dataset.

  7. 7.

    Supplementary Table 13

    This table contains derived allele frequencies of 104 SNP catalogue for putative selection; 1000 Genomes dataset.

  8. 8.

    Supplementary Table 14

    This table contains an overview of mtDNA haplogroups and identified variants.

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