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Population genomics of Bronze Age Eurasia

Naturevolume 522, pages167–172 (2015)Cite this article

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Abstract

The Bronze Age of Eurasia (around 3000–1000BC) 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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Figure 1: Distribution maps of ancient samples.
Figure 2: Genetic structure of ancient Europe and the Pontic-Caspian steppe.
Figure 3: Genetic structure of Bronze Age Asia.
Figure 4: Allele frequencies for putatively positively selected SNPs.

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Accession codes

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 numberPRJEB9021.

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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

  1. Morten E. Allentoft and Martin Sikora: These authors contributed equally to this work.

Authors and 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, Gothenburg, 405 30, Sweden

    Karl-Göran Sjögren, Dalia Pokutta & Kristian Kristiansen

  3. Department of Systems Biology, Center for Biological Sequence Analysis, Technical University of Denmark, Kgs Lyngby, 2800, Denmark

    Simon Rasmussen, Thomas Sicheritz-Pontén & Søren Brunak

  4. Faculty of Archaeology, Leiden University, Leiden, 2300, The Netherlands

    Hannes Schroeder

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

    Torbjörn Ahlström

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

    Tom Higham & David Chivall

  7. Department of Forensic Medicine, Unit of Forensic Anthropology, University of Copenhagen, Copenhagen, 2100, Denmark

    Niels Lynnerup & Lise Harvig

  8. Institute of Archaeology, University of Wrocław, Wrocław, 50-139, Poland

    Justyna Baron, Mirosław Furmanek, Tomasz Gralak & Irena Lasak

  9. Archaeological Institute, University of Zurich, Zurich, CH-8006, Switzerland

    Philippe Della Casa

  10. Department of Anatomy, Wrocław Medical University, Wrocław, 50-368, 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, Gorno-Altaisk, 649000, Russia

    Alexander V. Ebel

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

    Andrey Epimakhov

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

    Karin Frei

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

    Andrey Gromov, Valeri Khartanovich & Vyacheslav Moiseyev

  16. Department of Anthropology, Polish Academy of Sciences, Wrocław, 50–449, Poland

    Stanisław Gronkiewicz

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

    Gisela Grupe & George McGlynn

  18. Department of Biological Anthropology, Institute of Biology, Eötvös Loránd University, Budapest, H-1117, Hungary

    Tamás Hajdu

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

    Tamás Hajdu

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

    Radosław Jarysz

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

    Alexandr Khokhlov

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

    Viktória Kiss & Vajk Szeverényi

  23. Institute of Archaeology and Museology, Faculty of Arts, Masaryk University, Brno, CZ-602 00, Czech Republic

    Jan Kolář

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

    Jan Kolář

  25. Department of Archaeology, University of Tartu, Tartu, 51003, Estonia

    Aivar Kriiska & Liivi Varul

  26. Archaeological Superintendence of Lombardy, Milano, 20123, Italy

    Cristina Longhi

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

    Algimantas Merkevicius

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

    Inga Merkyte

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

    Mait Metspalu & Lehti Saag

  30. Department of History, Yerevan State University, Yerevan, 0025, Armenia

    Ruzan Mkrtchyan

  31. Hungarian National Museum, Budapest, H-1083, Hungary

    László Paja

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

    László Paja & György Pálfi

  33. Institute of Archaeology and Ethnology of the Polish Academy of Sciences, Poznań, 61-612, Poland

    Łukasz Pospieszny

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

    T. Douglas Price

  35. Zoological Institute of the Russian Academy of Sciences, St Petersburg, 199034, Russia

    Mikhail Sablin

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

    Natalia Shishlina

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

    Václav Smrčka

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

    Vasilii I. Soenov & Synaru V. Trifanova

  39. Department of Pre- and Early History, Institute of Archaeological Sciences, Faculty of Humanities, Eötvös Loránd University, Budapest, H-1088, Hungary

    Gusztáv Tóth

  40. Matrica Museum, Százhalombatta, 2440, Hungary

    Magdolna Vicze

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

    Levon Yepiskoposyan

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

    Vladislav Zhitenev

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

    Søren Brunak

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

    Rasmus Nielsen

Authors
  1. Morten E. Allentoft
  2. Martin Sikora
  3. Karl-Göran Sjögren
  4. Simon Rasmussen
  5. Morten Rasmussen
  6. Jesper Stenderup
  7. Peter B. Damgaard
  8. Hannes Schroeder
  9. Torbjörn Ahlström
  10. Lasse Vinner
  11. Anna-Sapfo Malaspinas
  12. Ashot Margaryan
  13. Tom Higham
  14. David Chivall
  15. Niels Lynnerup
  16. Lise Harvig
  17. Justyna Baron
  18. Philippe Della Casa
  19. Paweł Dąbrowski
  20. Paul R. Duffy
  21. Alexander V. Ebel
  22. Andrey Epimakhov
  23. Karin Frei
  24. Mirosław Furmanek
  25. Tomasz Gralak
  26. Andrey Gromov
  27. Stanisław Gronkiewicz
  28. Gisela Grupe
  29. Tamás Hajdu
  30. Radosław Jarysz
  31. Valeri Khartanovich
  32. Alexandr Khokhlov
  33. Viktória Kiss
  34. Jan Kolář
  35. Aivar Kriiska
  36. Irena Lasak
  37. Cristina Longhi
  38. George McGlynn
  39. Algimantas Merkevicius
  40. Inga Merkyte
  41. Mait Metspalu
  42. Ruzan Mkrtchyan
  43. Vyacheslav Moiseyev
  44. László Paja
  45. György Pálfi
  46. Dalia Pokutta
  47. Łukasz Pospieszny
  48. T. Douglas Price
  49. Lehti Saag
  50. Mikhail Sablin
  51. Natalia Shishlina
  52. Václav Smrčka
  53. Vasilii I. Soenov
  54. Vajk Szeverényi
  55. Gusztáv Tóth
  56. Synaru V. Trifanova
  57. Liivi Varul
  58. Magdolna Vicze
  59. Levon Yepiskoposyan
  60. Vladislav Zhitenev
  61. Ludovic Orlando
  62. Thomas Sicheritz-Pontén
  63. Søren Brunak
  64. Rasmus Nielsen
  65. Kristian Kristiansen
  66. Eske Willerslev

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.

Corresponding author

Correspondence toEske Willerslev.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Principal component analysis of ancient genomes.

a,b, Principal component analysis of ancient individuals projected onto contemporary individuals from non-African populations (a), Europe, West Asia and the Caucasus (b). Grey labels represent population codes indicating coordinates for individuals (small) and median of the population (large). Coloured labels indicate positions for ancient individuals (small) and median for ancient groups (large). Ancient individuals within a group are connected to the respective median position by coloured lines.

Extended Data Figure 2 Pairwise outgroupf3 statistics.

Panels depict pairwise plots of outgroupf3 statistics of the formf3(Ju’hoan North;Population1, Population2), showing the correlation of the amount of shared genetic drift for a pair of ancient groups (Population1) with all modern populations (Population2) in the Human Origins data set (panel A). Closely related ancient groups are expected to show highly correlated statistics.a, Sintashta/Corded Ware.b, Yamnaya/Afanasievo.c, Sintashta/Andronovo.d, Okunevo/Mal’ta. Coloured circles indicate modern populations; error bars indicate ± 1 standard error from the block jackknife.

Extended Data Figure 3 Yamnaya ancestry mirrors Mal’ta ancestry in present-day Europeans and Caucasians.

Panels show pairwise plots of D-statistics D(Outgroup, Ancient)(Bedouin, Modern), contrasting Mal’ta (MA1) and Hunter-gatherers (a), and MA1 and Yamnaya (b). Coloured labels indicate modern populations, with lines corresponding to ± 1 standard error of the respectiveD-statistic from block jacknife. Text away from the diagonal line indicates an ancient group with relative increase in allele sharing with the respective modern populations.

Extended Data Figure 4 Genetic differentiation between ancient and modern groups in Human Origins data set.

Panels showFST between pairs of modern and ancient groups (coloured lines) for subsets of ancient groups, with results for the remaining groups in the background (grey). Top, early Europeans. Middle, Bronze Age Europeans and steppe/Caucasus. Bottom, Bronze Age Asians. Results based on Human Origins data set (panel A).

Extended Data Figure 5 Genetic differentiation between ancient and modern groups in 1000 Genomes data set.

Matrix of pairwiseFST values between modern and ancient groups in the 1000 Genomes data set (panel B).

Extended Data Figure 6 Distribution of uniparental lineages in Bronze Age Eurasians.

a,b, Barplots showing the relative frequency of Y chromosome (a) and mitochondrial DNA lineages (b) in different Bronze Age groups. Top row shows overall frequencies for all individuals combined.

Extended Data Figure 7 Derived allele frequencies for lactase persistence in modern and ancient groups.

Derived allele frequency of rs4988235 in theLCT gene inferred from imputation of ancient individuals. Numbers indicate the total number of chromosomes for each group.

Extended Data Table 1 Selected D-test results from 1000 Genomes data set (panel B)
Extended Data Table 2f3 statistic results for ancient groups

Supplementary information

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). (PDF 4331 kb)

Supplementary Table 6

This table contains sequencing summary statistics. (XLSX 20 kb)

Supplementary Table 7

This table contains an overview of aDNA damage statistics. (XLS 44 kb)

Supplementary Table 8

This table contains results of DNA contamination tests. (XLSX 18 kb)

Supplementary Table 10

This table contains D-test for all combinations D(Outgroup,Ancient1)(Ancient2)(Ancient3); 1000 Genomes dataset. (XLSX 1915 kb)

Supplementary Table 11

This table contains “Outgroup” f3-statistics for all combinations of ancient and modern groups; Human Origins dataset. (XLSX 748 kb)

Supplementary Table 12

This table contains all-pair “admixture” f3-statistics; 1000 Genomes dataset. (XLSX 3921 kb)

Supplementary Table 13

This table contains derived allele frequencies of 104 SNP catalogue for putative selection; 1000 Genomes dataset. (XLSX 63 kb)

Supplementary Table 14

This table contains an overview of mtDNA haplogroups and identified variants. (XLS 97 kb)

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Allentoft, M., Sikora, M., Sjögren, KG.et al. Population genomics of Bronze Age Eurasia.Nature522, 167–172 (2015). https://doi.org/10.1038/nature14507

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Editorial Summary

Population changes in Bronze Age Eurasia

Was the Bronze Age of a period of major cultural changes because of circulation of ideas or because of large-scale migrations? The authors sequence and analyse low-coverage genomes from 101 ancient humans from across Eurasia to reveal large-scale population migrations and replacements during this time. Analyses indicate that light skin pigmentation was already frequent among Europeans in the Bronze Age but not lactose tolerance, indicating a more recent onset of positive selection on the latter trait than previously believed. The reported findings are also consistent with the spread of Indo-European languages during the Early Bronze Age reported onpage 207 of this issue.

Associated content

Massive migration from the steppe was a source for Indo-European languages in Europe

  • Wolfgang Haak
  • Iosif Lazaridis
  • David Reich
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Ancient DNA steps into the language debate

  • John Novembre
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