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The genetic history of Ice Age Europe

Naturevolume 534, pages200–205 (2016)Cite this article

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Abstract

Modern humans arrived in Europe ~45,000 years ago, but little is known about their genetic composition before the start of farming ~8,500 years ago. Here we analyse genome-wide data from 51 Eurasians from ~45,000–7,000 years ago. Over this time, the proportion of Neanderthal DNA decreased from 3–6% to around 2%, consistent with natural selection against Neanderthal variants in modern humans. Whereas there is no evidence of the earliest modern humans in Europe contributing to the genetic composition of present-day Europeans, all individuals between ~37,000 and ~14,000 years ago descended from a single founder population which forms part of the ancestry of present-day Europeans. An ~35,000-year-old individual from northwest Europe represents an early branch of this founder population which was then displaced across a broad region, before reappearing in southwest Europe at the height of the last Ice Age ~19,000 years ago. During the major warming period after ~14,000 years ago, a genetic component related to present-day Near Easterners became widespread in Europe. These results document how population turnover and migration have been recurring themes of European prehistory.

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Figure 1: Location and age of the 51 ancient modern humans.
Figure 2: Decrease of Neanderthal ancestry over time.
Figure 3: Genetic clustering of the ancient modern humans.
Figure 4: Population history inferences.

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Primary accessions

European Nucleotide Archive

Data deposits

The aligned sequences are available through the European Nucleotide Archive under accession numberPRJEB13123.

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Acknowledgements

We thank B. Alex, D. Meltzer, P. Moorjani, I. Olalde, S. Sankararaman and B. Viola for comments, K. Stewardson and E. Harney for sample screening, and F. Hallgren for sharing a radiocarbon date forMotala12. TheFig. 1 map is plotted using data available under the Open Database License © OpenStreetMap (http://www.openstreetmap.org/copyright). The Goyet project led by H.R. was funded by the Wenner-Gren Foundation (Gr. 7837), the College of Social and Behavioral Sciences of CSUN, the CSUN Competition for Research, Scholarship and Creative Activity Awards, and the RBINS. The excavation of the El Mirón Cave burial, led by L.G.S. and M.R.G.M., was supported by the Gobierno de Cantabria, the L.S.B. Leakey Foundation, the University of New Mexico, the Stone Age Research Fund (J. and R. Auel, principal donors), the town of Ramales de la Victoria and the Universidad de Cantabria. Excavations at Grotta Paglicci were performed by A. Palma di Cesnola in collaboration with the Soprintendenza Archeologia della Puglia (founded by MIUR and local Institutions). Research at Riparo Villabruna was supported by MIBACT and the Veneto Region. Q.F. was funded by the Special Foundation of the President of the Chinese Academy of Sciences (2015–2016), the Bureau of International Cooperation of the Chinese Academy of Sciences, the Chinese Academy of Sciences (XDA05130202), the National Natural Science Foundation of China (L1524016) and the Chinese Academy of Sciences Discipline Development Strategy Project (2015-DX-C-03). D.Fe was supported by an Irish Research Council grant (GOIPG/2013/36). I.M. was supported by a long-term fellowship from the Human Frontier Science Program LT001095/2014-L. P.Sk was supported by the Swedish Research Council (VR 2014-453). S.T., and M.P.R. were funded by the Max Planck Society. C.N.-M. was funded by FWF P-17258, P-19347, P-21660 and P-23612. S.C. and O.T.M. were funded by a ‘Karsthives’ Grant PCCE 31/2010 (CNCS-UEFISCDI, Romania). A.P.D., N.D., V.Sla and N.D. were funded by the Russian Science Foundation (project No.14-50-00036). M.A.M. was funded by a Marie Curie Intra-European Fellowship within the 7th European Community Framework Programme (grant number PIEF-GA-2008-219965). M.La and D.C. were funded by grants PRIN 2010-11 and 2010EL8TXP_003. C.C. and the research about the French Jura sites of Rochedane, Rigney and Ranchot was funded by the Collective Research Program (PCR) (2005-2008). K.H. was supported by the European Research Council (ERC StG 283503) and the Deutsche Forschungsgemeinschaft (DFG INST37/706-1FUGG, DFG FOR2237). D.G.D. was funded by the European Social Fund and Ministry of Science, Research and Arts of Baden-Württemberg. R.P. was funded by ERC starting grant ADNABIOARC (263441). J.Ke was funded by a grant from the Deutsche Forschungsgemeinschaft (SFB1052, project A02). J.Kr was funded by DFG grant KR 4015/1-1, the Baden Württemberg Foundation, and the Max Planck Society. S.P. were funded by the Max Planck Society and the Krekeler Foundation. D.R. was funded by NSF HOMINID grant BCS-1032255, NIH (NIGMS) grant GM100233, and the Howard Hughes Medical Institute.

Author information

Author notes

  1. Cosimo Posth and Mateja Hajdinjak: These authors contributed equally to this work.

  2. Johannes Krause, Svante Pääbo and David Reich: These authors jointly supervised this work.

Authors and Affiliations

  1. Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, IVPP, CAS, Beijing, 100044, China

    Qiaomei Fu

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

    Qiaomei Fu, Swapan Mallick, Nadin Rohland, Iosif Lazaridis, Mark Lipson, Iain Mathieson, Pontus Skoglund & David Reich

  3. Department of Evolutionary Genetics, Max Planck Institute for Evolutionary, Anthropology, 04103, Leipzig, Germany

    Qiaomei Fu, Mateja Hajdinjak, Martin Petr, Matthias Meyer, Birgit Nickel, Viviane Slon, Janet Kelso & Svante Pääbo

  4. Institute for Archaeological Sciences, Archaeo- and Palaeogenetics, University of Tübingen, Tübingen, 72070, Germany

    Cosimo Posth, Anja Furtwängler, Alissa Mittnik, Alexander Peltzer & Johannes Krause

  5. Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, 07745, Germany

    Cosimo Posth, Wolfgang Haak, Alissa Mittnik, Stephan Schiffels & Johannes Krause

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

    Swapan Mallick, Nick Patterson & David Reich

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

    Swapan Mallick & David Reich

  8. School of Archaeology and Earth Institute, University College Dublin, Belfield, 4, Dublin, Ireland

    Daniel Fernandes & Ron Pinhasi

  9. Department of Life Sciences, CIAS, University of Coimbra, Coimbra, 3000-456, Portugal

    Daniel Fernandes

  10. Australian Centre for Ancient DNA, School of Biological Sciences, The University of Adelaide, Adelaide, SA-5005, Australia

    Wolfgang Haak

  11. Department of Human Evolution, Max Planck Institute for Evolutionary, Anthropology, 04103, Leipzig, Germany

    Sahra Talamo, Stefano Benazzi, Marcello A. Mannino & Michael P. Richards

  12. Institute of Archaeology and Ethnography, Russian Academy of Sciences, Siberian Branch, 17, Novosibirsk, RU-630090, Russia

    Anatoly P. Derevianko, Nikolai Drozdov, Vyacheslav Slavinsky & Alexander Tsybankov

  13. Altai State University, Barnaul, RU-656049, Russia

    Anatoly P. Derevianko

  14. Dipartimento di Civiltà e Forme del Sapere, Università di Pisa, Pisa, 56126, Italy

    Renata Grifoni Cremonesi

  15. Department of Biology, University of Pisa, Pisa, 56126, Italy

    Francesco Mallegni

  16. Direction régionale des affaires culturelles Rhône-Alpes, Lyon, 69283, Cedex 01, France

    Bernard Gély

  17. Dipartimento di Biologia, Università degli Studi di Bari ‘Aldo Moro’, Bari, 70125, Italy

    Eligio Vacca

  18. Instituto Internacional de Investigaciones Prehistóricas, Universidad de Cantabria, Santander, 39005, Spain

    Manuel R. González Morales & Lawrence G. Straus

  19. Department of Anthropology, MSC01 1040, University of New Mexico, Albuquerque, 87131-0001, New Mexico, USA

    Lawrence G. Straus

  20. Quaternary Archaeology, Institute for Oriental and European Archaeology, Austrian Academy of Sciences, Vienna, 1010, Austria

    Christine Neugebauer-Maresch

  21. Department of Anthropology, Natural History Museum Vienna, Vienna, 1010, Austria

    Maria Teschler-Nicola

  22. Department of Anthropology, University of Vienna, Vienna, 1090, Austria

    Maria Teschler-Nicola

  23. “Emil Racoviţă” Institute of Speleology, Bucharest 12, 010986, Romania

    Silviu Constantin

  24. “Emil Racoviţă” Institute of Speleology, Cluj Branch, Cluj, 400006, Romania

    Oana Teodora Moldovan

  25. Department of Cultural Heritage, University of Bologna, Ravenna, 48121, Italy

    Stefano Benazzi

  26. Dipartimento di Studi Umanistici, Sezione di Scienze Preistoriche e Antropologiche, Università di Ferrara, Ferrara, 44100, Italy

    Marco Peresani

  27. Università degli Studi di Bari ‘Aldo Moro’, Bari, 70125, Italy

    Donato Coppola

  28. Museo di “Civiltà preclassiche della Murgia meridionale”, Ostuni, 72017, Italy

    Donato Coppola

  29. Dipartimento di Biologia, Università di Firenze, Florence, 50122, Italy

    Martina Lari & David Caramelli

  30. Dipartimento di Scienze Fisiche, della Terra e dell’Ambiente, U.R. Preistoria e Antropologia, Università degli Studi di Siena, Siena, 53100, Italy

    Stefano Ricci & Annamaria Ronchitelli

  31. CNRS/UMR, 7041 ArScAn MAE, Nanterre, 92023, France

    Frédérique Valentin

  32. INRAP/UMR, 8215 Trajectoires 21, Nanterre, 92023, France

    Corinne Thevenet

  33. Ulmer Museum, Ulm, 89073, Germany

    Kurt Wehrberger

  34. Department of Geology, University of Bucharest, Faculty of Geology and Geophysics, Bucharest, 01041, Romania

    Dan Grigorescu

  35. Department of Anthropology, California State University Northridge, Northridge, 91330-8244, California, USA

    Hélène Rougier

  36. Université de Bordeaux, CNRS, UMR 5199-PACEA, Pessac Cedex, 33615, France

    Isabelle Crevecoeur

  37. TRACES – UMR 5608, Université Toulouse Jean Jaurès, Maison de la Recherche, Toulouse, 31058, Cedex 9, France

    Damien Flas

  38. Royal Belgian Institute of Natural Sciences, Brussels, 1000, Belgium

    Patrick Semal

  39. Department of Archaeology, School of Culture and Society, Aarhus University, Højbjerg, 8270, Denmark

    Marcello A. Mannino

  40. Service Régional d’Archéologie de Franche-Comté, Besançon, 25043, Cedex, France

    Christophe Cupillard

  41. Laboratoire Chronoenvironnement, UMR 6249 du CNRS, UFR des Sciences et Techniques, Besançon, 25030, Cedex, France

    Christophe Cupillard

  42. Department of Geosciences, Biogeology, University of Tübingen, Tübingen, 72074, Germany

    Hervé Bocherens & Dorothée G. Drucker

  43. Senckenberg Centre for Human Evolution and Palaeoenvironment, University of Tübingen, Tübingen, 72072, Germany

    Hervé Bocherens, Nicholas J. Conard, Katerina Harvati & Johannes Krause

  44. Department of Early Prehistory and Quaternary Ecology, University of Tübingen, Tübingen, 72070, Germany

    Nicholas J. Conard

  45. Institute for Archaeological Sciences, Paleoanthropology, University of Tübingen, Tübingen, 72070, Germany

    Katerina Harvati

  46. Museum of Anthropology and Ethnography, Saint Petersburg, 34, Russia

    Vyacheslav Moiseyev

  47. Department of Anthropology, Faculty of Science, Masaryk University, Brno, 611 37, Czech Republic

    Jiří Svoboda

  48. Institute of Archaeology at Brno, Academy of Science of the Czech Republic, Dolní Vĕstonice, 69129, Czech Republic

    Jiří Svoboda

  49. Department of Archaeology, Simon Fraser University, Burnaby, V5A 1S6, British Columbia, Canada

    Michael P. Richards

Authors
  1. Qiaomei Fu

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  2. Cosimo Posth

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  3. Mateja Hajdinjak

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  4. Martin Petr

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  5. Swapan Mallick

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  6. Daniel Fernandes

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  7. Anja Furtwängler

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  8. Wolfgang Haak

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  9. Matthias Meyer

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  10. Alissa Mittnik

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Contributions

J.Kr, S.P. and D.R. conceived the idea for the study. Q.F., C.P., M.H., W.H., M.Me, V.Slo, R.G.C., A.P.D., N.D., V.Sla, A.T., F.M., B.G., E.V., M.R.G.M., L.G.S., C.N.-M., M.T.-N., S.C., O.T.M., S.B., M.Per, D.Co, M.La, S.R., A.R., F.V., C.T., K.W., D.G., H.R., I.C., D.Fl, P.Se, M.A.M., C.C., H.B., N.J.C., K.H., V.M., D.G.D., J.S., D.Ca, R.P., J.Kr, S.P. and D.R. assembled archaeological material. Q.F., C.P., M.H., D.Fe, A.F., W.H., M.Me, A.M., B.N., N.R., V.Slo, S.T., H.B., D.G.D., M.P.R., R.P., J.Kr, S.P. and D.R. performed or supervised wet laboratory work. Q.F., C.P., M.H., M.Pet, S.M., A.P., I.L., M.Li, I.M., S.S., P.Sk, J.Ke, N.P. and D.R. analysed data. Q.F., C.P., M.H., M.Pet, J.Ke, S.P. and D.R. wrote the manuscript and supplements.

Corresponding author

Correspondence toDavid Reich.

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Competing interests

The authors declare no competing financial interests.

Additional information

Reviewer InformationNature thanks C. Lalueza-Fox and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Figure 1 A decrease in Neanderthal ancestry in the last 45,000 years.

This is similar toFig. 2, except we use ancestry estimates from rates of alleles matching to Neanderthal rather thanf4-ratios, as described inSupplementary Information section 3. The least-squares fit excludesOase1 (as an outlier with recent Neanderthal ancestry) and Europeans (known to have reduced Neanderthal ancestry). The regression slope is significantly negative (P = 0.00004,Extended Data Table 3).

Extended Data Figure 2 Heat matrix of pairwisef3(X,Y; Mbuti) for selected ancient individuals.

Only individuals with at least 30,000 SNPs covered at least once are analysed.

Extended Data Figure 3 Studying how the relatedness of non-European populations to pairs of European hunter-gatherers changes over time.

Statistics were examined of the formD(W, X; Y, Mbuti), with theZ-score given on they axis, whereW is an early European hunter-gatherer,X is another European hunter-gatherer (in chronological order on thex axis), andY is a non-European population (see legend).a,W = Kostenki14.b,W = GoyetQ116-1.c,W = Vestonice16.d,W = ElMiron. |Z| > 3 scores are considered statistically significant (horizontal line). The similarFig. 4b gives absoluteD-statistic values rather thanZ-scores (for W = Kostenki14) and uses pooled regions rather than individual populationsY.

Extended Data Figure 4 Three admixture graph models that fit the data forSatsurblia, an Upper Palaeolithic individual from the Caucasus.

These models use 127,057 SNPs covered in all populations. Estimated genetic drifts are given along the solid lines in units off2-distance (parts per thousand), and estimated mixture proportions are given along the dotted lines. All three models provide a fit to the allele frequency correlation data amongMbuti,Ust’-Ishim,Kostenki14,Vestonice16,Malta1,ElMiron andSatsurblia to within the limits of our resolution, in the sense that all empiricalf2-,f3- andf4-statistics relating the individuals are within three standard errors of the expectation of the model. Models in whichSatsurblia is treated as unadmixed cannot be fit.

Extended Data Table 1 The 51 ancient modern humans analysed in this study
Extended Data Table 2 Estimated proportion of Neanderthal ancestry
Extended Data Table 3 Significant correlation of Neanderthal ancestry estimate with specimen age
Extended Data Table 4 Sex determination for newly reported individuals
Extended Data Table 5 Allele counts at SNPs affected by selection in individuals with >1-fold coverage
Extended Data Table 6 All European hunter-gatherers beginning withKostenki14 share genetic drift with present-day Europeans

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data, Supplementary Tables, Supplementary Figures and additional references (see Contents for more details). (PDF 8052 kb)

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Fu, Q., Posth, C., Hajdinjak, M.et al. The genetic history of Ice Age Europe.Nature534, 200–205 (2016). https://doi.org/10.1038/nature17993

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Editorial Summary

Eurasian humans of the Upper Paleolithic

David Reich, Svante Pääbo and colleagues analyse ancient genomic data from 51 Eurasian humans who lived between 45,000 and 7,000 years ago. The data provide the most comprehensive view to date of the population history of pre-Neolithic Europe, and provide support for recurring migration and population turnover in European populations during this period. Neanderthal ancestry has reduced during the past 45,000 years from 3–6% to the present day value of around 2%.

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Nobel Prize in Physiology or Medicine 2022

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