Abstract

Ancient DNA studies have established that Neolithic European populations were descended from Anatolian migrants1,2,3,4,5,6,7,8 who received a limited amount of admixture from resident hunter-gatherers3,4,5,9. Many open questions remain, however, about the spatial and temporal dynamics of population interactions and admixture during the Neolithic period. Here we investigate the population dynamics of Neolithization across Europe using a high-resolution genome-wide ancient DNA dataset with a total of 180 samples, of which 130 are newly reported here, from the Neolithic and Chalcolithic periods of Hungary (6000–2900 bc, n = 100), Germany (5500–3000 bc, n = 42) and Spain (5500–2200 bc, n = 38). We find that genetic diversity was shaped predominantly by local processes, with varied sources and proportions of hunter-gatherer ancestry among the three regions and through time. Admixture between groups with different ancestry profiles was pervasive and resulted in observable population transformation across almost all cultural transitions. Our results shed new light on the ways in which gene flow reshaped European populations throughout the Neolithic period and demonstrate the potential of time-series-based sampling and modelling approaches to elucidate multiple dimensions of historical population interactions.

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Acknowledgements

We thank I. Lazaridis, P.-R. Loh, I. Mathieson, I. Olalde, E. Palkopoulou, N. Patterson and P. Skoglund for helpful comments and suggestions; J. Krause for providing the Stuttgart sample for which we generated a new library in this study; A. Whittle and A. Bayliss from The Times of Their Lives project for providing the radiocarbon date for sample VEJ5a; and B. Havasi (Balaton Museum), G. V. Székely (Katona József Museum), C. Farkas (Dobó István Museum), B. Nagy (Herman Ottó Museum), I. Pap, A. Kustár, T. Hajdu (Hungarian Natural History Museum), J. Ódor (Wosinsky Mór Museum), E. Nagy (Janus Pannonius Museum), P. Rácz (King St Stephen Museum), L. Szathmáry (Debrecen University), N. Kalicz, V. Voicsek, O. Vajda-Kiss, V. Majerik and I. Ko˝vári for assistance with samples. This work was supported by the Australian Research Council (grant DP130102158 to B.L. and W.H.), Hungarian National Research, Development and Innovation Office (K 119540 to B.M.), German Research Foundation (Al 287/7-1, 10-1 and 14-1 to K.W.A.), FEDER and Ministry of Economy and Competitiveness of Spain (BFU2015-64699-P to C.L.-F.), National Science Foundation (HOMINID grant BCS-1032255 to D.R.), National Institutes of Health (NIGMS grant GM100233 to D.R.), and Howard Hughes Medical Institute (D.R.).

Author information

Author notes

    • Mark Lipson
    •  & Anna Szécsényi-Nagy

    These authors contributed equally to this work.

Affiliations

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

    • Mark Lipson
    • , Swapan Mallick
    • , Nadin Rohland
    • , Kristin Stewardson
    • , Matthew Ferry
    • , Megan Michel
    • , Jonas Oppenheimer
    • , Nasreen Broomandkhoshbacht
    • , Eadaoin Harney
    • , Susanne Nordenfelt
    •  & David Reich
  2. Institute of Archaeology, Research Centre for the Humanities, Hungarian Academy of Sciences, Budapest 1097, Hungary

    • Anna Szécsényi-Nagy
    • , Annamária Pósa
    • , Balázs Stégmár
    • , Balázs Gusztáv Mende
    • , Kitti Köhler
    • , Krisztián Oross
    • , Mária Bondár
    • , Tibor Marton
    • , Anett Osztás
    • , János Jakucs
    • , Gábor Serlegi
    •  & Eszter Bánffy
  3. Medical and Population Genetics Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA

    • Swapan Mallick
    •  & David Reich
  4. Institute of Organismic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz 55128, Germany

    • Victoria Keerl
    • , Ruth Bollongino
    •  & Joachim Burger
  5. Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02115, USA

    • Kristin Stewardson
    • , Matthew Ferry
    • , Megan Michel
    • , Jonas Oppenheimer
    • , Nasreen Broomandkhoshbacht
    • , Eadaoin Harney
    •  & David Reich
  6. Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia

    • Bastien Llamas
    • , Alan Cooper
    •  & Wolfgang Haak
  7. Móra Ferenc Museum, Szeged 6720, Hungary

    • Tibor Paluch
    •  & Ferenc Horváth
  8. Herman Ottó Museum, Miskolc 3529, Hungary

    • Piroska Csengeri
    •  & Judit Koós
  9. Institute of Archaeological Sciences, Eötvös Loránd University, Budapest 1088, Hungary

    • Katalin Sebők
    • , Alexandra Anders
    •  & Pál Raczky
  10. Laczkó Dezso˝ Museum, Veszprém 8200, Hungary

    • Judit Regenye
  11. Balaton Museum, Keszthely 8360, Hungary

    • Judit P. Barna
  12. Department of Archaeological Excavations and Artefact Processing, Hungarian National Museum, Budapest 1088, Hungary

    • Szilvia Fábián
  13. Jósa András Museum, Nyíregyháza 4400, Hungary

    • Zoltán Toldi
  14. Déri Museum, Debrecen 4026, Hungary

    • Emese Gyöngyvér Nagy
    •  & János Dani
  15. Department of Biological Anthropology, Szeged University, Szeged 6726, Hungary

    • Erika Molnár
    •  & György Pálfi
  16. Department of Biochemistry and Medical Chemistry, University of Pécs, Pécs 7624, Hungary

    • László Márk
  17. Imaging Center for Life and Material Sciences, University of Pécs, Pécs 7624, Hungary

    • László Márk
  18. Szentágothai Research Center, University of Pécs, Pécs 7624, Hungary

    • László Márk
    • , Béla Melegh
    •  & Zsolt Bánfai
  19. PTE-MTA Human Reproduction Research Group, Pécs 7624, Hungary.

    • László Márk
  20. Department of Medical Genetics and Szentágothai Research Center, University of Pécs, Pécs 7624, Hungary

    • Béla Melegh
    •  & Zsolt Bánfai
  21. Dobó István Castle Museum, Eger 3300, Hungary.

    • László Domboróczki
  22. Department of Geography, Prehistory, and Archaeology, University of the Basque Country, Investigation Group IT622-13, Vitoria-Gasteiz 01006, Spain

    • Javier Fernández-Eraso
    •  & José Antonio Mujika-Alustiza
  23. CRONOS SC, Burgos 09007, Spain

    • Carmen Alonso Fernández
    •  & Javier Jiménez Echevarría
  24. Department of Prehistoric Archaeology, Free University of Berlin, Berlin 14195, Germany

    • Jörg Orschiedt
  25. Curt-Engelhorn-Centre Archaeometry gGmbH, Mannheim 68159, Germany

    • Jörg Orschiedt
  26. Commission for Westphalian Antiquities, Westphalia-Lippe Regional Association, 48157 Münster, Germany

    • Kerstin Schierhold
  27. State Office for Heritage Management and Archaeology Saxony-Anhalt and State Heritage Museum, Halle 06114, Germany

    • Harald Meller
  28. Environment Institute, University of Adelaide, Adelaide, South Australia 5005, Australia

    • Alan Cooper
  29. Romano-Germanic Commission, German Archaeological Institute, Frankfurt am Main 60325, Germany

    • Eszter Bánffy
  30. Center of Natural and Cultural History of Man, Danube Private University, Krems-Stein 3500, Austria

    • Kurt W. Alt
  31. Department of Biomedical Engineering, University of Basel, Allschwil 4123, Switzerland

    • Kurt W. Alt
  32. Institute for Integrative Prehistory and Archaeological Science, University of Basel, Basel 4055, Switzerland

    • Kurt W. Alt
  33. Institute of Evolutionary Biology (CSIC-UPF), Barcelona 08003, Spain

    • Carles Lalueza-Fox
  34. Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena 07745, Germany

    • Wolfgang Haak

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Contributions

A.S.-N., J.B., E.B., K.W.A., C.L.-F., W.H. and D.R. designed and supervised the study. B.G.M., K.K., K.O., M.B., T.M., A.O., J.J., T.P., F.H., P.C., J.K., K.Se., A.A., P.R., J.R., J.P.B., S.F., G.S., Z.T., E.G.N., J.D., E.M., G.P., L.M., B.M., Z.B., L.D., J.F.-E., J.A.M.-A., C.A.F., J.J.E., R.B., J.Or., K.Sc., H.M., A.C., J.B., E.B., K.W.A., C.L.-F. and W.H. provided samples and assembled archaeological and anthropological information. A.S.-N., A.P., B.S., V.K., N.R., K.St., M.F., M.M., J.Op., N.B., E.H., S.N. and B.L. performed laboratory work. M.L., A.S.-N., S.M. and D.R. analysed genetic data. M.L., A.S.-N. and D.R. wrote the manuscript with input from all coauthors.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Mark Lipson or Anna Szécsényi-Nagy or David Reich.

Reviewer Information Nature thanks P. Bellwood and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Supplementary information

PDF files

  1. 1.

    Life Sciences Reporting Summary

  2. 2.

    Supplementary Information

    This file contains Supplementary Notes 1-9.

Excel files

  1. 1.

    Supplementary Table 1

    This file contains detailed sample information.

  2. 2.

    Supplementary Table 2

    This file contains detailed mitochondrial genome results.