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Parallel palaeogenomic transects reveal complex genetic history of early European farmers - Nature

  • ️Reich, David
  • ️Wed Nov 08 2017

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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

  1. Mark Lipson and Anna Szécsényi-Nagy: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Genetics, Harvard Medical School, Boston, 02115, Massachusetts, 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, 02142, Massachusetts, 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, 02115, Massachusetts, 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, 5005, South Australia, 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, Münster, 48157, 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

Authors

  1. Mark Lipson

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  2. Anna Szécsényi-Nagy

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  3. Swapan Mallick

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  4. Annamária Pósa

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  5. Balázs Stégmár

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  6. Victoria Keerl

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  7. Nadin Rohland

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  8. Kristin Stewardson

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  9. Matthew Ferry

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  10. Megan Michel

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  11. Jonas Oppenheimer

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  12. Nasreen Broomandkhoshbacht

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  13. Eadaoin Harney

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  14. Susanne Nordenfelt

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  15. Bastien Llamas

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  16. Balázs Gusztáv Mende

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  17. Kitti Köhler

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  18. Krisztián Oross

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  19. Mária Bondár

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  20. Tibor Marton

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  21. Anett Osztás

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  22. János Jakucs

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  23. Tibor Paluch

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  24. Ferenc Horváth

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  25. Piroska Csengeri

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  26. Judit Koós

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  27. Katalin Sebők

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  28. Alexandra Anders

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  29. Pál Raczky

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  30. Judit Regenye

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  31. Judit P. Barna

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  32. Szilvia Fábián

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  33. Gábor Serlegi

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  34. Zoltán Toldi

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  35. Emese Gyöngyvér Nagy

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  36. János Dani

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  37. Erika Molnár

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  38. György Pálfi

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  39. László Márk

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  40. Béla Melegh

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  41. Zsolt Bánfai

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  42. László Domboróczki

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  43. Javier Fernández-Eraso

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  44. José Antonio Mujika-Alustiza

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  45. Carmen Alonso Fernández

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  46. Javier Jiménez Echevarría

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  47. Ruth Bollongino

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  48. Jörg Orschiedt

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  49. Kerstin Schierhold

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  50. Harald Meller

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  51. Alan Cooper

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  52. Joachim Burger

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  53. Eszter Bánffy

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  54. Kurt W. Alt

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  55. Carles Lalueza-Fox

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  56. Wolfgang Haak

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  57. David Reich

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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.

Corresponding authors

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

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Competing interests

The authors declare no competing financial interests.

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

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Extended data figures and tables

Extended Data Figure 1 First two principal components from the PCA.

We computed the principal components (PCs) for a set of 782 present-day western Eurasian individuals genotyped on the Affymetrix Human Origins array (background grey points) and then projected ancient individuals onto these axes. A close-up omitting the present-day Bedouin population is shown.

Extended Data Figure 2 Scaffold admixture graph used for modelling the European Neolithic populations.

Dotted lines denote admixture events. Neolithic Anatolians, LB1 and KO1 are modelled as admixed, with basal Eurasian ancestry, deeper European hunter-gatherer ancestry and FEF ancestry, respectively. European test populations were fitted as a mixture of FEF and ancestry related to one or two of the four WHG individuals (here VIL-related as an example). See Supplementary Information section 6 for details.

Extended Data Figure 3 Examples of ALDER weighted linkage disequilibrium decay curves.

Weighted linkage disequilibrium (LD) curves are shown as a function of genetic distance d, using Neolithic Anatolians and WHG as references, for four individuals: BAM17b (Starčevo Early Neolithic), CB13 (Iberia Early Neolithic), Bla8 (Blätterhöhle hunter-gatherer) and KO1. The results shown here use helper individuals M11-363 (Neolithic Anatolian), L11-322 (Neolithic Anatolian), BIC and LB1, respectively, and have fitted dates (blue curves) of 3.8 ± 1.2, 18.3 ± 6.0, 13.1 ± 2.7 and 21.6 ± 8.8 generations (compared to final individual-level dates of 4.5 ± 1.9, 17.5 ± 3.5, 12.1 ± 2.9 and 21.0 ± 7.0 generations; see Supplementary Information section 7). Note that the x-axis scales are different for the four plots.

Extended Data Figure 4 Hunter-gatherer ancestry as a function of latitude and longitude for Neolithic individuals.

a, b, Early and Middle Neolithic Hungary. c, d, Late Neolithic and Chalcolithic Hungary. e, f, Iberia. HG, hunter-gatherer; Protob., Protoboleráz.

Extended Data Figure 5 Germany and Iberia time series and simulated data.

a, Dates of admixture. b, Hunter-gatherer ancestry proportions, normalized to the total of the most recent (rightmost) population. Symbols are as in Figs 1, 2 and indicate population-level mean ± 2 s.e.m. Yellow dashed lines represent continuous admixture simulations: from top to bottom, diminishing 5% per generation, diminishing 3%, diminishing 1% and uniform. Green solid lines represent pulse-plus-continuous admixture simulations: from top to bottom, all hunter-gatherer ancestry in a pulse at time zero; three-quarters of final hunter-gatherer ancestry in an initial pulse followed by uniform continuous gene flow; half in initial pulse and half continuous; and one-quarter in initial pulse.

Extended Data Table 1 Information for the Neolithic individuals from Hungary

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Extended Data Table 2 Information for the Neolithic individuals from Germany and Spain

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Extended Data Table 3 Admixture graph results for Neolithic populations

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Extended Data Table 4 Mean dates of admixture for Neolithic populations

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Supplementary information

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Lipson, M., Szécsényi-Nagy, A., Mallick, S. et al. Parallel palaeogenomic transects reveal complex genetic history of early European farmers. Nature 551, 368–372 (2017). https://doi.org/10.1038/nature24476

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  • Received: 01 March 2017

  • Accepted: 06 October 2017

  • Published: 08 November 2017

  • Issue Date: 16 November 2017

  • DOI: https://doi.org/10.1038/nature24476