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Genomic insights into the origin of farming in the ancient Near East

Nature 536, 419–424 (25 August 2016) | Download Citation

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Abstract

We report genome-wide ancient DNA from 44 ancient Near Easterners ranging in time between ~12,000 and 1,400 bc, from Natufian hunter–gatherers to Bronze Age farmers. We show that the earliest populations of the Near East derived around half their ancestry from a ‘Basal Eurasian’ lineage that had little if any Neanderthal admixture and that separated from other non-African lineages before their separation from each other. The first farmers of the southern Levant (Israel and Jordan) and Zagros Mountains (Iran) were strongly genetically differentiated, and each descended from local hunter–gatherers. By the time of the Bronze Age, these two populations and Anatolian-related farmers had mixed with each other and with the hunter–gatherers of Europe to greatly reduce genetic differentiation. The impact of the Near Eastern farmers extended beyond the Near East: farmers related to those of Anatolia spread westward into Europe; farmers related to those of the Levant spread southward into East Africa; farmers related to those of Iran spread northward into the Eurasian steppe; and people related to both the early farmers of Iran and to the pastoralists of the Eurasian steppe spread eastward into South Asia.

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Primary accessions

European Nucleotide Archive

Data deposits

The aligned sequences are available through the European Nucleotide Archive under accession number PRJEB14455. Fully public subsets of the analysis datasets are at http://genetics.med.harvard.edu/reichlab/Reich_Lab/Datasets.html. The complete dataset (including present-day humans for which the informed consent is not consistent with public posting of data) is available to researchers who send a signed letter to D.R. indicating that they will abide by specified usage conditions (Supplementary Information, section 2).

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Acknowledgements

We thank the 238 human subjects who donated samples for genome-wide analysis, and D. Labuda and P. Zalloua for sharing samples from Poland and Lebanon. The Fig. 1a map was plotted in R using the worldHiRes map of the ‘mapdata’ package (using public domain data from the CIA World Data Bank II). We thank O. Bar-Yosef, M. Bonogofsky, I. Hershkowitz, M. Lipson, I. Mathieson, H. May, R. Meadow, I. Olalde, S. Paabo, P. Skoglund, and N. Nakatsuka for comments and critiques, and D. Bradley, M. Dallakyan, S. Esoyan, M. Ferry and M. Michel, and A. Yesayan, for contributions to bone preparation and ancient DNA work. D.F. and M.N. were supported by Irish Research Council grants GOIPG/2013/36 and GOIPD/2013/1, respectively. S.C. was funded by the Irish Research Council for Humanities and Social Sciences (IRCHSS) ERC Support Programme. Q.F. was funded by the Bureau of International Cooperation of the Chinese Academy of Sciences, the National Natural Science Foundation of China (L1524016) and the Chinese Academy of Sciences Discipline Development Strategy Project (2015-DX-C-03). The Scottish diversity data was funded by the Chief Scientist Office of the Scottish Government Health Directorates (CZD/16/6), the Scottish Funding Council (HR03006), and a project grant from the Scottish Executive Health Department, Chief Scientist Office (CZB/4/285). M.S., A.Tön., M.B. and P.K. were supported by the German Research Foundation (CRC 1052; B01, B03, C01). M.S.-P. was funded by a Wenner-Gren Foundation Dissertation Fieldwork grant (9005), and by the National Science Foundation DDRIG (BCS-1455744). P.K. was funded by the Federal Ministry of Education and Research, Germany (FKZ: 01EO1501). J.F.W. acknowledge the MRC ‘QTL in Health and Disease’ programme grant. The Romanian diversity data was supported by the EC Commission, Directorate General XII (Supplementary Agreement ERBCIPDCT 940038 to the Contract ERBCHRXCT 920032, coordinated by A. Piazza, Turin, Italy). M.R. received support from the Leverhulme Trust’s Doctoral Scholarship programme. O.S. and A.Tor. were supported by the University of Pavia (MIGRAT-IN-G) and the Italian Ministry of Education, University and Research: Progetti Ricerca Interesse Nazionale 2012. The Raqefet Cave Natufian project was supported by funds from the National Geographic Society (grant 8915-11), the Wenner-Gren Foundation (grant 7481) and the Irene Levi-Sala CARE Foundation, while radiocarbon dating on the samples was funded by the Israel Science Foundation (grant 475/10; E. Boaretto). R.P. was supported by ERC starting grant ADNABIOARC (263441). D.R. was supported by NIH grant GM100233, by NSF HOMINID BCS-1032255, and is a Howard Hughes Medical Institute investigator.

Author information

    • Ron Pinhasi
    •  & David Reich

    These authors jointly supervised this work.

Affiliations

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

    • Iosif Lazaridis
    • , Nadin Rohland
    • , Swapan Mallick
    • , Kristin Stewardson
    • , Eadaoin Harney
    • , Qiaomei Fu
    •  & David Reich

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

    • Iosif Lazaridis
    • , Swapan Mallick
    • , Nick Patterson
    •  & David Reich

  3. The Zinman Institute of Archaeology, University of Haifa, Haifa 3498838, Israel

    • Dani Nadel

  4. Department of Anthropology, Whitman College, Walla Walla, Washington 99362, USA

    • Gary Rollefson

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

    • Deborah C. Merrett

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

    • Swapan Mallick
    • , Kristin Stewardson
    • , Eadaoin Harney
    •  & David Reich

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

    • Daniel Fernandes
    • , Mario Novak
    • , Beatriz Gamarra
    • , Kendra Sirak
    • , Sarah Connell
    •  & Ron Pinhasi

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

    • Daniel Fernandes

  9. Institute for Anthropological Research, Zagreb 10000, Croatia

    • Mario Novak

  10. Department of Anthropology, Emory University, Atlanta, Georgia 30322, USA

    • Kendra Sirak

  11. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Eadaoin Harney

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

    • Qiaomei Fu

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

    • Qiaomei Fu

  14. Department of Biology and Evolution, University of Ferrara, Ferrara I-44121, Italy

    • Gloria Gonzalez-Fortes

  15. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK

    • Eppie R. Jones

  16. J.M. van Nassaulaan 9, Santpoort-Noord 2071 VA, The Netherlands

    • Songül Alpaslan Roodenberg

  17. Department of Prehistory and Archaeology, University of Miskolc, Miskolc-Egyetemváros 3515, Hungary

    • György Lengyel

  18. French National Centre for Scientific Research, UMR 7041, Nanterre Cedex 92023, France

    • Fanny Bocquentin

  19. Institute of Archaeology and Ethnology, National Academy of Sciences of the Republic of Armenia, Yerevan 0025, Republic of Armenia

    • Boris Gasparian

  20. University of Pennsylvania Museum of Archaeology and Anthropology, Philadelphia, Pennsylvania 19104, USA

    • Janet M. Monge
    •  & Michael Gregg

  21. Israel Antiquities Authority, Jerusalem 91004, Israel

    • Vered Eshed
    •  & Ahuva-Sivan Mizrahi

  22. Department of Anthropology, University of Winnipeg, Winnipeg, Manitoba R3B 2E9, Canada

    • Christopher Meiklejohn

  23. Netherlands Institute in Turkey, Istanbul 34433, Turkey

    • Fokke Gerritsen

  24. Faculty of Biology, Alexandru Ioan Cuza University of Iasi, Iasi 700505, Romania

    • Luminita Bejenaru

  25. Department of Internal Medicine and Dermatology, Clinic of Endocrinology and Nephrology, Leipzig 04103, Germany

    • Matthias Blüher
    • , Michael Stumvoll
    •  & Anke Tönjes

  26. Generation Scotland, Centre for Genomic and Experimental Medicine, MRC Institute of Genetics and Molecular Medicine, University of Edinburgh, Western General Hospital, Edinburgh EH4 2XU, UK

    • Archie Campbell
    •  & Shona M. Kerr

  27. RCSI Molecular & Cellular Therapeutics, Royal College of Surgeons in Ireland, Dublin 2, Ireland

    • Gianpiero Cavalleri
    •  & Edmund Gilbert

  28. Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona 08003, Spain

    • David Comas

  29. Univ. Lille, CNRS, Institut Pasteur de Lille, UMR 8199 - EGID, Lille F-59000, France

    • Philippe Froguel
    •  & Loic Yengo

  30. Imperial College London, Department of Genomics of Common Disease, London Hammersmith Hospital, London W12 0HS, UK

    • Philippe Froguel

  31. Leipzig University Medical Center, IFB Adiposity Diseases, Leipzig 04103, Germany

    • Peter Kovacs

  32. Max Planck Institute for the Science of Human History, Jena 07745, Germany

    • Johannes Krause

  33. School of History, Newman Building, University College Dublin, Belfield, Dublin 4, Ireland

    • Darren McGettigan

  34. Genealogical Society of Ireland, Dún Laoghaire, County Dublin, Ireland

    • Michael Merrigan
    •  & Seamus O'Reilly

  35. Department of Anthropology, Binghamton University, State University of New York, New York 13902, USA

    • D. Andrew Merriwether
    •  & Michel Shamoon-Pour

  36. Department of Biological Sciences, School of Applied Sciences, University of Huddersfield, Queensgate, Huddersfield HD1 3DH, UK

    • Martin B. Richards

  37. Dipartimento di Biologia e Biotecnologie “L. Spallanzani”, Università di Pavia, Pavia 27100, Italy

    • Ornella Semino
    •  & Antonio Torroni

  38. Institutul de Cercetari Biologice, Iaşi 700505, Romania

    • Gheorghe Stefanescu

  39. Usher Institute for Population Health Sciences and Informatics, University of Edinburgh, Edinburgh EH8 9AG, UK

    • James F. Wilson

  40. MRC Human Genetics Unit, MRC Institute of Genetics and Molecular Medicine, University of Edinburgh, Edinburgh EH4 2XU, UK

    • James F. Wilson

  41. Center of Excellence in Applied Biosciences, Yerevan State University, Yerevan 0025, Republic of Armenia

    • Nelli A. Hovhannisyan

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Contributions

R.P. and D.R. conceived the idea for the study. D.N., G.R., D.C.M., S.C., S.A.R., G.L., F.B., B.Gas., J.M.M., M.G., V.E., A.M., C.M., F.G., N.A.H. and R.P. assembled skeletal material. N.R., D.F., M.N., B.Gam., K.Si., S.C., K.St., E.H., Q.F., G.G.-F., E.R.J., R.P. and D.R. performed or supervised ancient DNA wet laboratory work. L.B, M.B., A.C., G.C., D.C., P.F., E.G., S.M.K., P.K., J.K., D.M., M.M., D.A.M., S.O., M.B.R., O.S., M.S.-P., G.S., M.S., A.Tön., A.Tor., J.F.W., L.Y. and D.R. assembled present-day samples for genotyping. I.L, N.P. and D.R. developed methods for data analysis. I.L., S.M., Q.F., N.P. and D.R. analysed data. I.L., R.P. and D.R. wrote the manuscript and supplements.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Iosif Lazaridis or Ron Pinhasi or David Reich.

Reviewer Information

Nature thanks O. Bar-Yosef, G. Coop and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data

Extended data figures

  1. 1.

    Principal components analysis of 991 present-day West Eurasians.

  2. 2.

    Genetic structure in ancient West Eurasian populations across time and decline of genetic differentiation over time.

  3. 3.

    Outgroup f3(Mbuti; X, Y) for pairs of ancient populations.

  4. 4.

    Reduction of genetic differentiation in West Eurasia over time.

  5. 5.

    West Eurasian related admixture in East Africa, Eastern Eurasia and South Asia.

  6. 6.

    Inferred position of ancient populations in West Eurasian PCA according to the model of Fig. 4.

  7. 7.

    Admixture from ghost populations using ‘cline intersection’.

  8. 8.

    Admixture from a ‘ghost’ ANE population into both European and Eastern Eurasian ancestry.

Extended data tables

  1. 1.

    No evidence for admixture related to sub-Saharan Africans in Natufians

  2. 2.

    Admixture f3-statistics

Supplementary information

Excel files

  1. 1.

    Supplementary Table 1

    This file contains Supplementary Data Table 1.

  2. 2.

    Supplementary Table 2

    This file contains Supplementary Data Table 2.

  3. 3.

    Supplementary Table 3

    This file contains Supplementary Data Table 3.

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Text, Data and References – see contents page for details.

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