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

Naturevolume 536, pages419–424 (2016)Cite this article

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Abstract

We report genome-wide ancient DNA from 44 ancient Near Easterners ranging in time between ~12,000 and 1,400bc, 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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Figure 1: Genetic structure of ancient West Eurasia.
Figure 2: Basal Eurasian ancestry explains the reduced Neanderthal admixture in West Eurasians.
Figure 3: Genetic differentiation and its marked decrease over time in West Eurasia.
Figure 4: Modelling ancient West Eurasians, East Africans, East Eurasians and South Asians.

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Primary accessions

European Nucleotide Archive

Data deposits

The aligned sequences are available through the European Nucleotide Archive under accession numberPRJEB14455. Fully public subsets of the analysis datasets are athttp://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. TheFig. 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

Author notes

  1. Ron Pinhasi and David Reich: These authors jointly supervised this work.

Authors and Affiliations

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

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

  2. Broad Institute of MIT and Harvard, Cambridge, 02142, Massachusetts, 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, 99362, Washington, USA

    Gary Rollefson

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

    Deborah C. Merrett

  6. Howard Hughes Medical Institute, Harvard Medical School, Boston, 02115, Massachusetts, 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. Department of Life Sciences, CIAS, 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, 30322, Georgia, USA

    Kendra Sirak

  11. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, 02138, Massachusetts, 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, 100044, Beijing, 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, 19104, Pennsylvania, 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, R3B 2E9, Manitoba, 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. Department of Genomics of Common Disease, Imperial College London, 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, HD1 3DH, Huddersfield, 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

Authors
  1. Iosif Lazaridis
  2. Dani Nadel
  3. Gary Rollefson
  4. Deborah C. Merrett
  5. Nadin Rohland
  6. Swapan Mallick
  7. Daniel Fernandes
  8. Mario Novak
  9. Beatriz Gamarra
  10. Kendra Sirak
  11. Sarah Connell
  12. Kristin Stewardson
  13. Eadaoin Harney
  14. Qiaomei Fu
  15. Gloria Gonzalez-Fortes
  16. Eppie R. Jones
  17. Songül Alpaslan Roodenberg
  18. György Lengyel
  19. Fanny Bocquentin
  20. Boris Gasparian
  21. Janet M. Monge
  22. Michael Gregg
  23. Vered Eshed
  24. Ahuva-Sivan Mizrahi
  25. Christopher Meiklejohn
  26. Fokke Gerritsen
  27. Luminita Bejenaru
  28. Matthias Blüher
  29. Archie Campbell
  30. Gianpiero Cavalleri
  31. David Comas
  32. Philippe Froguel
  33. Edmund Gilbert
  34. Shona M. Kerr
  35. Peter Kovacs
  36. Johannes Krause
  37. Darren McGettigan
  38. Michael Merrigan
  39. D. Andrew Merriwether
  40. Seamus O'Reilly
  41. Martin B. Richards
  42. Ornella Semino
  43. Michel Shamoon-Pour
  44. Gheorghe Stefanescu
  45. Michael Stumvoll
  46. Anke Tönjes
  47. Antonio Torroni
  48. James F. Wilson
  49. Loic Yengo
  50. Nelli A. Hovhannisyan
  51. Nick Patterson
  52. Ron Pinhasi
  53. David Reich

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.

Corresponding authors

Correspondence toIosif Lazaridis,Ron Pinhasi orDavid Reich.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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 figures and tables

Extended Data Figure 1 Principal components analysis of 991 present-day West Eurasians.

The PCA analysis is performed on the same set of individuals as are reported inFig. 1b, using EIGENSOFT. Here, we colour the samples by population (to highlight the present-day populations) instead of using grey points as inFig. 1b (where the goal is to highlight ancient samples).

Extended Data Figure 2 Genetic structure in ancient West Eurasian populations across time and decline of genetic differentiation over time.

a, ADMIXTURE model-based clustering analysis of 2,583 present-day humans and 281 ancient samples; we show the results only for ancient samples forK = 11 clusters.b, PairwiseFST between 19 Ancient West Eurasian populations (arranged in approximate chronological order), and select present-day populations.

Extended Data Figure 3 Outgroupf3(Mbuti; X, Y) for pairs of ancient populations.

The dendrogram is plotted for convenience and should not be interpreted as a phylogenetic tree. Areas of high shared genetic drift are ‘yellow’ and include from top-right to bottom-left along the diagonal: early Anatolian and European farmers; European hunter–gatherers, Steppe populations and populations admixed with steppe ancestry; populations from the Levant from the Epipalaeolithic (Natufians) to the Bronze Age; populations from Iran from the Mesolithic to the Late Neolithic.

Extended Data Figure 4 Reduction of genetic differentiation in West Eurasia over time.

We measure differentiation byFST. Each column of the 5 × 5 matrix of plots represents a major region and each row the earliest population with at least two individuals from each major region.

Extended Data Figure 5 West Eurasian related admixture in East Africa, Eastern Eurasia and South Asia.

a, Levantine ancestry in Eastern Africa in the Human Origins dataset.b, Levantine ancestry in different Eastern African population in the dataset from Paganiet al. (2012); the remainder of the ancestry is a clade with Mota, a ~4,500 year old sample from Ethiopia49.c, EHG ancestry in Eastern Eurasians.d, Afontova Gora (AG2)-related ancestry in Eastern Eurasians; the remainder of their ancestry is a clade with Onge.e, Mixture proportions for South Asian populations showing that they can be modelled as having West Eurasian-related ancestry similar to that in populations from both the Eurasian steppe and Iran.

Extended Data Figure 7 Admixture from ghost populations using ‘cline intersection’.

a–f, We model eachTest population (purple) as a mixture (pink) of a fixed reference population (blue) and a ghost population (orange) residing on the cline defined by two other populations (red and green) according to the visualization method ofSupplementary Information, section 10.a, Early/Middle Bronze Age steppe populations are a mixture of Iran_ChL and a population on the WHG→SHG cline.b, Scandinavian hunter–gatherers (SHG) are a mixture of WHG and a population on the Iran_ChL→Steppe_EMBA cline.c, Caucasus hunter–gatherers (CHG) are a mixture of Iran_N and both WHG and EHG.d, Late Neolithic/Bronze Age Europeans are a mixture of the preceding Europe_MNChL population and a population with both EHG and Iran_ChL ancestry.e, Somali are a mixture of Mota49 and a population on the Iran_ChL→Levant_BA cline.f, Eastern European hunter–gatherers (EHG) are a mixture of WHG and a population on the Onge→Han cline.

Extended Data Figure 8 Admixture from a ‘ghost’ ANE population into both European and Eastern Eurasian ancestry.

EHG, and Upper Palaeolithic Siberians Mal’ta 1 (MA1) and Afontova Gora 2 (AG2) are positioned near the intersection of clines formed by European hunter–gatherers (WHG, SHG, EHG) and Eastern non-Africans in the space of outgroupf3-statistics of the formf3(Mbuti; Papuan,Test) andf3(Mbuti; Switzerland_HG,Test).

Extended Data Table 1 No evidence for admixture related to sub-Saharan Africans in Natufians
Extended Data Table 2 Admixturef3-statistics

Supplementary information

Supplementary Table 1

This file contains Supplementary Data Table 1. (XLSX 65 kb)

Supplementary Table 2

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Supplementary Table 3

This file contains Supplementary Data Table 3. (XLSX 60 kb)

Supplementary Information

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Lazaridis, I., Nadel, D., Rollefson, G.et al. Genomic insights into the origin of farming in the ancient Near East.Nature536, 419–424 (2016). https://doi.org/10.1038/nature19310

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Editorial Summary

Who were the early farmers?

David Reich and colleagues report the genomic analysis of samples from 44 individuals who lived from around 12,000 to 1,400BC in Near East regions, including modern Armenia, Turkey, Israel and Jordan. The analyses provide insights into demographics of the human populations that transitioned to farming.

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