Genomic insights into the origin of farming in the ancient Near East (original) (raw)

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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.

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

Corresponding authors

Correspondence toIosif Lazaridis, Ron Pinhasi or David Reich.

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The authors declare no competing financial interests.

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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 in Fig. 1b, using EIGENSOFT. Here, we colour the samples by population (to highlight the present-day populations) instead of using grey points as in Fig. 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 for K = 11 clusters. b, Pairwise _F_ST between 19 Ancient West Eurasian populations (arranged in approximate chronological order), and select present-day populations.

Extended Data Figure 3 Outgroup _f_3(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 by _F_ST. 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 Pagani et 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 6 Inferred position of ancient populations in West Eurasian PCA according to the model of Fig. 4.

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

a–f, We model each Test 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 of Supplementary 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 outgroup _f_3-statistics of the form _f_3(Mbuti; Papuan, Test) and _f_3(Mbuti; Switzerland_HG, Test).

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

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Extended Data Table 2 Admixture _f_3-statistics

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Lazaridis, I., Nadel, D., Rollefson, G. et al. Genomic insights into the origin of farming in the ancient Near East.Nature 536, 419–424 (2016). https://doi.org/10.1038/nature19310

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• Received: 08 March 2016
• Accepted: 18 July 2016
• Published: 25 July 2016
• Issue Date: 25 August 2016
• DOI: https://doi.org/10.1038/nature19310