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

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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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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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

Authors and Affiliations

Authors

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 to Iosif Lazaridis, Ron Pinhasi or David Reich.

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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 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 FST between 19 Ancient West Eurasian populations (arranged in approximate chronological order), and select present-day populations.

Extended Data Figure 3 Outgroup f3(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 FST. 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’.

af, 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 f3-statistics of the form f3(Mbuti; Papuan, Test) and f3(Mbuti; Switzerland_HG, Test).

Extended Data Table 1 No evidence for admixture related to sub-Saharan Africans in Natufians
Extended Data Table 2 Admixture f3-statistics

Supplementary information

Supplementary Table 1

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Supplementary Table 2

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Supplementary Table 3

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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. Nature 536, 419–424 (2016). https://doi.org/10.1038/nature19310

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