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The genetic history of Ice Age Europe

Abstract

Modern humans arrived in Europe ~45,000 years ago, but little is known about their genetic composition before the start of farming ~8,500 years ago. Here we analyse genome-wide data from 51 Eurasians from ~45,000–7,000 years ago. Over this time, the proportion of Neanderthal DNA decreased from 3–6% to around 2%, consistent with natural selection against Neanderthal variants in modern humans. Whereas there is no evidence of the earliest modern humans in Europe contributing to the genetic composition of present-day Europeans, all individuals between ~37,000 and ~14,000 years ago descended from a single founder population which forms part of the ancestry of present-day Europeans. An ~35,000-year-old individual from northwest Europe represents an early branch of this founder population which was then displaced across a broad region, before reappearing in southwest Europe at the height of the last Ice Age ~19,000 years ago. During the major warming period after ~14,000 years ago, a genetic component related to present-day Near Easterners became widespread in Europe. These results document how population turnover and migration have been recurring themes of European prehistory.

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Figure 1: Location and age of the 51 ancient modern humans.
Figure 2: Decrease of Neanderthal ancestry over time.
Figure 3: Genetic clustering of the ancient modern humans.
Figure 4: Population history inferences.

Accession codes

Primary accessions

European Nucleotide Archive

Data deposits

The aligned sequences are available through the European Nucleotide Archive under accession number PRJEB13123.

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Acknowledgements

We thank B. Alex, D. Meltzer, P. Moorjani, I. Olalde, S. Sankararaman and B. Viola for comments, K. Stewardson and E. Harney for sample screening, and F. Hallgren for sharing a radiocarbon date for Motala12. The Fig. 1 map is plotted using data available under the Open Database License © OpenStreetMap (http://www.openstreetmap.org/copyright). The Goyet project led by H.R. was funded by the Wenner-Gren Foundation (Gr. 7837), the College of Social and Behavioral Sciences of CSUN, the CSUN Competition for Research, Scholarship and Creative Activity Awards, and the RBINS. The excavation of the El Mirón Cave burial, led by L.G.S. and M.R.G.M., was supported by the Gobierno de Cantabria, the L.S.B. Leakey Foundation, the University of New Mexico, the Stone Age Research Fund (J. and R. Auel, principal donors), the town of Ramales de la Victoria and the Universidad de Cantabria. Excavations at Grotta Paglicci were performed by A. Palma di Cesnola in collaboration with the Soprintendenza Archeologia della Puglia (founded by MIUR and local Institutions). Research at Riparo Villabruna was supported by MIBACT and the Veneto Region. Q.F. was funded by the Special Foundation of the President of the Chinese Academy of Sciences (2015–2016), the Bureau of International Cooperation of the Chinese Academy of Sciences, the Chinese Academy of Sciences (XDA05130202), the National Natural Science Foundation of China (L1524016) and the Chinese Academy of Sciences Discipline Development Strategy Project (2015-DX-C-03). D.Fe was supported by an Irish Research Council grant (GOIPG/2013/36). I.M. was supported by a long-term fellowship from the Human Frontier Science Program LT001095/2014-L. P.Sk was supported by the Swedish Research Council (VR 2014-453). S.T., and M.P.R. were funded by the Max Planck Society. C.N.-M. was funded by FWF P-17258, P-19347, P-21660 and P-23612. S.C. and O.T.M. were funded by a ‘Karsthives’ Grant PCCE 31/2010 (CNCS-UEFISCDI, Romania). A.P.D., N.D., V.Sla and N.D. were funded by the Russian Science Foundation (project No.14-50-00036). M.A.M. was funded by a Marie Curie Intra-European Fellowship within the 7th European Community Framework Programme (grant number PIEF-GA-2008-219965). M.La and D.C. were funded by grants PRIN 2010-11 and 2010EL8TXP_003. C.C. and the research about the French Jura sites of Rochedane, Rigney and Ranchot was funded by the Collective Research Program (PCR) (2005-2008). K.H. was supported by the European Research Council (ERC StG 283503) and the Deutsche Forschungsgemeinschaft (DFG INST37/706-1FUGG, DFG FOR2237). D.G.D. was funded by the European Social Fund and Ministry of Science, Research and Arts of Baden-Württemberg. R.P. was funded by ERC starting grant ADNABIOARC (263441). J.Ke was funded by a grant from the Deutsche Forschungsgemeinschaft (SFB1052, project A02). J.Kr was funded by DFG grant KR 4015/1-1, the Baden Württemberg Foundation, and the Max Planck Society. S.P. were funded by the Max Planck Society and the Krekeler Foundation. D.R. was funded by NSF HOMINID grant BCS-1032255, NIH (NIGMS) grant GM100233, and the Howard Hughes Medical Institute.

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Authors

Contributions

J.Kr, S.P. and D.R. conceived the idea for the study. Q.F., C.P., M.H., W.H., M.Me, V.Slo, R.G.C., A.P.D., N.D., V.Sla, A.T., F.M., B.G., E.V., M.R.G.M., L.G.S., C.N.-M., M.T.-N., S.C., O.T.M., S.B., M.Per, D.Co, M.La, S.R., A.R., F.V., C.T., K.W., D.G., H.R., I.C., D.Fl, P.Se, M.A.M., C.C., H.B., N.J.C., K.H., V.M., D.G.D., J.S., D.Ca, R.P., J.Kr, S.P. and D.R. assembled archaeological material. Q.F., C.P., M.H., D.Fe, A.F., W.H., M.Me, A.M., B.N., N.R., V.Slo, S.T., H.B., D.G.D., M.P.R., R.P., J.Kr, S.P. and D.R. performed or supervised wet laboratory work. Q.F., C.P., M.H., M.Pet, S.M., A.P., I.L., M.Li, I.M., S.S., P.Sk, J.Ke, N.P. and D.R. analysed data. Q.F., C.P., M.H., M.Pet, J.Ke, S.P. and D.R. wrote the manuscript and supplements.

Corresponding author

Correspondence to David Reich.

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The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks C. Lalueza-Fox 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 A decrease in Neanderthal ancestry in the last 45,000 years.

This is similar to Fig. 2, except we use ancestry estimates from rates of alleles matching to Neanderthal rather than f4-ratios, as described in Supplementary Information section 3. The least-squares fit excludes Oase1 (as an outlier with recent Neanderthal ancestry) and Europeans (known to have reduced Neanderthal ancestry). The regression slope is significantly negative (P = 0.00004, Extended Data Table 3).

Extended Data Figure 2 Heat matrix of pairwise f3(X, Y; Mbuti) for selected ancient individuals.

Only individuals with at least 30,000 SNPs covered at least once are analysed.

Extended Data Figure 3 Studying how the relatedness of non-European populations to pairs of European hunter-gatherers changes over time.

Statistics were examined of the form D(W, X; Y, Mbuti), with the Z-score given on the y axis, where W is an early European hunter-gatherer, X is another European hunter-gatherer (in chronological order on the x axis), and Y is a non-European population (see legend). a, W = Kostenki14. b, W = GoyetQ116-1. c, W = Vestonice16. d, W = ElMiron. |Z| > 3 scores are considered statistically significant (horizontal line). The similar Fig. 4b gives absolute D-statistic values rather than Z-scores (for W = Kostenki14) and uses pooled regions rather than individual populations Y.

Extended Data Figure 4 Three admixture graph models that fit the data for Satsurblia, an Upper Palaeolithic individual from the Caucasus.

These models use 127,057 SNPs covered in all populations. Estimated genetic drifts are given along the solid lines in units of f2-distance (parts per thousand), and estimated mixture proportions are given along the dotted lines. All three models provide a fit to the allele frequency correlation data among Mbuti, Ust’-Ishim, Kostenki14, Vestonice16, Malta1, ElMiron and Satsurblia to within the limits of our resolution, in the sense that all empirical f2-, f3- and f4-statistics relating the individuals are within three standard errors of the expectation of the model. Models in which Satsurblia is treated as unadmixed cannot be fit.

Extended Data Table 1 The 51 ancient modern humans analysed in this study
Extended Data Table 2 Estimated proportion of Neanderthal ancestry
Extended Data Table 3 Significant correlation of Neanderthal ancestry estimate with specimen age
Extended Data Table 4 Sex determination for newly reported individuals
Extended Data Table 5 Allele counts at SNPs affected by selection in individuals with >1-fold coverage
Extended Data Table 6 All European hunter-gatherers beginning with Kostenki14 share genetic drift with present-day Europeans

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Fu, Q., Posth, C., Hajdinjak, M. et al. The genetic history of Ice Age Europe. Nature 534, 200–205 (2016). https://doi.org/10.1038/nature17993

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