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Parallel palaeogenomic transects reveal complex genetic history of early European farmers

Abstract

Ancient DNA studies have established that Neolithic European populations were descended from Anatolian migrants1,2,3,4,5,6,7,8 who received a limited amount of admixture from resident hunter-gatherers3,4,5,9. Many open questions remain, however, about the spatial and temporal dynamics of population interactions and admixture during the Neolithic period. Here we investigate the population dynamics of Neolithization across Europe using a high-resolution genome-wide ancient DNA dataset with a total of 180 samples, of which 130 are newly reported here, from the Neolithic and Chalcolithic periods of Hungary (6000–2900 bc, n = 100), Germany (5500–3000 bc, n = 42) and Spain (5500–2200 bc, n = 38). We find that genetic diversity was shaped predominantly by local processes, with varied sources and proportions of hunter-gatherer ancestry among the three regions and through time. Admixture between groups with different ancestry profiles was pervasive and resulted in observable population transformation across almost all cultural transitions. Our results shed new light on the ways in which gene flow reshaped European populations throughout the Neolithic period and demonstrate the potential of time-series-based sampling and modelling approaches to elucidate multiple dimensions of historical population interactions.

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Figure 1: Spatial and temporal contexts of European Neolithic samples.
Figure 2: Admixture parameters for test individuals and populations.
Figure 3: Hungary time series and simulated data.

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Acknowledgements

We thank I. Lazaridis, P.-R. Loh, I. Mathieson, I. Olalde, E. Palkopoulou, N. Patterson and P. Skoglund for helpful comments and suggestions; J. Krause for providing the Stuttgart sample for which we generated a new library in this study; A. Whittle and A. Bayliss from The Times of Their Lives project for providing the radiocarbon date for sample VEJ5a; and B. Havasi (Balaton Museum), G. V. Székely (Katona József Museum), C. Farkas (Dobó István Museum), B. Nagy (Herman Ottó Museum), I. Pap, A. Kustár, T. Hajdu (Hungarian Natural History Museum), J. Ódor (Wosinsky Mór Museum), E. Nagy (Janus Pannonius Museum), P. Rácz (King St Stephen Museum), L. Szathmáry (Debrecen University), N. Kalicz, V. Voicsek, O. Vajda-Kiss, V. Majerik and I. Ko˝vári for assistance with samples. This work was supported by the Australian Research Council (grant DP130102158 to B.L. and W.H.), Hungarian National Research, Development and Innovation Office (K 119540 to B.M.), German Research Foundation (Al 287/7-1, 10-1 and 14-1 to K.W.A.), FEDER and Ministry of Economy and Competitiveness of Spain (BFU2015-64699-P to C.L.-F.), National Science Foundation (HOMINID grant BCS-1032255 to D.R.), National Institutes of Health (NIGMS grant GM100233 to D.R.), and Howard Hughes Medical Institute (D.R.).

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Authors and Affiliations

Authors

Contributions

A.S.-N., J.B., E.B., K.W.A., C.L.-F., W.H. and D.R. designed and supervised the study. B.G.M., K.K., K.O., M.B., T.M., A.O., J.J., T.P., F.H., P.C., J.K., K.Se., A.A., P.R., J.R., J.P.B., S.F., G.S., Z.T., E.G.N., J.D., E.M., G.P., L.M., B.M., Z.B., L.D., J.F.-E., J.A.M.-A., C.A.F., J.J.E., R.B., J.Or., K.Sc., H.M., A.C., J.B., E.B., K.W.A., C.L.-F. and W.H. provided samples and assembled archaeological and anthropological information. A.S.-N., A.P., B.S., V.K., N.R., K.St., M.F., M.M., J.Op., N.B., E.H., S.N. and B.L. performed laboratory work. M.L., A.S.-N., S.M. and D.R. analysed genetic data. M.L., A.S.-N. and D.R. wrote the manuscript with input from all coauthors.

Corresponding authors

Correspondence to Mark Lipson, Anna Szécsényi-Nagy or David Reich.

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Reviewer Information Nature thanks P. Bellwood and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 First two principal components from the PCA.

We computed the principal components (PCs) for a set of 782 present-day western Eurasian individuals genotyped on the Affymetrix Human Origins array (background grey points) and then projected ancient individuals onto these axes. A close-up omitting the present-day Bedouin population is shown.

Extended Data Figure 2 Scaffold admixture graph used for modelling the European Neolithic populations.

Dotted lines denote admixture events. Neolithic Anatolians, LB1 and KO1 are modelled as admixed, with basal Eurasian ancestry, deeper European hunter-gatherer ancestry and FEF ancestry, respectively. European test populations were fitted as a mixture of FEF and ancestry related to one or two of the four WHG individuals (here VIL-related as an example). See Supplementary Information section 6 for details.

Extended Data Figure 3 Examples of ALDER weighted linkage disequilibrium decay curves.

Weighted linkage disequilibrium (LD) curves are shown as a function of genetic distance d, using Neolithic Anatolians and WHG as references, for four individuals: BAM17b (Starčevo Early Neolithic), CB13 (Iberia Early Neolithic), Bla8 (Blätterhöhle hunter-gatherer) and KO1. The results shown here use helper individuals M11-363 (Neolithic Anatolian), L11-322 (Neolithic Anatolian), BIC and LB1, respectively, and have fitted dates (blue curves) of 3.8 ± 1.2, 18.3 ± 6.0, 13.1 ± 2.7 and 21.6 ± 8.8 generations (compared to final individual-level dates of 4.5 ± 1.9, 17.5 ± 3.5, 12.1 ± 2.9 and 21.0 ± 7.0 generations; see Supplementary Information section 7). Note that the x-axis scales are different for the four plots.

Extended Data Figure 4 Hunter-gatherer ancestry as a function of latitude and longitude for Neolithic individuals.

a, b, Early and Middle Neolithic Hungary. c, d, Late Neolithic and Chalcolithic Hungary. e, f, Iberia. HG, hunter-gatherer; Protob., Protoboleráz.

Extended Data Figure 5 Germany and Iberia time series and simulated data.

a, Dates of admixture. b, Hunter-gatherer ancestry proportions, normalized to the total of the most recent (rightmost) population. Symbols are as in Figs 1, 2 and indicate population-level mean ± 2 s.e.m. Yellow dashed lines represent continuous admixture simulations: from top to bottom, diminishing 5% per generation, diminishing 3%, diminishing 1% and uniform. Green solid lines represent pulse-plus-continuous admixture simulations: from top to bottom, all hunter-gatherer ancestry in a pulse at time zero; three-quarters of final hunter-gatherer ancestry in an initial pulse followed by uniform continuous gene flow; half in initial pulse and half continuous; and one-quarter in initial pulse.

Extended Data Table 1 Information for the Neolithic individuals from Hungary
Extended Data Table 2 Information for the Neolithic individuals from Germany and Spain
Extended Data Table 3 Admixture graph results for Neolithic populations
Extended Data Table 4 Mean dates of admixture for Neolithic populations

Supplementary information

Life Sciences Reporting Summary (PDF 67 kb)

Supplementary Information

This file contains Supplementary Notes 1-9. (PDF 3722 kb)

Supplementary Table 1

This file contains detailed sample information. (XLSX 92 kb)

Supplementary Table 2

This file contains detailed mitochondrial genome results. (XLSX 59 kb)

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Lipson, M., Szécsényi-Nagy, A., Mallick, S. et al. Parallel palaeogenomic transects reveal complex genetic history of early European farmers. Nature 551, 368–372 (2017). https://doi.org/10.1038/nature24476

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