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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References
Bramanti, B. et al. Genetic discontinuity between local hunter-gatherers and central Europe’s first farmers. Science 326, 137–140 (2009)
Haak, W. et al. Ancient DNA from European Early Neolithic farmers reveals their Near Eastern affinities. PLoS Biol. 8, e1000536 (2010)
Skoglund, P. et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336, 466–469 (2012)
Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014)
Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015)
Günther, T. et al. Ancient genomes link early farmers from Atapuerca in Spain to modern-day Basques. Proc. Natl Acad. Sci. USA 112, 11917–11922 (2015)
Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015)
Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886–6891 (2016)
Brandt, G. et al. Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342, 257–261 (2013)
Ammerman, A. J. & Cavalli-Sforza, L. L. The Neolithic Transition and the Genetics of Populations in Europe (Princeton, 1984)
Price, T. D. (ed.) in Europe’s First Farmers 301–318 (Cambridge, 2000)
Zvelebil, M. The agricultural transition and the origins of Neolithic society in Europe. Documenta Praehistorica 28, 1–26 (2001)
Richards, M. The Neolithic invasion of Europe. Annu. Rev. Anthropol. 32, 135–162 (2003)
Tringham, R. in Europe’s First Farmers (ed. Price, T. D. ) 19–56 (Cambridge, 2000)
Bollongino, R. et al. 2000 years of parallel societies in Stone Age central Europe. Science 342, 479–481 (2013)
Skoglund, P. et al. Genomic diversity and admixture differs for Stone-Age Scandinavian foragers and farmers. Science 344, 747–750 (2014)
Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014)
Olalde, I. et al. A common genetic origin for early farmers from Mediterranean Cardial and central European LBK cultures. Mol. Biol. Evol. 32, 3132–3142 (2015)
Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014)
Fu, Q. et al. The genetic history of Ice Age Europe. Nature 534, 200–205 (2016)
Seguin-Orlando, A. et al. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113–1118 (2014)
Loh, P.-R. et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193, 1233–1254 (2013)
Bánffy, E. Eastern, central and western Hungary — variations of Neolithisation models. Documenta Praehistorica 33, 125–142 (2006)
Domboróczki, L., Kaczanowska, M. & Kozłowski, J. The Neolithic settlement at Tiszaszo˝lo˝s-Domaháza-puszta and the question of the northern spread of the Körös Culture. Atti Soc. Preist. Protost. Friuli-VG 17, 101–155 (2010)
Szécsényi-Nagy, A . et al. Tracing the genetic origin of Europe’s first farmers reveals insights into their social organization. Proc. R. Soc. Lond. B 282, 20150339 (2015)
Raczky, P. in The Copper Age Cemetery of Budakalász (eds Bondár, M. & Raczky, P. ) 475–485 (Pytheas, 2009)
Martins, H. et al. Radiocarbon dating the beginning of the Neolithic in Iberia: new results, new problems. J. Medit. Arch. 28, 105–131 (2015)
Jakucs, J. et al. Between the Vincˇa and Linearbandkeramik worlds: the diversity of practices and identities in the 54th–53rd centuries cal BC in southwest Hungary and beyond. J. World Prehist. 29, 267–336 (2016)
Oross, K. et al. Midlife changes: the Sopot burial ground at Alsónyék. Bericht der Römisch-Germanischen Kommission 94, 151–178 (2016)
Jones, E. R. et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat. Commun. 6, 8912 (2015)
Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl Acad. Sci. USA 110, 15758–15763 (2013)
Korlevic´, P. et al. Reducing microbial and human contamination in DNA extractions from ancient bones and teeth. Biotechniques 59, 87–93 (2015)
Lazaridis, I. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419–424 (2016)
Rohland, N., Harney, E., Mallick, S., Nordenfelt, S. & Reich, D. Partial uracil–DNA–glycosylase treatment for screening of ancient DNA. Phil. Trans. R. Soc. Lond. B 370, 20130624 (2015)
DeAngelis, M. M., Wang, D. G. & Hawkins, T. L. Solid-phase reversible immobilization for the isolation of PCR products. Nucleic Acids Res. 23, 4742–4743 (1995)
Rohland, N. & Reich, D. Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res. 22, 939–946 (2012)
Meyer, M. et al. A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505, 403–406 (2014)
Sawyer, S., Krause, J., Guschanski, K., Savolainen, V. & Pääbo, S. Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS ONE 7, e34131 (2012)
Andrews, R. M. et al. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 23, 147 (1999)
Behar, D. M. et al. A “Copernican” reassessment of the human mitochondrial DNA tree from its root. Am. J. Hum. Genet. 90, 675–684 (2012)
Mallick, S. et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538, 201–206 (2016)
Fu, Q. et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl Acad. Sci. USA 110, 2223–2227 (2013)
Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics 15, 356 (2014)
Domboróczki, L. in The First Neolithic Sites in Central/South-East European Transect. Volume III: The Körös Culture in Eastern Hungary (eds Anders, A. & Siklósi, Z. ) 107–111 (Oxford, 2012)
Oross, K. et al. The early days of Neolithic Alsónyék: the Starcˇevo occupation. Bericht der Römisch-Germanischen Kommission 94, 93–121 (2016)
Ramsey, C. B. & Lee, S. Recent and planned developments of the program OxCal. Radiocarbon 55, 720–730 (2013)
Reimer, P. J. et al. Intcal13 and marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 1869–1887 (2013)
Patterson, N., Price, A. L. & Reich, D. Population structure and eigenanalysis. PLoS Genet. 2, e190 (2006)
Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012)
Fenner, J. N. Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am. J. Phys. Anthropol. 128, 415–423 (2005)
Moorjani, P. et al. A genetic method for dating ancient genomes provides a direct estimate of human generation interval in the last 45,000 years. Proc. Natl Acad. Sci. USA 113, 5652–5657 (2016)
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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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.
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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.
Supplementary information
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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DOI: https://doi.org/10.1038/nature24476
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