Abstract

The roles of migration, admixture and acculturation in the European transition to farming have been debated for over 100 years. Genome-wide ancient DNA studies indicate predominantly Aegean ancestry for continental Neolithic farmers, but also variable admixture with local Mesolithic hunter-gatherers. Neolithic cultures first appear in Britain circa 4000 bc, a millennium after they appeared in adjacent areas of continental Europe. The pattern and process of this delayed British Neolithic transition remain unclear. We assembled genome-wide data from 6 Mesolithic and 67 Neolithic individuals found in Britain, dating 8500–2500 bc. Our analyses reveal persistent genetic affinities between Mesolithic British and Western European hunter-gatherers. We find overwhelming support for agriculture being introduced to Britain by incoming continental farmers, with small, geographically structured levels of hunter-gatherer ancestry. Unlike other European Neolithic populations, we detect no resurgence of hunter-gatherer ancestry at any time during the Neolithic in Britain. Genetic affinities with Iberian Neolithic individuals indicate that British Neolithic people were mostly descended from Aegean farmers who followed the Mediterranean route of dispersal. We also infer considerable variation in pigmentation levels in Europe by circa 6000 bc.

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Data availability

BAM files (one file per library, before realigning around InDels; see Supplementary Table 1) have been deposited at the European Nucleotide Archive under study accession PRJEB31249.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  1. 1.

    Collard, M., Edinborough, K., Shennan, S. & Thomas, M. G. Radiocarbon evidence indicates that migrants introduced farming to Britain. J. Arch. Sci. 37, 866–870 (2010).

  2. 2.

    Sheridan, J. A. in Landscapes in Transition (eds Finlayson, B. & Warren, G.) 89–105 (Oxbow, 2010).

  3. 3.

    Thomas, J The Birth of Neolithic Britain: an Interpretive Account (Oxford University Press: 2013. .

  4. 4.

    Skoglund, P. et al. Genomic diversity and admixture differs for Stone Age Scandinavian foragers and farmers. Science 344, 747–750 (2014).

  5. 5.

    Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).

  6. 6.

    Cassidy, L. M. et al. Neolithic and Bronze Age migration to Ireland and establishment of the insular Atlantic genome. Proc. Natl Acad. Sci. USA 113, 368–373 (2015).

  7. 7.

    Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015).

  8. 8.

    Broushaki, F. et al. Early Neolithic genomes from the eastern Fertile Crescent. Science 353, 499–503 (2016).

  9. 9.

    Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886–6891 (2016).

  10. 10.

    Lazaridis, I. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419–424 (2016).

  11. 11.

    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).

  12. 12.

    Olalde, I. et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Nature 555, 190–196 (2018).

  13. 13.

    González-Fortes, G. et al. Paleogenomic evidence for multi-generational mixing between Neolithic farmers and mesolithic hunter-gatherers in the lower Danube basin. Curr. Biol. 27, 1801–1810 (2017).

  14. 14.

    Lipson, M. et al. Parallel palaeogenomic transects reveal complex genetic history of early European farmers. Nature 551, 368–372 (2017).

  15. 15.

    Mathieson, I. et al. The genomic history of southeastern Europe. Nature 555, 197–203 (2018).

  16. 16.

    Günther, T. et al. Genomics of Mesolithic Scandinavia reveal colonization routes and high-latitude adaptation. PLoS Biol. 16, e2003703 (2018).

  17. 17.

    Fu, Q. et al. The genetic history of Ice Age Europe. Nature 534, 200–205 (2016).

  18. 18.

    Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014).

  19. 19.

    Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015).

  20. 20.

    Kılınç, G. M. et al. The demographic development of the first farmers in Anatolia. Curr. Biol. 26, 2659–2666 (2016).

  21. 21.

    Jones, E. R. et al. The Neolithic transition in the Baltic was not driven by admixture with early European farmers. Curr. Biol. 27, 576–582 (2017).

  22. 22.

    Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014).

  23. 23.

    Mallick, S. et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538, 201–206 (2016).

  24. 24.

    Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).

  25. 25.

    Lawson, D. J. et al. Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012).

  26. 26.

    Chacon-Duque, J. C. et al. Latin Americans show wide-spread Converso ancestry and the imprint of local Native ancestry on physical appearance. Nat. Commun. 9, 5388 (2018).

  27. 27.

    Loh, P.-R. et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193, 1233–1254 (2013).

  28. 28.

    Bronk Ramsey, C. Bayesian analysis of radiocarbon dates. Radiocarbon 51, 337–360 (2009).

  29. 29.

    Chaitanya, L. et al. The HIrisPlex-S system for eye, hair and skin colour prediction from DNA: introduction and forensic developmental validation. Forensic Sci. Int. Genet 35, 123–135 (2018).

  30. 30.

    Whittle, A. W. R, Healy, F, Bayliss, A. & Allen, M. J. Gathering Time: Dating the Early Neolithic Enclosures of Southern Britain and Ireland. (Oxbow Books, 2011).

  31. 31.

    Scarre, C. The early Neolithic of western France and Megalithic origins in Atlantic Europe. Oxford J. Archaeol. 11, 121–154 (1992).

  32. 32.

    Bollongino, R. et al. 2000 years of parallel societies in Stone Age Central Europe. Science 342, 479–481 (2013).

  33. 33.

    Fraser, M. et al. New insights on cultural dualism and population structure in the Middle Neolithic Funnel Beaker culture on the island of Gotland. Sci. Rep. 17, 325–334 (2018).

  34. 34.

    Charlton, S. et al. Finding Britain’s last hunter-gatherers: a new biomolecular approach to ‘unidentifiable’ bone fragments utilising bone collagen. J. Archaeol. Sci. 73, 55–61 (2016).

  35. 35.

    Schulting, R. J. and Borić, D. in Neolithic Europe: Essays in Honour of Professor Alasdair Whittle (eds P. Bickle, V. Cummings, D. Hofmann & J. Pollard) 82–104 (Oxford, 2017).

  36. 36.

    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).

  37. 37.

    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, 20130624–20130624 (2014).

  38. 38.

    Meyer, M. & Kircher, M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. https://doi.org/10.1101/pdb.prot5448 (2010).

  39. 39.

    Kircher, M., Sawyer, S. & Meyer, M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3 (2011).

  40. 40.

    Schubert, M., Lindgreen, S. & Orlando, L. Adapter Removal v2: rapid adapter trimming, identification, and read merging. BMC Res. Notes 9, 88 (2016).

  41. 41.

    Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

  42. 42.

    Mckenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

  43. 43.

    Link, V. et al. ATLAS: analysis tools for low-depth and ancient samples. Preprint at Biorxiv https://doi.org/10.1101/105346 (2017).

  44. 44.

    Fu, Q. et al. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr. Biol. 23, 553–559 (2013).

  45. 45.

    Navarro-Gomez, D. et al. Phy-Mer: a novel alignment-free and reference-independent mitochondrial haplogroup classifier. Bioinformatics 31, 1310–1312 (2014).

  46. 46.

    Ralf, A., Montiel González, D., Zhong, K. & Kayser, M. Yleaf: software for human Y-chromosomal haplogroup inference from next generation sequencing data. Mol. Biol. Evol. 35, 1291–1294 (2018).

  47. 47.

    Wang, C., Zhan, X., Liang, L., Abecasis, G. R. & Lin, X. Improved ancestry estimation for both genotyping and sequencing data using projection procrustes analysis and genotype imputation. Am. J. Hum. Genet. 96, 926–937 (2015).

  48. 48.

    Hellenthal, G. et al. A genetic atlas of human admixture history. Science 343, 747–751 (2014).

  49. 49.

    Busby, G. B. et al. The role of recent admixture in forming the contemporary West Eurasian genomic landscape. Curr. Biol. 25, 2518–2526 (2015).

  50. 50.

    Leslie, S. et al. The fine-scale genetic structure of the British population. Nature 519, 309 (2015).

  51. 51.

    Delaneau, O. et al. A linear complexity phasing method for thousands of genomes. Nat. Methods 9, 179–181 (2012).

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Acknowledgements

The authors would like to thank the Longleat Estate, T. Lord at Lower Winskill Farm, B. Chandler at Torquay Museum, A. Chamberlain at the University of Manchester, L. Wilson and G. Mullan at the University of Bristol Spelaeological Society, E. Walker, A. Gwilt and J. Deacon at the National Museum of Wales, A. Maxted at Brighton Museum, M. Lahr at the Duckworth Laboratory, B. Lane at Wells Museum, M. Smith at Bournemouth University, D. Rice at the Museum of Gloucester and R. Kruszynski at the Natural History Museum for providing access to samples. In addition, Y.D. wishes to thank J. Blöcher, A. Scheu, C. Sell and J. Burger for discussions on the bioinformatic pipeline, and V. Link for help with ATLAS. M.G.T. and I.B. were supported by a Wellcome Trust Investigator Award (project No. 100713/Z/12/Z). S.C. was supported by the Natural Environment Research Council (NE/K500987/1). L.v.D acknowledges financial support from the Newton Trust (grant No. MR/P007597/1). R.M. was supported by an EMBO Long-Term Fellowship (No. ALTF 133-2017). D.R. was supported by a NIH grant (No. GM100233), by NSF HOMINID (No. BCS-1032255) and by an Allen Discovery Center of the Paul Allen Foundation, and is a Howard Hughes Medical Institute investigator. C.S. is supported by the Calleva Foundation and the Human Origins Research Fund. S.W. was supported by the US National Institute of Justice (grant No. 2014-DN-BX-K031).

Author information

Author notes

  1. These authors contributed equally: Selina Brace, Yoan Diekmann, Thomas J. Booth.

  2. These authors jointly supervised this work: David Reich, Mark G. Thomas, Ian Barnes.

Affiliations

  1. Department of Earth Sciences, Natural History Museum, London, UK

    • Selina Brace
    • , Thomas J. Booth
    • , Sophy Charlton
    • , Chris Stringer
    •  & Ian Barnes
  2. Research Department of Genetics, Evolution and Environment, University College London, London, UK

    • Yoan Diekmann
    • , Zuzana Faltyskova
    •  & Mark G. Thomas
  3. UCL Genetics Institute, University College London, London, UK

    • Lucy van Dorp
    • , Swapan Mallick
    • , Garrett Hellenthal
    •  & Mark G. Thomas
  4. Department of Genetics, Harvard Medical School, Boston, MA, USA

    • Nadin Rohland
    • , Iñigo Olalde
    • , Matthew Ferry
    • , Megan Michel
    • , Jonas Oppenheimer
    • , Nasreen Broomandkhoshbacht
    • , Kristin Stewardson
    •  & David Reich
  5. Broad Institute of MIT and Harvard, Cambridge, MA, USA

    • Swapan Mallick
    •  & David Reich
  6. Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA

    • Swapan Mallick
    • , Matthew Ferry
    • , Megan Michel
    • , Jonas Oppenheimer
    • , Nasreen Broomandkhoshbacht
    • , Kristin Stewardson
    •  & David Reich
  7. Department of Genetics, University of Cambridge, Cambridge, UK

    • Rui Martiniano
  8. Department of Biology, Indiana University-Purdue University Indianapolis, Indianapolis, IN, USA

    • Susan Walsh
  9. Department of Genetic Identification, Erasmus University Medical Centre Rotterdam, Rotterdam, the Netherlands

    • Manfred Kayser
  10. Bioarch, University of York, York, UK

    • Sophy Charlton
    •  & Oliver E. Craig
  11. School of Archaeological and Forensic Sciences, University of Bradford, Bradford, UK

    • Ian Armit
  12. Institute of Archaeology, University of Oxford, Oxford, UK

    • Rick Schulting
  13. National Museums Scotland, Edinburgh, UK

    • Alison Sheridan
  14. Institute of Archaeology, University College London, London, UK

    • Mike Parker Pearson

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Contributions

I.B. and M.G.T. conceived the project. Y.D., S.B., Z.F., O.C. and T.B. contributed to the project design. S.B., Y.D., T.B., L.v.D, N.R., S.M., I.O., M.F., M.M., J.O., N.B., K.S., R.M., S.C. and S.W. generated and analysed data. I.B., M.G.T., Y.D., S.B., T.B., M.K., S.W., G.H., I.A., R.S., O.C., A.S., M.P.P., C.S. and D.R. contributed to the sampling strategy and the interpretation of results. I.B., M.G.T., Y.D., S.B. and T.B. wrote the paper, with contributions from all other authors.

Competing interests

The authors declare no competing interests.

Corresponding authors

Correspondence to Mark G. Thomas or Ian Barnes.

Supplementary information

  1. Supplementary Information

    Supplementary Notes 1–7 and Supplementary Figs. 1–23

  2. Reporting Summary

  3. Supplementary Data 1

    Summary of sequencing data per individual with relevant metadata

  4. Supplementary Data 2

    Functional variation

  5. Supplementary Data 3

    Admixture dates

  6. Supplementary Data 4

    Pairwise comparison of WHG admixture proportions

  7. Supplementary Data 5

    Y-chromosomal lineages

  8. Supplementary Data 6

    New radiocarbon dates and stable isotopes

  9. Supplementary Data 7

    Chronological model outputs

  10. Supplementary Data 8

    SOURCEFIND inferred proportions of ancient ancestry

  11. Supplementary Data 9

    SOURCEFIND inferred proportions of modern ancestry

  12. Supplementary Data 10

    qpGraph outliers

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DOI

https://doi.org/10.1038/s41559-019-0871-9