Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Ancient genomes indicate population replacement in Early Neolithic Britain

Nature Ecology & Evolution volume 3, pages 765–771 (2019)Cite this article

Subjects

An Author Correction to this article was published on 08 May 2019

This article has been updated

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.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Map of sample locations.
Fig. 2: Principal component analysis of modern and ancient West Eurasians.
Fig. 3: WHG and ANF ancestry components of British and Central European Neolithic populations.
Fig. 4: Affinities of British and continental Neolithic populations.
Fig. 5: Patterns of haplotype sharing across high-coverage aDNA samples.

Similar content being viewed by others

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.

Change history

  • 08 May 2019

    In the version of this Article originally published, there were errors in the colour ordering of the legend in Fig. 5b, and in the positions of the target and surrogate populations in Fig. 5c. This has now been corrected. The conclusions of the study are in no way affected. The errors have been corrected in the HTML and PDF versions of the article.

References

  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).

    Article  Google Scholar 

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

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

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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. 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).

    Article  CAS  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

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.

Authors and 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

Authors
  1. Selina Brace
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoan Diekmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas J. Booth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lucy van Dorp
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zuzana Faltyskova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nadin Rohland
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Swapan Mallick
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Iñigo Olalde
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Matthew Ferry
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Megan Michel
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jonas Oppenheimer
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Nasreen Broomandkhoshbacht
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Kristin Stewardson
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Rui Martiniano
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Susan Walsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Manfred Kayser
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Sophy Charlton
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Garrett Hellenthal
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Ian Armit
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Rick Schulting
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Oliver E. Craig
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Alison Sheridan
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Mike Parker Pearson
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Chris Stringer
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. David Reich
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Mark G. Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. Ian Barnes
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding authors

Correspondence to Mark G. Thomas or Ian Barnes.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Supplementary Information

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

Reporting Summary

Supplementary Data 1

Summary of sequencing data per individual with relevant metadata

Supplementary Data 2

Functional variation

Supplementary Data 3

Admixture dates

Supplementary Data 4

Pairwise comparison of WHG admixture proportions

Supplementary Data 5

Y-chromosomal lineages

Supplementary Data 6

New radiocarbon dates and stable isotopes

Supplementary Data 7

Chronological model outputs

Supplementary Data 8

SOURCEFIND inferred proportions of ancient ancestry

Supplementary Data 9

SOURCEFIND inferred proportions of modern ancestry

Supplementary Data 10

qpGraph outliers

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brace, S., Diekmann, Y., Booth, T.J. et al. Ancient genomes indicate population replacement in Early Neolithic Britain. Nat Ecol Evol 3, 765–771 (2019). https://doi.org/10.1038/s41559-019-0871-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing