Ancient genomes indicate population replacement in Early Neolithic Britain.


Journal

Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577

Informations de publication

Date de publication:
05 2019
Historique:
received: 17 12 2018
accepted: 06 03 2019
pubmed: 17 4 2019
medline: 12 10 2019
entrez: 17 4 2019
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 30988490
doi: 10.1038/s41559-019-0871-9
pii: 10.1038/s41559-019-0871-9
pmc: PMC6520225
mid: EMS82120
doi:

Substances chimiques

DNA, Ancient 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

765-771

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 100713
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R01 GM100233
Pays : United States

Commentaires et corrections

Type : ErratumIn

Références

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).
doi: 10.1016/j.jas.2009.11.016
Sheridan, J. A. in Landscapes in Transition (eds Finlayson, B. & Warren, G.) 89–105 (Oxbow, 2010).
Thomas, J The Birth of Neolithic Britain: an Interpretive Account (Oxford University Press: 2013. .
Skoglund, P. et al. Genomic diversity and admixture differs for Stone Age Scandinavian foragers and farmers. Science 344, 747–750 (2014).
doi: 10.1126/science.1253448
Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).
doi: 10.1038/ncomms6257
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).
doi: 10.1073/pnas.1518445113
Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015).
doi: 10.1038/nature14317
Broushaki, F. et al. Early Neolithic genomes from the eastern Fertile Crescent. Science 353, 499–503 (2016).
doi: 10.1126/science.aaf7943
Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886–6891 (2016).
doi: 10.1073/pnas.1523951113
Lazaridis, I. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419–424 (2016).
doi: 10.1038/nature19310
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).
pubmed: 26337550 pmcid: 4652622
Olalde, I. et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Nature 555, 190–196 (2018).
doi: 10.1038/nature25738
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).
doi: 10.1016/j.cub.2017.05.023
Lipson, M. et al. Parallel palaeogenomic transects reveal complex genetic history of early European farmers. Nature 551, 368–372 (2017).
doi: 10.1038/nature24476
Mathieson, I. et al. The genomic history of southeastern Europe. Nature 555, 197–203 (2018).
doi: 10.1038/nature25778
Günther, T. et al. Genomics of Mesolithic Scandinavia reveal colonization routes and high-latitude adaptation. PLoS Biol. 16, e2003703 (2018).
doi: 10.1371/journal.pbio.2003703
Fu, Q. et al. The genetic history of Ice Age Europe. Nature 534, 200–205 (2016).
doi: 10.1038/nature17993
Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014).
doi: 10.1038/nature12960
Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015).
doi: 10.1038/nature16152
Kılınç, G. M. et al. The demographic development of the first farmers in Anatolia. Curr. Biol. 26, 2659–2666 (2016).
doi: 10.1016/j.cub.2016.07.057
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).
doi: 10.1016/j.cub.2016.12.060
Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014).
doi: 10.1038/nature13673
Mallick, S. et al. The Simons Genome Diversity Project: 300 genomes from 142 diverse populations. Nature 538, 201–206 (2016).
doi: 10.1038/nature18964
Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).
doi: 10.1534/genetics.112.145037
Lawson, D. J. et al. Inference of population structure using dense haplotype data. PLoS Genet. 8, e1002453 (2012).
doi: 10.1371/journal.pgen.1002453
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).
doi: 10.1038/s41467-018-07748-z
Loh, P.-R. et al. Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193, 1233–1254 (2013).
doi: 10.1534/genetics.112.147330
Bronk Ramsey, C. Bayesian analysis of radiocarbon dates. Radiocarbon 51, 337–360 (2009).
doi: 10.1017/S0033822200033865
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).
doi: 10.1016/j.fsigen.2018.04.004
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).
Scarre, C. The early Neolithic of western France and Megalithic origins in Atlantic Europe. Oxford J. Archaeol. 11, 121–154 (1992).
doi: 10.1111/j.1468-0092.1992.tb00261.x
Bollongino, R. et al. 2000 years of parallel societies in Stone Age Central Europe. Science 342, 479–481 (2013).
doi: 10.1126/science.1245049
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).
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).
doi: 10.1016/j.jas.2016.07.014
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).
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).
doi: 10.1073/pnas.1314445110
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).
doi: 10.1098/rstb.2013.0624
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).
doi: 10.1101/pdb.prot5448
Kircher, M., Sawyer, S. & Meyer, M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3 (2011).
doi: 10.1093/nar/gkr771
Schubert, M., Lindgreen, S. & Orlando, L. Adapter Removal v2: rapid adapter trimming, identification, and read merging. BMC Res. Notes 9, 88 (2016).
doi: 10.1186/s13104-016-1900-2
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
doi: 10.1093/bioinformatics/btp324
Mckenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
doi: 10.1101/gr.107524.110
Link, V. et al. ATLAS: analysis tools for low-depth and ancient samples. Preprint at Biorxiv https://doi.org/10.1101/105346 (2017).
Fu, Q. et al. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr. Biol. 23, 553–559 (2013).
doi: 10.1016/j.cub.2013.02.044
Navarro-Gomez, D. et al. Phy-Mer: a novel alignment-free and reference-independent mitochondrial haplogroup classifier. Bioinformatics 31, 1310–1312 (2014).
doi: 10.1093/bioinformatics/btu825
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).
doi: 10.1093/molbev/msy032
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).
doi: 10.1016/j.ajhg.2015.04.018
Hellenthal, G. et al. A genetic atlas of human admixture history. Science 343, 747–751 (2014).
doi: 10.1126/science.1243518
Busby, G. B. et al. The role of recent admixture in forming the contemporary West Eurasian genomic landscape. Curr. Biol. 25, 2518–2526 (2015).
doi: 10.1016/j.cub.2015.08.007
Leslie, S. et al. The fine-scale genetic structure of the British population. Nature 519, 309 (2015).
doi: 10.1038/nature14230
Delaneau, O. et al. A linear complexity phasing method for thousands of genomes. Nat. Methods 9, 179–181 (2012).
doi: 10.1038/nmeth.1785

Auteurs

Selina Brace (S)

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

Yoan Diekmann (Y)

Research Department of Genetics, Evolution and Environment, University College London, London, UK.

Thomas J Booth (TJ)

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

Lucy van Dorp (L)

UCL Genetics Institute, University College London, London, UK.

Zuzana Faltyskova (Z)

Research Department of Genetics, Evolution and Environment, University College London, London, UK.

Nadin Rohland (N)

Department of Genetics, Harvard Medical School, Boston, MA, USA.

Swapan Mallick (S)

UCL Genetics Institute, University College London, London, UK.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

Iñigo Olalde (I)

Department of Genetics, Harvard Medical School, Boston, MA, USA.

Matthew Ferry (M)

Department of Genetics, Harvard Medical School, Boston, MA, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

Megan Michel (M)

Department of Genetics, Harvard Medical School, Boston, MA, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

Jonas Oppenheimer (J)

Department of Genetics, Harvard Medical School, Boston, MA, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

Nasreen Broomandkhoshbacht (N)

Department of Genetics, Harvard Medical School, Boston, MA, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

Kristin Stewardson (K)

Department of Genetics, Harvard Medical School, Boston, MA, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

Rui Martiniano (R)

Department of Genetics, University of Cambridge, Cambridge, UK.

Susan Walsh (S)

Department of Biology, Indiana University-Purdue University Indianapolis, Indianapolis, IN, USA.

Manfred Kayser (M)

Department of Genetic Identification, Erasmus University Medical Centre Rotterdam, Rotterdam, the Netherlands.

Sophy Charlton (S)

Department of Earth Sciences, Natural History Museum, London, UK.
Bioarch, University of York, York, UK.

Garrett Hellenthal (G)

UCL Genetics Institute, University College London, London, UK.

Ian Armit (I)

School of Archaeological and Forensic Sciences, University of Bradford, Bradford, UK.

Rick Schulting (R)

Institute of Archaeology, University of Oxford, Oxford, UK.

Oliver E Craig (OE)

Bioarch, University of York, York, UK.

Alison Sheridan (A)

National Museums Scotland, Edinburgh, UK.

Mike Parker Pearson (M)

Institute of Archaeology, University College London, London, UK.

Chris Stringer (C)

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

David Reich (D)

Department of Genetics, Harvard Medical School, Boston, MA, USA.
Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.

Mark G Thomas (MG)

Research Department of Genetics, Evolution and Environment, University College London, London, UK. m.thomas@ucl.ac.uk.
UCL Genetics Institute, University College London, London, UK. m.thomas@ucl.ac.uk.

Ian Barnes (I)

Department of Earth Sciences, Natural History Museum, London, UK. I.Barnes@nhm.ac.uk.

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