100 ancient genomes show repeated population turnovers in Neolithic Denmark

Morten E Allentoft, Martin Sikora, Anders Fischer, Karl-Göran Sjögren, Andrés Ingason, Ruairidh Macleod, Anders Rosengren, Bettina Schulz Paulsson, Marie Louise Schjellerup Jørkov, Maria Novosolov, Jesper Stenderup, T Douglas Price, Morten Fischer Mortensen, Anne Birgitte Nielsen, Mikkel Ulfeldt Hede, Lasse Sørensen, Poul Otto Nielsen, Peter Rasmussen, Theis Zetner Trolle Jensen, Alba Refoyo-MartínezEvan K Irving-Pease, William Barrie, Alice Pearson, Bárbara Sousa da Mota, Fabrice Demeter, Rasmus A Henriksen, Tharsika Vimala, Hugh McColl, Andrew Vaughn, Lasse Vinner, Gabriel Renaud, Aaron Stern, Niels Nørkjær Johannsen, Abigail Daisy Ramsøe, Andrew Joseph Schork, Anthony Ruter, Anne Birgitte Gotfredsen, Bjarne Henning Nielsen, Erik Brinch Petersen, Esben Kannegaard, Jesper Hansen, Kristoffer Buck Pedersen, Lisbeth Pedersen, Lutz Klassen, Morten Meldgaard, Morten Johansen, Otto Christian Uldum, Per Lotz, Per Lysdahl, Pernille Bangsgaard, Peter Vang Petersen, Rikke Maring, Rune Iversen, Sidsel Wåhlin, Søren Anker Sørensen, Søren H Andersen, Thomas Jørgensen, Niels Lynnerup, Daniel J Lawson, Simon Rasmussen, Thorfinn Sand Korneliussen, Kurt H Kjær, Richard Durbin, Rasmus Nielsen, Olivier Delaneau, Thomas Werge, Kristian Kristiansen, Eske Willerslev

Research output: Contribution to journalArticle (Academic Journal)peer-review

14 Citations (Scopus)

Abstract

Major migration events in Holocene Eurasia have been characterized genetically at broad regional scales 1-4. However, insights into the population dynamics in the contact zones are hampered by a lack of ancient genomic data sampled at high spatiotemporal resolution 5-7. Here, to address this, we analysed shotgun-sequenced genomes from 100 skeletons spanning 7,300 years of the Mesolithic period, Neolithic period and Early Bronze Age in Denmark and integrated these with proxies for diet ( 13C and 15N content), mobility ( 87Sr/ 86Sr ratio) and vegetation cover (pollen). We observe that Danish Mesolithic individuals of the Maglemose, Kongemose and Ertebølle cultures form a distinct genetic cluster related to other Western European hunter-gatherers. Despite shifts in material culture they displayed genetic homogeneity from around 10,500 to 5,900 calibrated years before present, when Neolithic farmers with Anatolian-derived ancestry arrived. Although the Neolithic transition was delayed by more than a millennium relative to Central Europe, it was very abrupt and resulted in a population turnover with limited genetic contribution from local hunter-gatherers. The succeeding Neolithic population, associated with the Funnel Beaker culture, persisted for only about 1,000 years before immigrants with eastern Steppe-derived ancestry arrived. This second and equally rapid population replacement gave rise to the Single Grave culture with an ancestry profile more similar to present-day Danes. In our multiproxy dataset, these major demographic events are manifested as parallel shifts in genotype, phenotype, diet and land use.

Original languageEnglish
Pages (from-to)329-337
Number of pages9
JournalNature
Volume625
Issue number7994
DOIs
Publication statusPublished - 10 Jan 2024

Bibliographical note

Funding Information:
The Lundbeck Foundation GeoGenetics Centre is supported by grants from the Lundbeck Foundation (R302-2018-2155, R155-2013-16338), the Novo Nordisk Foundation (NNF18SA0035006), the Wellcome Trust (WT214300), Carlsberg Foundation (CF18-0024), the Danish National Research Foundation (DNRF94, DNRF174), the University of Copenhagen (KU2016 programme) and Ferring Pharmaceuticals A/S, to E.W. This research has been conducted using the UK Biobank Resource and the iPSYCH Initiative, funded by the Lundbeck Foundation (R102-A9118 and R155-2014-1724). This work was further supported by the Swedish Foundation for Humanities and Social Sciences grant (Riksbankens Jubileumsfond M16-0455:1) to K.K. M.E.A. was supported by Marie Skłodowska-Curie Actions of the EU (grant no. 300554), The Villum Foundation (grant no. 10120) and Independent Research Fund Denmark (grant no. 7027-00147B). A.F. was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy–EXC 2150–390870439. R. Macleod was supported by an SSHRC doctoral studentship grant (G101449: ‘Individual Life Histories in Long-Term Cultural Change’). B.S.P. has received funding from the European Union’s Horizon 2020 research and innovation programme under the ERC-StG grant agreement No 94924. M.N. is funded by the Human Frontier Science Program Postdoctoral Fellowship LT000143/2019-L4. A.R.-M. was supported by the Lundbeck Foundation (grant R302-2018-2155) and the Novo Nordisk Foundation (grant NNF18SA0035006); E.K.I.-P. was supported by the Lundbeck Foundation (grant R302-2018-2155) and the Novo Nordisk Foundation (grant NNF18SA0035006). W.B. is supported by the Hanne and Torkel Weis-Fogh Fund (Department of Zoology, University of Cambridge). A.P. is funded by Wellcome grant WT214300. B.S.d.M. and O.D. are supported by the Swiss National Science Foundation (SFNS PP00P3_176977) and European Research Council (ERC 679330). G.R. is supported by a Novo Nordisk Foundation Fellowship (gNNF20OC0062491). N.N.J. is supported by Aarhus University Research Foundation. A.J.S. is supported by a Lundbeckfonden Fellowship (R335-2019-2318) and the National Institute on Aging (NIH award numbers U19AG023122, U24AG051129 and UH2AG064706). R. Maring was funded by the Aarhus University Research Foundation through a grant awarded to M. A. Mannino for the project titled Danish and European Diets in Time (AUFF-E-2015-FLS-8-2). S.R. was funded by the Novo Nordisk Foundation (NNF14CC0001). T.S.K. is funded by Carlsberg grant CF19-0712. R.D. is funded by the Wellcome Trust (WT214300). R.N. is funded by the National Institute of General Medical Sciences (NIH grant R01GM138634). T.W. is supported by the Lundbeck Foundation iPSYCH initiative (R248-2017-2003). We are indebted to P. Bennike for her contribution during the formative years of the project until shortly before her death in 2017. We acknowledge staff at the National Museum, the Anthropological Laboratory, and the regional museums in Denmark, responsible for collecting, recording and curating prehistoric skeletal remains studied herein. The process of identifying and sampling suitable archaeological remains for the current study was dependent on numerous specialists in Danish archaeology including researchers, museum employees and citizen scientists. We thank the following in this regard (alphabetically ordered): A. H. Andersen, S. Bergerbrant, K. Christensen, K. M. Gregersen, V. Grimes, E. Johansen, O. T. Kastholm, T. Lotz, E. Lundberg, M. Mannino, J. Olsen, K. Rosenlund and H. H. Sørensen. We also acknowledge those who have assisted in the sampling process or the gathering of provenance data on prehistoric human remains which were not analysed here owing to insufficient DNA preservation. These include H. Dahl (Tybrind Vig), I. B. Enghoff (Østenkær), A. B. Gurlev (Vedbæk Havn), L. Holten (Aldersro), O. Lass (Hesselbjerg/Ferle Enge and Nivå), L. Matthes (Knudsgrund/Knudshoved) and K. Randsborg (deceased) (Nivå). We are grateful for contributions from F. Racimo, and express our gratitude to the many researchers who have supported laboratory work, analytical procedures and evaluation of results that are presented here, including M. Mannino, P. Reimer and M. Thompson. E.W. thanks St. John’s College, Cambridge, for providing a stimulating environment of discussion and learning.

Funding Information:
The Lundbeck Foundation GeoGenetics Centre is supported by grants from the Lundbeck Foundation (R302-2018-2155, R155-2013-16338), the Novo Nordisk Foundation (NNF18SA0035006), the Wellcome Trust (WT214300), Carlsberg Foundation (CF18-0024), the Danish National Research Foundation (DNRF94, DNRF174), the University of Copenhagen (KU2016 programme) and Ferring Pharmaceuticals A/S, to E.W. This research has been conducted using the UK Biobank Resource and the iPSYCH Initiative, funded by the Lundbeck Foundation (R102-A9118 and R155-2014-1724). This work was further supported by the Swedish Foundation for Humanities and Social Sciences grant (Riksbankens Jubileumsfond M16-0455:1) to K.K. M.E.A. was supported by Marie Skłodowska-Curie Actions of the EU (grant no. 300554), The Villum Foundation (grant no. 10120) and Independent Research Fund Denmark (grant no. 7027-00147B). A.F. was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany´s Excellence Strategy–EXC 2150–390870439. R. Macleod was supported by an SSHRC doctoral studentship grant (G101449: ‘Individual Life Histories in Long-Term Cultural Change’). B.S.P. has received funding from the European Union’s Horizon 2020 research and innovation programme under the ERC-StG grant agreement No 94924. M.N. is funded by the Human Frontier Science Program Postdoctoral Fellowship LT000143/2019-L4. A.R.-M. was supported by the Lundbeck Foundation (grant R302-2018-2155) and the Novo Nordisk Foundation (grant NNF18SA0035006); E.K.I.-P. was supported by the Lundbeck Foundation (grant R302-2018-2155) and the Novo Nordisk Foundation (grant NNF18SA0035006). W.B. is supported by the Hanne and Torkel Weis-Fogh Fund (Department of Zoology, University of Cambridge). A.P. is funded by Wellcome grant WT214300. B.S.d.M. and O.D. are supported by the Swiss National Science Foundation (SFNS PP00P3_176977) and European Research Council (ERC 679330). G.R. is supported by a Novo Nordisk Foundation Fellowship (gNNF20OC0062491). N.N.J. is supported by Aarhus University Research Foundation. A.J.S. is supported by a Lundbeckfonden Fellowship (R335-2019-2318) and the National Institute on Aging (NIH award numbers U19AG023122, U24AG051129 and UH2AG064706). R. Maring was funded by the Aarhus University Research Foundation through a grant awarded to M. A. Mannino for the project titled Danish and European Diets in Time (AUFF-E-2015-FLS-8-2). S.R. was funded by the Novo Nordisk Foundation (NNF14CC0001). T.S.K. is funded by Carlsberg grant CF19-0712. R.D. is funded by the Wellcome Trust (WT214300). R.N. is funded by the National Institute of General Medical Sciences (NIH grant R01GM138634). T.W. is supported by the Lundbeck Foundation iPSYCH initiative (R248-2017-2003). We are indebted to P. Bennike for her contribution during the formative years of the project until shortly before her death in 2017. We acknowledge staff at the National Museum, the Anthropological Laboratory, and the regional museums in Denmark, responsible for collecting, recording and curating prehistoric skeletal remains studied herein. The process of identifying and sampling suitable archaeological remains for the current study was dependent on numerous specialists in Danish archaeology including researchers, museum employees and citizen scientists. We thank the following in this regard (alphabetically ordered): A. H. Andersen, S. Bergerbrant, K. Christensen, K. M. Gregersen, V. Grimes, E. Johansen, O. T. Kastholm, T. Lotz, E. Lundberg, M. Mannino, J. Olsen, K. Rosenlund and H. H. Sørensen. We also acknowledge those who have assisted in the sampling process or the gathering of provenance data on prehistoric human remains which were not analysed here owing to insufficient DNA preservation. These include H. Dahl (Tybrind Vig), I. B. Enghoff (Østenkær), A. B. Gurlev (Vedbæk Havn), L. Holten (Aldersro), O. Lass (Hesselbjerg/Ferle Enge and Nivå), L. Matthes (Knudsgrund/Knudshoved) and K. Randsborg (deceased) (Nivå). We are grateful for contributions from F. Racimo, and express our gratitude to the many researchers who have supported laboratory work, analytical procedures and evaluation of results that are presented here, including M. Mannino, P. Reimer and M. Thompson. E.W. thanks St. John’s College, Cambridge, for providing a stimulating environment of discussion and learning.

Publisher Copyright:
© 2024, The Author(s).

Keywords

  • Humans
  • Denmark/ethnology
  • Emigrants and Immigrants/history
  • Genomics
  • Genotype
  • Scandinavians and Nordic People/genetics
  • Human Migration/history
  • Genome, Human/genetics
  • History, Ancient
  • Pollen
  • Diet/history
  • Hunting/history
  • Farmers/history
  • Culture
  • Phenotype
  • Datasets as Topic

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