Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe

Laurent A.F. Frantz*, James Haile, Audrey T. Lin, Amelie Scheu, Christina Geörg, Norbert Benecke, Michelle Alexander, Anna Linderholm, Victoria E. Mullin, Kevin G. Daly, Vincent M. Battista, Max Price, Kurt J. Gron, Panoraia Alexandri, Rose Marie Arbogast, Benjamin Arbuckle, Adrian Bǎlǎşescu, Ross Barnett, László Bartosiewicz, Gennady BaryshnikovClive Bonsall, Dušan Borić, Adina Boroneanţ, Jelena Bulatović, Canan Çakirlar, José Miguel Carretero, John Chapman, Mike Church, Richard Crooijmans, Bea De Cupere, Cleia Detry, Vesna Dimitrijevic, Valentin Dumitraşcu, Louis Du Plessis, Ceiridwen J. Edwards, Cevdet Merih Erek, Asli Erim-Özdoǧan, Anton Ervynck, Domenico Fulgione, Mihai Gligor, Anders Götherström, Lionel Gourichon, Martien A.M. Groenen, Daniel Helmer, Hitomi Hongo, Liora K. Horwitz, Evan K. Irving-Pease, Ophélie Lebrasseur, Joséphine Lesur, Caroline Malone, Ninna Manaseryan, Arkadiusz Marciniak, Holley Martlew, Marjan Mashkour, Roger Matthews, Giedre Motuzaite Matuzeviciute, Sepideh Maziar, Erik Meijaard, Tom McGovern, Hendrik Jan Megens, Rebecca Miller, Azadeh Fatemeh Mohaseb, Jörg Orschiedt, David Orton, Anastasia Papathanasiou, Mike Parker Pearson, Ron Pinhasi, Darko Radmanović, François Xavier Ricaut, Mike Richards, Richard Sabin, Lucia Sarti, Wolfram Schier, Shiva Sheikhi, Elisabeth Stephan, John R. Stewart, Simon Stoddart, Antonio Tagliacozzo, Nenad Tasić, Katerina Trantalidou, Anne Tresset, Cristina Valdiosera, Youri Van Den Hurk, Sophie Van Poucke, Jean Denis Vigne, Alexander Yanevich, Andrea Zeeb-Lanz, Alexandros Triantafyllidis, M. Thomas P. Gilbert, Jörg Schibler, Peter Rowley-Conwy, Melinda Zeder, Joris Peters, Thomas Cucchi, Daniel G. Bradley, Keith Dobney, Joachim Burger, Allowen Evin, Linus Girdland-Flink, Greger Larson

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

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Abstract

Archaeological evidence indicates that pig domestication had begun by ∼10,500 y before the present (BP) in the Near East, and mitochondrial DNA (mtDNA) suggests that pigs arrived in Europe alongside farmers ∼8,500 y BP. A few thousand years after the introduction of Near Eastern pigs into Europe, however, their characteristic mtDNA signature disappeared and was replaced by haplotypes associated with European wild boars. This turnover could be accounted for by substantial gene flow from local European wild boars, although it is also possible that European wild boars were domesticated independently without any genetic contribution from the Near East. To test these hypotheses, we obtained mtDNA sequences from 2,099 modern and ancient pig samples and 63 nuclear ancient genomes from Near Eastern and European pigs. Our analyses revealed that European domestic pigs dating from 7,100 to 6,000 y BP possessed both Near Eastern and European nuclear ancestry, while later pigs possessed no more than 4% Near Eastern ancestry, indicating that gene flow from European wild boars resulted in a near-complete disappearance of Near East ancestry. In addition, we demonstrate that a variant at a locus encoding black coat color likely originated in the Near East and persisted in European pigs. Altogether, our results indicate that while pigs were not independently domesticated in Europe, the vast majority of human-mediated selection over the past 5,000 y focused on the genomic fraction derived from the European wild boars, and not on the fraction that was selected by early Neolithic farmers over the first 2,500 y of the domestication process.

Original languageEnglish
Pages (from-to)17231-17238
Number of pages8
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number35
Early online date12 Aug 2019
DOIs
Publication statusPublished - 27 Aug 2019

Bibliographical note

Data deposition: The reads from both ancient and modern samples have been deposited at the European Nucleotide Archive (ENA) (project no. PRJEB30282).


Correction for Frantz et al., Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe PNAS June 23, 2020 117 (25) 14610-14611; first published June 15, 2020; https://doi.org/10.1073/pnas.2008793117

Keywords

  • Domestication
  • Evolution
  • Gene flow
  • Neolithic
  • gene flow
  • WILD
  • SIZE
  • evolution
  • DOMESTIC PIGS
  • INTROGRESSION
  • DNA
  • domestication
  • SPREAD
  • BREEDS
  • HISTORY
  • LONG

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