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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 Baryshnikov
  • Clive 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
  • Queen Mary University of London
  • Johannes Gutenberg University Mainz
  • German Archaeological Institute
  • University of York
  • Texas A&M University
  • The Natural History Museum, London
  • Trinity College Dublin
  • University of Michigan, Ann Arbor
  • Massachusetts Institute of Technology
  • Durham University
  • CNRS
  • Aristotle University of Thessaloniki
  • University of North Carolina at Chapel Hill
  • 'Vasile Pârvan' Institute of Archaeology
  • Russian Academy of Sciences
  • University of Belgrade
  • University of Groningen
  • Universidad de Burgos
  • Wageningen University & Research
  • Royal Belgian Institute of Natural Sciences
  • University of Lisbon
  • University of Huddersfield
  • Gazi University
  • Canakkale Onsekiz Mart University
  • Flanders Heritage Agency
  • University of Naples Federico II
  • 1 Decembrie 1918 University of Alba Iulia
  • Moyen Âge (UMR 7264)
  • The Graduate University for Advanced Studies
  • Hebrew University of Jerusalem
  • Muséum national d'histoire naturelle
  • Queen's University Belfast
  • Institute of Zoology
  • Adam Mickiewicz University in Poznań
  • Hellenic Archaeological Research Foundation
  • University of Reading
  • Vilnius University
  • Goethe University Frankfurt
  • International Union for Conservation of Nature/Species Survival Commission Wild Pig Specialist Group
  • University of Queensland
  • University of Kent
  • City University of New York
  • University of Liege
  • Free University of Berlin
  • Curt-Engelhorn-Zentrum Archäometrie gGmbH
  • Greek Ministry of Culture
  • University College London
  • University of Vienna
  • Museum of Vojvodina
  • Université Fédérale Toulouse Midi-Pyrénées
  • University of Siena
  • Osteologie
  • Bournemouth University
  • Museo delle Civiltà
  • La Trobe University
  • National Academy of Sciences of Ukraine
  • Generaldirektion Kulturelles Erbe Rheinland-Pfalz
  • University of Copenhagen
  • Norwegian University of Science and Technology
  • University of Basel
  • Smithsonian Institution
  • Ludwig Maximilian University of Munich
  • Bavarian Natural History Collections
  • Unite Archeozoologie
  • Institut de recherche pour le développement
  • University of Oxford
  • University of Stockholm
  • University of Edinburgh
  • University of Liverpool
  • University of Cambridge
  • Simon Fraser University
  • Liverpool John Moores University
  • Columbia University

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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

Funding

ACKNOWLEDGMENTS. We thank L. Orlando and J. Schraiber for their valuable comments and R. Redding, A. Dinu, A. Devault, A. Mahforozi, A. Hammon, A. McMahon, B. Wilkens, C. Commenge, C. Minniti, D. Kennet, D. Mol, D. Binder, E. Vika, G. Bayle, H.-J. Döhle, I. Dubset, I. Fiore, J. de Grossi Mazzorin, J. Enk, J. Glimmerveen, J. Courtin, J. L. Arsuaga, J. Lev-Tov, K. Aaris-Sørensen, K. Post, M. Özdog˘ an, M. Özbas¸aran, P. Miracle, R. Portela-Miguez, R. Meadow, S. Davis, S. Bréhard, S. Hanik, U. Albarella, T. O’Connor, S. Hansen, M. Toderas, P. Bogucki, D. Lo Vetro, R. Andreescu, P. Mirea, D. Popovici, C. Micu, I. M. Chicideanu, P. Damian, C. Becker, R. Gleser, S. Hansen, R. Hofmann, R. Krauss, M. Lichardus-Itten, N. Müller-Scheessel, B. Weninger, and I. Österholm for providing material and support. We also thank the team working at the site of As¸ıklı Höyük: M. Özbas¸aran, H. Buitenhuis, N. Munro, N. Pöllath, and M. Stiner. For the Iranian material, we thank Eberhard Sauer, Jebreil Nokandeh (Iranian Cultural Heritage Handicraft and Tourism Organization) and European Research Council (ERC) Persia and Neighbours (ERC-2011-ADG_20110406). We also thank the staff of the Danish National High-Throughput Sequencing Centre for assistance in data generation. We acknowledge the University of Oxford Advanced Research Computing facility for providing computing time. L.A.F.F. was supported by the Wellcome Trust (Grant 210119/Z/18/Z) and by Wolfson College (University of Oxford). L.A.F.F., J.H., A. Linderholm, K.D., and G.L. were supported by the ERC (Grant ERC-2013-StG-337574-UNDEAD), Natural Environmental Research Council (Grants NE/K005243/1 and NE/K003259/1), or both. M.T.P.G. was supported by the ERC (Grant ERC-2015-CoG-681396–Extinction Genomics). D.B., V.E.M., and K.D. were supported by the ERC (Grant 295729-CodeX). A. Ba˘la˘s¸escu and V. Dumitrascu (Romanian archaeozoological research) were supported by the Romanian National Authority for Scientific Research (Project PN‐III-P4‐ID‐PCE‐2016‐0676) T.M. was supported by the National Geographic Society, Icelandic Centre for Research (RANNÍS), and US National Science Foundation (NSF) (Grants 0732327, 1140106, 1119354, 1203823, 1203268, 1202692, 1249313, 0527732, 0638897, 0629500, 0947862, and 1446308). J.P. was supported by the General Directorate of Antiquities in Turkey and the Deutsche Forschungsgemeinschaft (Grant PE 424/10,1-3). C.V. and J.-M.C. were supported by the Atapuerca Project (CGL2015-65387-C3-2-P MINECO-FEDER, Ministerio de Economía y Competitividad, Spain), the Junta de Castilla y León, and the Fundación Atapuerca. L.d.P. was supported by the ERC (Grant ERC-2013-CoG-614725–PATHPHYLODYN). M.C. was supported by the NSF (Grants 0732327 and 1202692). M.G. was supported by a grant from the Romanian National Authority for Scientific Research (Project PN-II-RU-TE-2012-3-0461). V. Dimitrijevic was supported by the Ministry of Culture and Information and the Ministry of Education and Science of the Republic of Serbia (Project III 47001). B.A. was supported by the NSF (Grants BCS-0530699 and BCS-1311551), the National Geographic Society, and the American Research Institute in Turkey. C.D. was supported by the Fundação para a Ciência e Tecnologia (Grant SFRH/BPD/ 108326/2015). A.S. and C.G. were supported by the German Archaeological Institute, Berlin (Research Cluster 1, Project: Genetische Studien zur Zucht-und Nutzungsgeschichte der ältesten Wirtschaftshaustiere). L.G.-F. was supported by the British Academy and Leverhulme Trust (Grant SG143331). A.M. was supported by the National Science Centre, Poland (Grant 2017/25/B/HS3/01242).

Keywords

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

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