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 language | English |
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Pages (from-to) | 17231-17238 |
Number of pages | 8 |
Journal | Proceedings of the National Academy of Sciences of the United States of America |
Volume | 116 |
Issue number | 35 |
DOIs | |
State | Published - 27 Aug 2019 |
Externally published | Yes |
Bibliographical note
Publisher Copyright:© 2019 National Academy of Sciences. All rights reserved.
Funding
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. Özdoǧan, M. Özbaşaran, 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 Aşikli Höyük: M. Özbaşaran, 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. Bǎlǎşescu 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). 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).
Funders | Funder number |
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British Academy and Leverhulme Trust | SG143331 |
Fundación Atapuerca | ERC-2013-CoG-614725–PATHPHYLODYN |
General Directorate of Antiquities in Turkey | |
Genetische Studien zur Zucht | |
Genetische Studien zur Zucht-und Nutzungsgeschichte der ältesten Wirtschaftshaustiere | |
Iranian Cultural Heritage Handicraft and Tourism Organization | |
Ministry of Culture and Information | |
Nutzungsgeschichte der ältesten Wirtschaftshaustiere | |
National Science Foundation | 1203268, 1119354, 0638897, 1202692, 0629500, 1249313, 1203823, 1446308, 0732327, 1140106, 0527732, 0947862 |
American Research Institute in Turkey | |
National Geographic Society | |
Wellcome Trust | 210119/Z/18/Z |
Natural Environment Research Council | ERC-2015-CoG-681396, NE/K003259/1, NE/K005243/1, 295729-CodeX |
Wolfson College, University of Oxford | |
Oxford University | ERC-2013-StG-337574-UNDEAD |
European Commission | ERC-2011-ADG-20110406 |
Deutsche Forschungsgemeinschaft | PE 424/10,1-3, CGL2015-65387-C3-2-P MINECO-FEDER |
Icelandic Centre for Research | |
Fundação para a Ciência e a Tecnologia | SFRH/BPD/108326/2015 |
Ministerio de Economía y Competitividad | |
Narodowe Centrum Nauki | 2017/25/B/HS3/01242 |
Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja | BCS-1311551, III 47001, BCS-0530699 |
Autoritatea Natională pentru Cercetare Stiintifică | PN-II-RU-TE-2012-3-0461, PN‐III-P4‐ID‐PCE‐2016‐0676 |
Consejería de Educación, Junta de Castilla y León | |
Rannís | |
Neurosciences Foundation |
Keywords
- Domestication
- Evolution
- Gene flow
- Neolithic