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 & 80 others 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

Research output: Contribution to journalArticle

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.

LanguageEnglish
Pages17231-17238
Number of pages8
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number35
DOIs
Publication statusPublished - 27 Aug 2019

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Sus scrofa
Swine
Middle East
Mitochondrial DNA
Gene Flow
Haplotypes
Color
Genome

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Frantz, Laurent A.F. ; Haile, James ; Lin, Audrey T. ; Scheu, Amelie ; Geörg, Christina ; Benecke, Norbert ; Alexander, Michelle ; Linderholm, Anna ; Mullin, Victoria E. ; Daly, Kevin G. ; Battista, Vincent M. ; Price, Max ; Gron, Kurt J. ; Alexandri, Panoraia ; Arbogast, Rose Marie ; Arbuckle, Benjamin ; Bǎlǎşescu, Adrian ; Barnett, Ross ; Bartosiewicz, László ; Baryshnikov, Gennady ; Bonsall, Clive ; Borić, Dušan ; Boroneanţ, Adina ; Bulatović, Jelena ; Çakirlar, Canan ; Carretero, José Miguel ; Chapman, John ; Church, Mike ; Crooijmans, Richard ; De Cupere, Bea ; Detry, Cleia ; Dimitrijevic, Vesna ; Dumitraşcu, Valentin ; Du Plessis, Louis ; Edwards, Ceiridwen J. ; Erek, Cevdet Merih ; Erim-Özdoǧan, Asli ; Ervynck, Anton ; Fulgione, Domenico ; Gligor, Mihai ; Götherström, Anders ; Gourichon, Lionel ; Groenen, Martien A.M. ; Helmer, Daniel ; Hongo, Hitomi ; Horwitz, Liora K. ; Irving-Pease, Evan K. ; Lebrasseur, Ophélie ; Lesur, Joséphine ; Malone, Caroline ; Manaseryan, Ninna ; Marciniak, Arkadiusz ; Martlew, Holley ; Mashkour, Marjan ; Matthews, Roger ; Matuzeviciute, Giedre Motuzaite ; Maziar, Sepideh ; Meijaard, Erik ; McGovern, Tom ; Megens, Hendrik Jan ; Miller, Rebecca ; Mohaseb, Azadeh Fatemeh ; Orschiedt, Jörg ; Orton, David ; Papathanasiou, Anastasia ; Pearson, Mike Parker ; Pinhasi, Ron ; Radmanović, Darko ; Ricaut, François Xavier ; Richards, Mike ; Sabin, Richard ; Sarti, Lucia ; Schier, Wolfram ; Sheikhi, Shiva ; Stephan, Elisabeth ; Stewart, John R. ; Stoddart, Simon ; Tagliacozzo, Antonio ; Tasić, Nenad ; Trantalidou, Katerina ; Tresset, Anne ; Valdiosera, Cristina ; Van Den Hurk, Youri ; Van Poucke, Sophie ; Vigne, Jean Denis ; Yanevich, Alexander ; Zeeb-Lanz, Andrea ; Triantafyllidis, Alexandros ; Gilbert, M. Thomas P. ; Schibler, Jörg ; Rowley-Conwy, Peter ; Zeder, Melinda ; Peters, Joris ; Cucchi, Thomas ; Bradley, Daniel G. ; Dobney, Keith ; Burger, Joachim ; Evin, Allowen ; Girdland-Flink, Linus ; Larson, Greger. / Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe. In: Proceedings of the National Academy of Sciences of the United States of America. 2019 ; Vol. 116, No. 35. pp. 17231-17238.
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title = "Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe",
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.",
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Frantz, LAF, Haile, J, Lin, AT, Scheu, A, Geörg, C, Benecke, N, Alexander, M, Linderholm, A, Mullin, VE, Daly, KG, Battista, VM, Price, M, Gron, KJ, Alexandri, P, Arbogast, RM, Arbuckle, B, Bǎlǎşescu, A, Barnett, R, Bartosiewicz, L, Baryshnikov, G, Bonsall, C, Borić, D, Boroneanţ, A, Bulatović, J, Çakirlar, C, Carretero, JM, Chapman, J, Church, M, Crooijmans, R, De Cupere, B, Detry, C, Dimitrijevic, V, Dumitraşcu, V, Du Plessis, L, Edwards, CJ, Erek, CM, Erim-Özdoǧan, A, Ervynck, A, Fulgione, D, Gligor, M, Götherström, A, Gourichon, L, Groenen, MAM, Helmer, D, Hongo, H, Horwitz, LK, Irving-Pease, EK, Lebrasseur, O, Lesur, J, Malone, C, Manaseryan, N, Marciniak, A, Martlew, H, Mashkour, M, Matthews, R, Matuzeviciute, GM, Maziar, S, Meijaard, E, McGovern, T, Megens, HJ, Miller, R, Mohaseb, AF, Orschiedt, J, Orton, D, Papathanasiou, A, Pearson, MP, Pinhasi, R, Radmanović, D, Ricaut, FX, Richards, M, Sabin, R, Sarti, L, Schier, W, Sheikhi, S, Stephan, E, Stewart, JR, Stoddart, S, Tagliacozzo, A, Tasić, N, Trantalidou, K, Tresset, A, Valdiosera, C, Van Den Hurk, Y, Van Poucke, S, Vigne, JD, Yanevich, A, Zeeb-Lanz, A, Triantafyllidis, A, Gilbert, MTP, Schibler, J, Rowley-Conwy, P, Zeder, M, Peters, J, Cucchi, T, Bradley, DG, Dobney, K, Burger, J, Evin, A, Girdland-Flink, L & Larson, G 2019, 'Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe', Proceedings of the National Academy of Sciences of the United States of America, vol. 116, no. 35, pp. 17231-17238. https://doi.org/10.1073/pnas.1901169116

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

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 35, 27.08.2019, p. 17231-17238.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe

AU - Frantz, Laurent A.F.

AU - Haile, James

AU - Lin, Audrey T.

AU - Scheu, Amelie

AU - Geörg, Christina

AU - Benecke, Norbert

AU - Alexander, Michelle

AU - Linderholm, Anna

AU - Mullin, Victoria E.

AU - Daly, Kevin G.

AU - Battista, Vincent M.

AU - Price, Max

AU - Gron, Kurt J.

AU - Alexandri, Panoraia

AU - Arbogast, Rose Marie

AU - Arbuckle, Benjamin

AU - Bǎlǎşescu, Adrian

AU - Barnett, Ross

AU - Bartosiewicz, László

AU - Baryshnikov, Gennady

AU - Bonsall, Clive

AU - Borić, Dušan

AU - Boroneanţ, Adina

AU - Bulatović, Jelena

AU - Çakirlar, Canan

AU - Carretero, José Miguel

AU - Chapman, John

AU - Church, Mike

AU - Crooijmans, Richard

AU - De Cupere, Bea

AU - Detry, Cleia

AU - Dimitrijevic, Vesna

AU - Dumitraşcu, Valentin

AU - Du Plessis, Louis

AU - Edwards, Ceiridwen J.

AU - Erek, Cevdet Merih

AU - Erim-Özdoǧan, Asli

AU - Ervynck, Anton

AU - Fulgione, Domenico

AU - Gligor, Mihai

AU - Götherström, Anders

AU - Gourichon, Lionel

AU - Groenen, Martien A.M.

AU - Helmer, Daniel

AU - Hongo, Hitomi

AU - Horwitz, Liora K.

AU - Irving-Pease, Evan K.

AU - Lebrasseur, Ophélie

AU - Lesur, Joséphine

AU - Malone, Caroline

AU - Manaseryan, Ninna

AU - Marciniak, Arkadiusz

AU - Martlew, Holley

AU - Mashkour, Marjan

AU - Matthews, Roger

AU - Matuzeviciute, Giedre Motuzaite

AU - Maziar, Sepideh

AU - Meijaard, Erik

AU - McGovern, Tom

AU - Megens, Hendrik Jan

AU - Miller, Rebecca

AU - Mohaseb, Azadeh Fatemeh

AU - Orschiedt, Jörg

AU - Orton, David

AU - Papathanasiou, Anastasia

AU - Pearson, Mike Parker

AU - Pinhasi, Ron

AU - Radmanović, Darko

AU - Ricaut, François Xavier

AU - Richards, Mike

AU - Sabin, Richard

AU - Sarti, Lucia

AU - Schier, Wolfram

AU - Sheikhi, Shiva

AU - Stephan, Elisabeth

AU - Stewart, John R.

AU - Stoddart, Simon

AU - Tagliacozzo, Antonio

AU - Tasić, Nenad

AU - Trantalidou, Katerina

AU - Tresset, Anne

AU - Valdiosera, Cristina

AU - Van Den Hurk, Youri

AU - Van Poucke, Sophie

AU - Vigne, Jean Denis

AU - Yanevich, Alexander

AU - Zeeb-Lanz, Andrea

AU - Triantafyllidis, Alexandros

AU - Gilbert, M. Thomas P.

AU - Schibler, Jörg

AU - Rowley-Conwy, Peter

AU - Zeder, Melinda

AU - Peters, Joris

AU - Cucchi, Thomas

AU - Bradley, Daniel G.

AU - Dobney, Keith

AU - Burger, Joachim

AU - Evin, Allowen

AU - Girdland-Flink, Linus

AU - Larson, Greger

PY - 2019/8/27

Y1 - 2019/8/27

N2 - 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.

AB - 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.

KW - Domestication

KW - Evolution

KW - Gene flow

KW - Neolithic

UR - http://www.scopus.com/inward/record.url?scp=85071714237&partnerID=8YFLogxK

U2 - 10.1073/pnas.1901169116

DO - 10.1073/pnas.1901169116

M3 - Article

VL - 116

SP - 17231

EP - 17238

JO - Proceedings of the National Academy of Sciences of the United States of America

T2 - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 35

ER -