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 Geoerg; 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 Balasescu; Ross Barnett; Laszlo Bartosiewicz; Gennady Baryshnikov; Clive Bonsall; Dusan Boric; Adina Boroneant; Jelena Bulatovic; Canan Cakirlar; Jose-Miguel Carretero; John Chapman; Mike Church; Richard Crooijmans; Bea De Cupere; Cleia Detry; Vesna Dimitrijevic; Valentin Dumitrascu; Louis du Plessis; Ceiridwen J. Edwards; Cevdet Merih Erek; Asli Erim-Ozdogan; Anton Ervynck; Domenico Fulgione; Mihai Gligor; Anders Gotherstrom; Lionel Gourichon; Martien A. M. Groenen; Daniel Helmer; Hitomi Hongo; Liora K. Horwitz; Evan K. Irving-Pease; Ophelie Lebrasseur; Josephine 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; Joerg Orschiedt; David Orton; Anastasia Papathanasiou; Mike Parker Pearson; Ron Pinhasi; Darko Radmanovic; Francois-Xavier Ricaut; Mike Richards; Richard Sabin; Lucia Sarti; Wolfram Schier; Shiva Sheikhi; Elisabeth Stephan; John R. Stewart; Simon Stoddart; Antonio Tagliacozzo; Nenad Tasic; 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; Jorg Schibler; Peter Rowley-Conwy; Melinda Zeder; Joris Peters; Thomas Cucchi; Daniel G. Bradley; Keith Dobney; Joachim Burger; Allowen Evin; Linus Girdland-Flink; Greger Larson

doi:10.1073/pnas.1901169116

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 Geoerg, 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 Balasescu, Ross Barnett, Laszlo Bartosiewicz, Gennady BaryshnikovClive Bonsall, Dusan Boric, Adina Boroneant, Jelena Bulatovic, Canan Cakirlar, Jose-Miguel Carretero, John Chapman, Mike Church, Richard Crooijmans, Bea De Cupere, Cleia Detry, Vesna Dimitrijevic, Valentin Dumitrascu, Louis du Plessis, Ceiridwen J. Edwards, Cevdet Merih Erek, Asli Erim-Ozdogan, Anton Ervynck, Domenico Fulgione, Mihai Gligor, Anders Gotherstrom, Lionel Gourichon, Martien A. M. Groenen, Daniel Helmer, Hitomi Hongo, Liora K. Horwitz, Evan K. Irving-Pease, Ophelie Lebrasseur, Josephine 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, Joerg Orschiedt, David Orton, Anastasia Papathanasiou, Mike Parker Pearson, Ron Pinhasi, Darko Radmanovic, Francois-Xavier Ricaut, Mike Richards, Richard Sabin, Lucia Sarti, Wolfram Schier, Shiva Sheikhi, Elisabeth Stephan, John R. Stewart, Simon Stoddart, Antonio Tagliacozzo, Nenad Tasic, 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, Jorg Schibler, Peter Rowley-Conwy, Melinda Zeder, Joris Peters, Thomas Cucchi, Daniel G. Bradley, Keith Dobney, Joachim Burger, Allowen Evin, Linus Girdland-Flink, Greger Larson

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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 language	English
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	116
Issue number	35
Pages (from-to)	17231-17238
ISSN	0027-8424
DOIs	https://doi.org/10.1073/pnas.1901169116
Publication status	Published - 27 Aug 2019

Keywords

domestication
evolution
gene flow
Neolithic

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10.1073/pnas.1901169116Licence: CC BY

17231.fullFinal published version, 1.12 MBLicence: CC BY

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Frantz, L. A. F., Haile, J., Lin, A. T., Scheu, A., Geoerg, C., Benecke, N., Alexander, M., Linderholm, A., Mullin, V. E., Daly, K. G., Battista, V. M., Price, M., Gron, K. J., Alexandri, P., Arbogast, R.-M., Arbuckle, B., Balasescu, A., Barnett, R., Bartosiewicz, 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, 116(35), 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. et al.
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 journal › Journal article › Research › peer-review

Frantz, LAF, Haile, J, Lin, AT, Scheu, A, Geoerg, C, Benecke, N, Alexander, M, Linderholm, A, Mullin, VE, Daly, KG, Battista, VM, Price, M, Gron, KJ, Alexandri, P, Arbogast, R-M, Arbuckle, B, Balasescu, A, Barnett, R, Bartosiewicz, L, Baryshnikov, G, Bonsall, C, Boric, D, Boroneant, A, Bulatovic, J, Cakirlar, C, Carretero, J-M, Chapman, J, Church, M, Crooijmans, R, De Cupere, B, Detry, C, Dimitrijevic, V, Dumitrascu, V, du Plessis, L, Edwards, CJ, Erek, CM, Erim-Ozdogan, A, Ervynck, A, Fulgione, D, Gligor, M, Gotherstrom, 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, H-J, Miller, R, Mohaseb, AF, Orschiedt, J, Orton, D, Papathanasiou, A, Pearson, MP, Pinhasi, R, Radmanovic, D, Ricaut, F-X, Richards, M, Sabin, R, Sarti, L, Schier, W, Sheikhi, S, Stephan, E, Stewart, JR, Stoddart, S, Tagliacozzo, A, Tasic, N, Trantalidou, K, Tresset, A, Valdiosera, C, van den Hurk, Y, Van Poucke, S, Vigne, J-D, 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

@article{cfb1a5c94cf94ef9851f0dfa76e0538a,

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.",

keywords = "domestication, evolution, gene flow, Neolithic",

author = "Frantz, {Laurent A. F.} and James Haile and Lin, {Audrey T.} and Amelie Scheu and Christina Geoerg and Norbert Benecke and Michelle Alexander and Anna Linderholm and Mullin, {Victoria E.} and Daly, {Kevin G.} and Battista, {Vincent M.} and Max Price and Gron, {Kurt J.} and Panoraia Alexandri and Rose-Marie Arbogast and Benjamin Arbuckle and Adrian Balasescu and Ross Barnett and Laszlo Bartosiewicz and Gennady Baryshnikov and Clive Bonsall and Dusan Boric and Adina Boroneant and Jelena Bulatovic and Canan Cakirlar and Jose-Miguel Carretero and John Chapman and Mike Church and Richard Crooijmans and {De Cupere}, Bea and Cleia Detry and Vesna Dimitrijevic and Valentin Dumitrascu and {du Plessis}, Louis and Edwards, {Ceiridwen J.} and Erek, {Cevdet Merih} and Asli Erim-Ozdogan and Anton Ervynck and Domenico Fulgione and Mihai Gligor and Anders Gotherstrom and Lionel Gourichon and Groenen, {Martien A. M.} and Daniel Helmer and Hitomi Hongo and Horwitz, {Liora K.} and Irving-Pease, {Evan K.} and Ophelie Lebrasseur and Josephine Lesur and Caroline Malone and Ninna Manaseryan and Arkadiusz Marciniak and Holley Martlew and Marjan Mashkour and Roger Matthews and Matuzeviciute, {Giedre Motuzaite} and Sepideh Maziar and Erik Meijaard and Tom McGovern and Hendrik-Jan Megens and Rebecca Miller and Mohaseb, {Azadeh Fatemeh} and Joerg Orschiedt and David Orton and Anastasia Papathanasiou and Pearson, {Mike Parker} and Ron Pinhasi and Darko Radmanovic and Francois-Xavier Ricaut and Mike Richards and Richard Sabin and Lucia Sarti and Wolfram Schier and Shiva Sheikhi and Elisabeth Stephan and Stewart, {John R.} and Simon Stoddart and Antonio Tagliacozzo and Nenad Tasic and Katerina Trantalidou and Anne Tresset and Cristina Valdiosera and {van den Hurk}, Youri and {Van Poucke}, Sophie and Jean-Denis Vigne and Alexander Yanevich and Andrea Zeeb-Lanz and Alexandros Triantafyllidis and Gilbert, {M. Thomas P.} and Jorg Schibler and Peter Rowley-Conwy and Melinda Zeder and Joris Peters and Thomas Cucchi and Bradley, {Daniel G.} and Keith Dobney and Joachim Burger and Allowen Evin and Linus Girdland-Flink and Greger Larson",

year = "2019",

month = aug,

day = "27",

doi = "10.1073/pnas.1901169116",

language = "English",

volume = "116",

pages = "17231--17238",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "The National Academy of Sciences of the United States of America",

number = "35",

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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 - Geoerg, 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 - Balasescu, Adrian

AU - Barnett, Ross

AU - Bartosiewicz, Laszlo

AU - Baryshnikov, Gennady

AU - Bonsall, Clive

AU - Boric, Dusan

AU - Boroneant, Adina

AU - Bulatovic, Jelena

AU - Cakirlar, Canan

AU - Carretero, Jose-Miguel

AU - Chapman, John

AU - Church, Mike

AU - Crooijmans, Richard

AU - De Cupere, Bea

AU - Detry, Cleia

AU - Dimitrijevic, Vesna

AU - Dumitrascu, Valentin

AU - du Plessis, Louis

AU - Edwards, Ceiridwen J.

AU - Erek, Cevdet Merih

AU - Erim-Ozdogan, Asli

AU - Ervynck, Anton

AU - Fulgione, Domenico

AU - Gligor, Mihai

AU - Gotherstrom, 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, Ophelie

AU - Lesur, Josephine

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, Joerg

AU - Orton, David

AU - Papathanasiou, Anastasia

AU - Pearson, Mike Parker

AU - Pinhasi, Ron

AU - Radmanovic, Darko

AU - Ricaut, Francois-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 - Tasic, 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, Jorg

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

U2 - 10.1073/pnas.1901169116

DO - 10.1073/pnas.1901169116

M3 - Journal article

C2 - 31405970

SN - 0027-8424

VL - 116

SP - 17231

EP - 17238

JO - 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

IS - 35

ER -

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

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