Analyses of pig genomes provide insight into porcine demography and evolution

Martien A M Groenen, Alan L Archibald, Hirohide Uenishi, Christopher K Tuggle, Yasuhiro Takeuchi, Max F Rothschild, Claire Rogel-Gaillard, Chankyu Park, Denis Milan, Hendrik-Jan Megens, Shengting Li, Denis M Larkin, Heebal Kim, Laurent A F Frantz, Mario Caccamo, Hyeonju Ahn, Bronwen L Aken, Anna Anselmo, Christian Anthon, Loretta AuvilBouabid Badaoui, Craig W Beattie, Christian Bendixen, Daniel Berman, Frank Blecha, Jonas Blomberg, Lars Bolund, Mirte Bosse, Sara Botti, Zhan Bujie, Megan Bystrom, Boris Capitanu, Denise Carvalho-Silva, Patrick Chardon, Celine Chen, Ryan Cheng, Sang-Haeng Choi, William Chow, Richard C Clark, Christopher Clee, Richard P M A Crooijmans, Harry D Dawson, Patrice Dehais, Fioravante De Sapio, Bert Dibbits, Nizar Drou, Zhi-Qiang Du, Kellye Eversole, João Fadista, Susan Fairley, Thomas Faraut, Geoffrey J Faulkner, Katie E Fowler, Merete Fredholm, Eric Fritz, James G R Gilbert, Elisabetta Giuffra, Jan Gorodkin, Darren K Griffin, Jennifer L Harrow, Alexander Hayward, Kerstin Howe, Zhi-Liang Hu, Sean J Humphray, Toby Hunt, Henrik Hornshøj, Jin-Tae Jeon, Patric Jern, Matthew Jones, Jerzy Jurka, Hiroyuki Kanamori, Ronan Kapetanovic, Jaebum Kim, Jae-Hwan Kim, Kyu-Won Kim, Tae-Hun Kim, Greger Larson, Kyooyeol Lee, Kyung-Tai Lee, Richard Leggett, Harris A Lewin, Yingrui Li, Wansheng Liu, Jane E Loveland, Yao Lu, Joan K Lunney, Jian Ma, Ole Madsen, Katherine Mann, Lucy Matthews, Stuart McLaren, Takeya Morozumi, Michael P Murtaugh, Jitendra Narayan, Dinh Truong Nguyen, Peixiang Ni, Song-Jung Oh, Suneel Onteru, Frank Panitz, Eung-Woo Park, Hong-Seog Park, Geraldine Pascal, Yogesh Paudel, Miguel Perez-Enciso, Ricardo Ramirez-Gonzalez, James M Reecy, Sandra Rodriguez-Zas, Gary A Rohrer, Lauretta Rund, Yongming Sang, Kyle Schachtschneider, Joshua G Schraiber, John Schwartz, Linda Scobie, Carol Scott, Stephen Searle, Bertrand Servin, Bruce R Southey, Goran Sperber, Peter Stadler, Jonathan V Sweedler, Hakim Tafer, Bo Thomsen, Rashmi Wali, Jian Wang, Jun Wang, Simon White, Xun Xu, Martine Yerle, Guojie Zhang, Jianguo Zhang, Jie Zhang, Shuhong Zhao, Jane Rogers, Carol Churcher, Lawrence B Schook

Research output: Contribution to journalArticle

707 Citations (Scopus)

Abstract

For 10,000 years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ~1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.
Original languageEnglish
Pages (from-to)393-398
Number of pages6
JournalNature
Volume491
Issue number7424
DOIs
Publication statusPublished - 15 Nov 2012

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Sus scrofa
Swine
Demography
Genome
Smell
Odorant Receptors
Genes
Far East
Livestock
Breeding
Sequence Analysis
RNA

Cite this

Groenen, M. A. M., Archibald, A. L., Uenishi, H., Tuggle, C. K., Takeuchi, Y., Rothschild, M. F., ... Schook, L. B. (2012). Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 491(7424), 393-398. https://doi.org/10.1038/nature11622

Analyses of pig genomes provide insight into porcine demography and evolution. / Groenen, Martien A M; Archibald, Alan L; Uenishi, Hirohide; Tuggle, Christopher K; Takeuchi, Yasuhiro; Rothschild, Max F; Rogel-Gaillard, Claire; Park, Chankyu; Milan, Denis; Megens, Hendrik-Jan; Li, Shengting; Larkin, Denis M; Kim, Heebal; Frantz, Laurent A F; Caccamo, Mario; Ahn, Hyeonju; Aken, Bronwen L; Anselmo, Anna; Anthon, Christian; Auvil, Loretta; Badaoui, Bouabid; Beattie, Craig W; Bendixen, Christian; Berman, Daniel; Blecha, Frank; Blomberg, Jonas; Bolund, Lars; Bosse, Mirte; Botti, Sara; Bujie, Zhan; Bystrom, Megan; Capitanu, Boris; Carvalho-Silva, Denise; Chardon, Patrick; Chen, Celine; Cheng, Ryan; Choi, Sang-Haeng; Chow, William; Clark, Richard C; Clee, Christopher; Crooijmans, Richard P M A; Dawson, Harry D; Dehais, Patrice; De Sapio, Fioravante; Dibbits, Bert; Drou, Nizar; Du, Zhi-Qiang; Eversole, Kellye; Fadista, João; Fairley, Susan; Faraut, Thomas; Faulkner, Geoffrey J; Fowler, Katie E; Fredholm, Merete; Fritz, Eric; Gilbert, James G R; Giuffra, Elisabetta; Gorodkin, Jan; Griffin, Darren K; Harrow, Jennifer L; Hayward, Alexander; Howe, Kerstin; Hu, Zhi-Liang; Humphray, Sean J; Hunt, Toby; Hornshøj, Henrik; Jeon, Jin-Tae; Jern, Patric; Jones, Matthew; Jurka, Jerzy; Kanamori, Hiroyuki; Kapetanovic, Ronan; Kim, Jaebum; Kim, Jae-Hwan; Kim, Kyu-Won; Kim, Tae-Hun; Larson, Greger; Lee, Kyooyeol; Lee, Kyung-Tai; Leggett, Richard; Lewin, Harris A; Li, Yingrui; Liu, Wansheng; Loveland, Jane E; Lu, Yao; Lunney, Joan K; Ma, Jian; Madsen, Ole; Mann, Katherine; Matthews, Lucy; McLaren, Stuart; Morozumi, Takeya; Murtaugh, Michael P; Narayan, Jitendra; Nguyen, Dinh Truong; Ni, Peixiang; Oh, Song-Jung; Onteru, Suneel; Panitz, Frank; Park, Eung-Woo; Park, Hong-Seog; Pascal, Geraldine; Paudel, Yogesh; Perez-Enciso, Miguel; Ramirez-Gonzalez, Ricardo; Reecy, James M; Rodriguez-Zas, Sandra; Rohrer, Gary A; Rund, Lauretta; Sang, Yongming; Schachtschneider, Kyle; Schraiber, Joshua G; Schwartz, John; Scobie, Linda; Scott, Carol; Searle, Stephen; Servin, Bertrand; Southey, Bruce R; Sperber, Goran; Stadler, Peter; Sweedler, Jonathan V; Tafer, Hakim; Thomsen, Bo; Wali, Rashmi; Wang, Jian; Wang, Jun; White, Simon; Xu, Xun; Yerle, Martine; Zhang, Guojie; Zhang, Jianguo; Zhang, Jie; Zhao, Shuhong; Rogers, Jane; Churcher, Carol; Schook, Lawrence B.

In: Nature, Vol. 491, No. 7424, 15.11.2012, p. 393-398.

Research output: Contribution to journalArticle

Groenen, MAM, Archibald, AL, Uenishi, H, Tuggle, CK, Takeuchi, Y, Rothschild, MF, Rogel-Gaillard, C, Park, C, Milan, D, Megens, H-J, Li, S, Larkin, DM, Kim, H, Frantz, LAF, Caccamo, M, Ahn, H, Aken, BL, Anselmo, A, Anthon, C, Auvil, L, Badaoui, B, Beattie, CW, Bendixen, C, Berman, D, Blecha, F, Blomberg, J, Bolund, L, Bosse, M, Botti, S, Bujie, Z, Bystrom, M, Capitanu, B, Carvalho-Silva, D, Chardon, P, Chen, C, Cheng, R, Choi, S-H, Chow, W, Clark, RC, Clee, C, Crooijmans, RPMA, Dawson, HD, Dehais, P, De Sapio, F, Dibbits, B, Drou, N, Du, Z-Q, Eversole, K, Fadista, J, Fairley, S, Faraut, T, Faulkner, GJ, Fowler, KE, Fredholm, M, Fritz, E, Gilbert, JGR, Giuffra, E, Gorodkin, J, Griffin, DK, Harrow, JL, Hayward, A, Howe, K, Hu, Z-L, Humphray, SJ, Hunt, T, Hornshøj, H, Jeon, J-T, Jern, P, Jones, M, Jurka, J, Kanamori, H, Kapetanovic, R, Kim, J, Kim, J-H, Kim, K-W, Kim, T-H, Larson, G, Lee, K, Lee, K-T, Leggett, R, Lewin, HA, Li, Y, Liu, W, Loveland, JE, Lu, Y, Lunney, JK, Ma, J, Madsen, O, Mann, K, Matthews, L, McLaren, S, Morozumi, T, Murtaugh, MP, Narayan, J, Nguyen, DT, Ni, P, Oh, S-J, Onteru, S, Panitz, F, Park, E-W, Park, H-S, Pascal, G, Paudel, Y, Perez-Enciso, M, Ramirez-Gonzalez, R, Reecy, JM, Rodriguez-Zas, S, Rohrer, GA, Rund, L, Sang, Y, Schachtschneider, K, Schraiber, JG, Schwartz, J, Scobie, L, Scott, C, Searle, S, Servin, B, Southey, BR, Sperber, G, Stadler, P, Sweedler, JV, Tafer, H, Thomsen, B, Wali, R, Wang, J, Wang, J, White, S, Xu, X, Yerle, M, Zhang, G, Zhang, J, Zhang, J, Zhao, S, Rogers, J, Churcher, C & Schook, LB 2012, 'Analyses of pig genomes provide insight into porcine demography and evolution', Nature, vol. 491, no. 7424, pp. 393-398. https://doi.org/10.1038/nature11622
Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF et al. Analyses of pig genomes provide insight into porcine demography and evolution. Nature. 2012 Nov 15;491(7424):393-398. https://doi.org/10.1038/nature11622
Groenen, Martien A M ; Archibald, Alan L ; Uenishi, Hirohide ; Tuggle, Christopher K ; Takeuchi, Yasuhiro ; Rothschild, Max F ; Rogel-Gaillard, Claire ; Park, Chankyu ; Milan, Denis ; Megens, Hendrik-Jan ; Li, Shengting ; Larkin, Denis M ; Kim, Heebal ; Frantz, Laurent A F ; Caccamo, Mario ; Ahn, Hyeonju ; Aken, Bronwen L ; Anselmo, Anna ; Anthon, Christian ; Auvil, Loretta ; Badaoui, Bouabid ; Beattie, Craig W ; Bendixen, Christian ; Berman, Daniel ; Blecha, Frank ; Blomberg, Jonas ; Bolund, Lars ; Bosse, Mirte ; Botti, Sara ; Bujie, Zhan ; Bystrom, Megan ; Capitanu, Boris ; Carvalho-Silva, Denise ; Chardon, Patrick ; Chen, Celine ; Cheng, Ryan ; Choi, Sang-Haeng ; Chow, William ; Clark, Richard C ; Clee, Christopher ; Crooijmans, Richard P M A ; Dawson, Harry D ; Dehais, Patrice ; De Sapio, Fioravante ; Dibbits, Bert ; Drou, Nizar ; Du, Zhi-Qiang ; Eversole, Kellye ; Fadista, João ; Fairley, Susan ; Faraut, Thomas ; Faulkner, Geoffrey J ; Fowler, Katie E ; Fredholm, Merete ; Fritz, Eric ; Gilbert, James G R ; Giuffra, Elisabetta ; Gorodkin, Jan ; Griffin, Darren K ; Harrow, Jennifer L ; Hayward, Alexander ; Howe, Kerstin ; Hu, Zhi-Liang ; Humphray, Sean J ; Hunt, Toby ; Hornshøj, Henrik ; Jeon, Jin-Tae ; Jern, Patric ; Jones, Matthew ; Jurka, Jerzy ; Kanamori, Hiroyuki ; Kapetanovic, Ronan ; Kim, Jaebum ; Kim, Jae-Hwan ; Kim, Kyu-Won ; Kim, Tae-Hun ; Larson, Greger ; Lee, Kyooyeol ; Lee, Kyung-Tai ; Leggett, Richard ; Lewin, Harris A ; Li, Yingrui ; Liu, Wansheng ; Loveland, Jane E ; Lu, Yao ; Lunney, Joan K ; Ma, Jian ; Madsen, Ole ; Mann, Katherine ; Matthews, Lucy ; McLaren, Stuart ; Morozumi, Takeya ; Murtaugh, Michael P ; Narayan, Jitendra ; Nguyen, Dinh Truong ; Ni, Peixiang ; Oh, Song-Jung ; Onteru, Suneel ; Panitz, Frank ; Park, Eung-Woo ; Park, Hong-Seog ; Pascal, Geraldine ; Paudel, Yogesh ; Perez-Enciso, Miguel ; Ramirez-Gonzalez, Ricardo ; Reecy, James M ; Rodriguez-Zas, Sandra ; Rohrer, Gary A ; Rund, Lauretta ; Sang, Yongming ; Schachtschneider, Kyle ; Schraiber, Joshua G ; Schwartz, John ; Scobie, Linda ; Scott, Carol ; Searle, Stephen ; Servin, Bertrand ; Southey, Bruce R ; Sperber, Goran ; Stadler, Peter ; Sweedler, Jonathan V ; Tafer, Hakim ; Thomsen, Bo ; Wali, Rashmi ; Wang, Jian ; Wang, Jun ; White, Simon ; Xu, Xun ; Yerle, Martine ; Zhang, Guojie ; Zhang, Jianguo ; Zhang, Jie ; Zhao, Shuhong ; Rogers, Jane ; Churcher, Carol ; Schook, Lawrence B. / Analyses of pig genomes provide insight into porcine demography and evolution. In: Nature. 2012 ; Vol. 491, No. 7424. pp. 393-398.
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abstract = "For 10,000 years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ~1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.",
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AU - Archibald, Alan L

AU - Uenishi, Hirohide

AU - Tuggle, Christopher K

AU - Takeuchi, Yasuhiro

AU - Rothschild, Max F

AU - Rogel-Gaillard, Claire

AU - Park, Chankyu

AU - Milan, Denis

AU - Megens, Hendrik-Jan

AU - Li, Shengting

AU - Larkin, Denis M

AU - Kim, Heebal

AU - Frantz, Laurent A F

AU - Caccamo, Mario

AU - Ahn, Hyeonju

AU - Aken, Bronwen L

AU - Anselmo, Anna

AU - Anthon, Christian

AU - Auvil, Loretta

AU - Badaoui, Bouabid

AU - Beattie, Craig W

AU - Bendixen, Christian

AU - Berman, Daniel

AU - Blecha, Frank

AU - Blomberg, Jonas

AU - Bolund, Lars

AU - Bosse, Mirte

AU - Botti, Sara

AU - Bujie, Zhan

AU - Bystrom, Megan

AU - Capitanu, Boris

AU - Carvalho-Silva, Denise

AU - Chardon, Patrick

AU - Chen, Celine

AU - Cheng, Ryan

AU - Choi, Sang-Haeng

AU - Chow, William

AU - Clark, Richard C

AU - Clee, Christopher

AU - Crooijmans, Richard P M A

AU - Dawson, Harry D

AU - Dehais, Patrice

AU - De Sapio, Fioravante

AU - Dibbits, Bert

AU - Drou, Nizar

AU - Du, Zhi-Qiang

AU - Eversole, Kellye

AU - Fadista, João

AU - Fairley, Susan

AU - Faraut, Thomas

AU - Faulkner, Geoffrey J

AU - Fowler, Katie E

AU - Fredholm, Merete

AU - Fritz, Eric

AU - Gilbert, James G R

AU - Giuffra, Elisabetta

AU - Gorodkin, Jan

AU - Griffin, Darren K

AU - Harrow, Jennifer L

AU - Hayward, Alexander

AU - Howe, Kerstin

AU - Hu, Zhi-Liang

AU - Humphray, Sean J

AU - Hunt, Toby

AU - Hornshøj, Henrik

AU - Jeon, Jin-Tae

AU - Jern, Patric

AU - Jones, Matthew

AU - Jurka, Jerzy

AU - Kanamori, Hiroyuki

AU - Kapetanovic, Ronan

AU - Kim, Jaebum

AU - Kim, Jae-Hwan

AU - Kim, Kyu-Won

AU - Kim, Tae-Hun

AU - Larson, Greger

AU - Lee, Kyooyeol

AU - Lee, Kyung-Tai

AU - Leggett, Richard

AU - Lewin, Harris A

AU - Li, Yingrui

AU - Liu, Wansheng

AU - Loveland, Jane E

AU - Lu, Yao

AU - Lunney, Joan K

AU - Ma, Jian

AU - Madsen, Ole

AU - Mann, Katherine

AU - Matthews, Lucy

AU - McLaren, Stuart

AU - Morozumi, Takeya

AU - Murtaugh, Michael P

AU - Narayan, Jitendra

AU - Nguyen, Dinh Truong

AU - Ni, Peixiang

AU - Oh, Song-Jung

AU - Onteru, Suneel

AU - Panitz, Frank

AU - Park, Eung-Woo

AU - Park, Hong-Seog

AU - Pascal, Geraldine

AU - Paudel, Yogesh

AU - Perez-Enciso, Miguel

AU - Ramirez-Gonzalez, Ricardo

AU - Reecy, James M

AU - Rodriguez-Zas, Sandra

AU - Rohrer, Gary A

AU - Rund, Lauretta

AU - Sang, Yongming

AU - Schachtschneider, Kyle

AU - Schraiber, Joshua G

AU - Schwartz, John

AU - Scobie, Linda

AU - Scott, Carol

AU - Searle, Stephen

AU - Servin, Bertrand

AU - Southey, Bruce R

AU - Sperber, Goran

AU - Stadler, Peter

AU - Sweedler, Jonathan V

AU - Tafer, Hakim

AU - Thomsen, Bo

AU - Wali, Rashmi

AU - Wang, Jian

AU - Wang, Jun

AU - White, Simon

AU - Xu, Xun

AU - Yerle, Martine

AU - Zhang, Guojie

AU - Zhang, Jianguo

AU - Zhang, Jie

AU - Zhao, Shuhong

AU - Rogers, Jane

AU - Churcher, Carol

AU - Schook, Lawrence B

PY - 2012/11/15

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N2 - For 10,000 years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ~1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.

AB - For 10,000 years pigs and humans have shared a close and complex relationship. From domestication to modern breeding practices, humans have shaped the genomes of domestic pigs. Here we present the assembly and analysis of the genome sequence of a female domestic Duroc pig (Sus scrofa) and a comparison with the genomes of wild and domestic pigs from Europe and Asia. Wild pigs emerged in South East Asia and subsequently spread across Eurasia. Our results reveal a deep phylogenetic split between European and Asian wild boars ~1 million years ago, and a selective sweep analysis indicates selection on genes involved in RNA processing and regulation. Genes associated with immune response and olfaction exhibit fast evolution. Pigs have the largest repertoire of functional olfactory receptor genes, reflecting the importance of smell in this scavenging animal. The pig genome sequence provides an important resource for further improvements of this important livestock species, and our identification of many putative disease-causing variants extends the potential of the pig as a biomedical model.

U2 - 10.1038/nature11622

DO - 10.1038/nature11622

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VL - 491

SP - 393

EP - 398

JO - Nature

JF - Nature

SN - 0028-0836

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