Analyses of pig genomes provide insight into porcine demography and evolution

Martien A Groenen; Alan L. Archibald; Hirohide Uenishi; Christopher K. Tuggle; Yasuhiro Takeuchi; Max F. Rothschild; Claire Rogel-Gaillard; Chankyu Park; Dennis 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 Auvil; Bouabid Badaoui; Craig W. Beattie; Christian Bendixen; Daniel Berman; Frank Blecha; Jonas Blomberg; Lars Bolund; Mirte Bosse; Sara Botti; Bujie Zhan; 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 Jensen; Jin-Tae Jeon; Patric Jern; Matthew Jones; Jerzy Jurka; Hiroyuki Kanamori; Ronan Kapetanovic; Jaebum Kim; Jae-Hwan Kim; Kyu-Won Kim; Tai-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 Yerke; Guojie Zhang; Jianguo Zhang; Jie Zhang; Shuhong Zhao; Jane Rogers; Carol Churcher; Lawrence B.  Schook

doi:10.1038/nature11622

Analyses of pig genomes provide insight into porcine demography and evolution

Martien A Groenen, Alan L. Archibald, Hirohide Uenishi, Christopher K. Tuggle, Yasuhiro Takeuchi, Max F. Rothschild, Claire Rogel-Gaillard, Chankyu Park, Dennis 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, Bujie Zhan, 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 Jensen, Jin-Tae Jeon, Patric Jern, Matthew Jones, Jerzy Jurka, Hiroyuki Kanamori, Ronan Kapetanovic, Jaebum Kim, Jae-Hwan Kim, Kyu-Won Kim, Tai-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 Yerke, Guojie Zhang, Jianguo Zhang, Jie Zhang, Shuhong Zhao, Jane Rogers, Carol Churcher, Lawrence B. Schook

Department of Biology

815 Citations (Scopus)

Abstract

For 10,000a €‰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 language	English
Journal	Nature
Volume	491
Issue number	7424
Pages (from-to)	393-398
Number of pages	6
ISSN	0028-0836
DOIs	https://doi.org/10.1038/nature11622
Publication status	Published - 15 Nov 2012

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Groenen, M. A., Archibald, A. L., Uenishi, H., Tuggle, C. K., Takeuchi, Y., Rothschild, M. F., Rogel-Gaillard, C., Park, C., Milan, D., Megens, H.-J., Li, S., Larkin, D. M., Kim, H., Frantz, L. A. F., Caccamo, M., Ahn, H., Aken, B. L., Anselmo, A., Anthon, C., ... 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

Groenen, MA, 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, Zhan, B, 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, Sapio, FD, 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, Jensen, HH, 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, Yerke, 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

@article{dbdf769e917a431ba35b23f2a0d36594,

title = "Analyses of pig genomes provide insight into porcine demography and evolution",

abstract = "For 10,000a €‰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.",

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

year = "2012",

month = nov,

day = "15",

doi = "10.1038/nature11622",

language = "English",

volume = "491",

pages = "393--398",

journal = "Nature",

issn = "0028-0836",

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TY - JOUR

T1 - Analyses of pig genomes provide insight into porcine demography and evolution

AU - Groenen, Martien A

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, Dennis

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 - Zhan, Bujie

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 - Sapio, Fioravante De

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 - Jensen, Henrik Hornshøj

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, Tai-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 - Yerke, 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

Y1 - 2012/11/15

N2 - For 10,000a €‰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 10,000a €‰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

M3 - Journal article

C2 - 23151582

SN - 0028-0836

VL - 491

SP - 393

EP - 398

JO - Nature

JF - Nature

IS - 7424

ER -

Analyses of pig genomes provide insight into porcine demography and evolution

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