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 Auvil, Bouabid 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 and Lawrence B. Schook
Additional contact information
Martien A. M. Groenen: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Alan L. Archibald: The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK.
Hirohide Uenishi: National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan.
Christopher K. Tuggle: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Yasuhiro Takeuchi: MRC/UCL Centre for Medical Molecular Virology and Wohl Virion Centre, University College London, Cruciform Building, Gower Street, London WC1E 6BT, UK.
Max F. Rothschild: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Claire Rogel-Gaillard: INRA, Laboratory of Animal Genetics and Integrative Biology/AgroParisTech, Laboratory of Animal Genetics and Integrative Biology/CEA, DSV, IRCM, Laboratoire de Radiobiologie et Etude du Génome, Domaine de Vilvert, F-78350 Jouy-en-Josas, France.
Chankyu Park: Konkuk University, 1 Hwayang-dong, Kwangjin-gu, Seoul 143-701, South Korea.
Denis Milan: INRA, Laboratoire de Génétique Cellulaire, Chemin de Borde-Rouge, Auzeville, 31320 Castanet Tolosan, France.
Hendrik-Jan Megens: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Shengting Li: BGI-Shenzhen
Denis M. Larkin: Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Penglais Campus, Aberystwyth, Ceredigion SY23 3DA, UK.
Heebal Kim: Seoul National University, Gwanakgu, Seoul 151-742, South Korea.
Laurent A. F. Frantz: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Mario Caccamo: The Genome Analysis Centre, Norwich Research Park
Hyeonju Ahn: Seoul National University, Gwanakgu, Seoul 151-742, South Korea.
Bronwen L. Aken: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Anna Anselmo: Parco Tecnologico Padano, Via Einstein, Loc. C. Codazza, 26900 Lodi, Italy.
Christian Anthon: Center for non-coding RNA in Technology and Health, IBHV University of Copenhagen, Frederiksberg
Loretta Auvil: Illinois Informatics Institute, University of Illinois
Bouabid Badaoui: Parco Tecnologico Padano, Via Einstein, Loc. C. Codazza, 26900 Lodi, Italy.
Craig W. Beattie: University of Illinois
Christian Bendixen: Aarhus University
Daniel Berman: USDA ARS BARC Animal Parasitic Diseases Laboratory
Frank Blecha: College of Veterinary Medicine, Kansas State University
Jonas Blomberg: Clinical Virology, Uppsala University, Building D1, Academic Hospital, 751 85 Uppsala, Sweden.
Lars Bolund: BGI-Shenzhen
Mirte Bosse: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Sara Botti: Parco Tecnologico Padano, Via Einstein, Loc. C. Codazza, 26900 Lodi, Italy.
Zhan Bujie: Aarhus University
Megan Bystrom: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Boris Capitanu: Illinois Informatics Institute, University of Illinois
Denise Carvalho-Silva: European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton
Patrick Chardon: INRA, Laboratory of Animal Genetics and Integrative Biology/AgroParisTech, Laboratory of Animal Genetics and Integrative Biology/CEA, DSV, IRCM, Laboratoire de Radiobiologie et Etude du Génome, Domaine de Vilvert, F-78350 Jouy-en-Josas, France.
Celine Chen: Diet, Genomics, Immunology Laboratory, Beltsville Human Nutrition Research Center, BARC-East 10300 Baltimore Ave Beltsville, Maryland 20705, USA.
Ryan Cheng: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Sang-Haeng Choi: Korean Research Institute of Bioscience and Biotechnology, 125 Gwahak ro, Yuseong gu, Daejeon 305-806, South Korea.
William Chow: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Richard C. Clark: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Christopher Clee: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Richard P. M. A. Crooijmans: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Harry D. Dawson: Diet, Genomics, Immunology Laboratory, Beltsville Human Nutrition Research Center, BARC-East 10300 Baltimore Ave Beltsville, Maryland 20705, USA.
Patrice Dehais: INRA, Laboratoire de Génétique Cellulaire, Chemin de Borde-Rouge, Auzeville, 31320 Castanet Tolosan, France.
Fioravante De Sapio: The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK.
Bert Dibbits: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Nizar Drou: The Genome Analysis Centre, Norwich Research Park
Zhi-Qiang Du: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Kellye Eversole: Eversole Associates and the Alliance for Animal Genome Research, 5207 Wyoming Road, Bethesda, Maryland 20816, USA.
João Fadista: Aarhus University
Susan Fairley: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Thomas Faraut: INRA, Laboratoire de Génétique Cellulaire, Chemin de Borde-Rouge, Auzeville, 31320 Castanet Tolosan, France.
Geoffrey J. Faulkner: The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK.
Katie E. Fowler: School of Biosciences, The University of Kent, Giles Lane, Canterbury
Merete Fredholm: Center for non-coding RNA in Technology and Health, IBHV University of Copenhagen, Frederiksberg
Eric Fritz: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
James G. R. Gilbert: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Elisabetta Giuffra: INRA, Laboratory of Animal Genetics and Integrative Biology/AgroParisTech, Laboratory of Animal Genetics and Integrative Biology/CEA, DSV, IRCM, Laboratoire de Radiobiologie et Etude du Génome, Domaine de Vilvert, F-78350 Jouy-en-Josas, France.
Jan Gorodkin: Center for non-coding RNA in Technology and Health, IBHV University of Copenhagen, Frederiksberg
Darren K. Griffin: School of Biosciences, The University of Kent, Giles Lane, Canterbury
Jennifer L. Harrow: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Alexander Hayward: Science for Life Laboratory, Uppsala University, BMC, Box 582, SE75123 Uppsala, Sweden.
Kerstin Howe: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Zhi-Liang Hu: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Sean J. Humphray: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Toby Hunt: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Henrik Hornshøj: Aarhus University
Jin-Tae Jeon: College of Agriculture and Life Sciences, Gyeongsang National University, Jinju 660-701, South Korea.
Patric Jern: Science for Life Laboratory, Uppsala University, BMC, Box 582, SE75123 Uppsala, Sweden.
Matthew Jones: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Jerzy Jurka: Genetic Information Research Institute, 1925 Landings Drive
Hiroyuki Kanamori: National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan.
Ronan Kapetanovic: The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK.
Jaebum Kim: Konkuk University, 1 Hwayang-dong, Kwangjin-gu, Seoul 143-701, South Korea.
Jae-Hwan Kim: Animal Genetic Resources Station, National Institute of Animal Science, RDA, San 4, Yongsanri, Unbong eup, Namwon 590-832, South Korea.
Kyu-Won Kim: C&K Genomics, Gwanakgu
Tae-Hun Kim: National Institute of Animal Science, RDA, 77 Chuksan gil, Kwonsun gu, Suwon 441-706, South Korea.
Greger Larson: Durham Evolution and Ancient DNA, Durham University
Kyooyeol Lee: Konkuk University, 1 Hwayang-dong, Kwangjin-gu, Seoul 143-701, South Korea.
Kyung-Tai Lee: National Institute of Animal Science, RDA, 77 Chuksan gil, Kwonsun gu, Suwon 441-706, South Korea.
Richard Leggett: The Genome Analysis Centre, Norwich Research Park
Harris A. Lewin: The UC Davis Genome Center, University of California
Yingrui Li: BGI-Shenzhen
Wansheng Liu: Center for Reproductive Biology and Health (CRBH), College of Agricultural Sciences, The Pennsylvania State University, 305 Henning Building, University Park, Pennsylvania 16802, USA.
Jane E. Loveland: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Yao Lu: BGI-Shenzhen
Joan K. Lunney: USDA ARS BARC Animal Parasitic Diseases Laboratory
Jian Ma: University of Illinois
Ole Madsen: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Katherine Mann: USDA ARS BARC Animal Parasitic Diseases Laboratory
Lucy Matthews: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Stuart McLaren: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Takeya Morozumi: Institute of Japan Association for Techno-innovation in Agriculture, Forestry and Fisheries, 446-1 Ippaizuka, Kamiyokoba, Tsukuba, Ibaraki 305-0854, Japan.
Michael P. Murtaugh: University of Minnesota, 1971 Commonwealth Avenue, St Paul, Minnesota 55108, USA.
Jitendra Narayan: Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Penglais Campus, Aberystwyth, Ceredigion SY23 3DA, UK.
Dinh Truong Nguyen: Konkuk University, 1 Hwayang-dong, Kwangjin-gu, Seoul 143-701, South Korea.
Peixiang Ni: BGI-Shenzhen
Song-Jung Oh: Jeju National University, 102 Jejudaehakno, Jeju 690-756, South Korea.
Suneel Onteru: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Frank Panitz: Aarhus University
Eung-Woo Park: National Institute of Animal Science, RDA, 77 Chuksan gil, Kwonsun gu, Suwon 441-706, South Korea.
Hong-Seog Park: Korean Research Institute of Bioscience and Biotechnology, 125 Gwahak ro, Yuseong gu, Daejeon 305-806, South Korea.
Geraldine Pascal: INRA UMR85/CNRS UMR7247 Physiologie de la Reproduction et des Comportements/IFCE, F-37380 Nouzilly, France and Université François Rabelais de Tours
Yogesh Paudel: Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
Miguel Perez-Enciso: ICREA, Centre for Research in Agricultural Genomics (CRAG) and Facultat de Veterinaria UAB, Campus Universitat Autonoma Barcelona
Ricardo Ramirez-Gonzalez: The Genome Analysis Centre, Norwich Research Park
James M. Reecy: Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
Sandra Rodriguez-Zas: University of Illinois
Gary A. Rohrer: USDA, ARS, US Meat Animal Research Center, Clay Center
Lauretta Rund: University of Illinois
Yongming Sang: College of Veterinary Medicine, Kansas State University
Kyle Schachtschneider: University of Illinois
Joshua G. Schraiber: University of California
John Schwartz: University of Minnesota, 1971 Commonwealth Avenue, St Paul, Minnesota 55108, USA.
Linda Scobie: Glasgow Caledonian University
Carol Scott: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Stephen Searle: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Bertrand Servin: INRA, Laboratoire de Génétique Cellulaire, Chemin de Borde-Rouge, Auzeville, 31320 Castanet Tolosan, France.
Bruce R. Southey: University of Illinois
Goran Sperber: Biomedical Centre, Uppsala University, PO Box 593, 751 24 Uppsala, Sweden.
Peter Stadler: Bioinformatics Group, Interdisciplinary Center for Bioinformatics, Universität Leipzig
Jonathan V. Sweedler: University of Illinois
Hakim Tafer: Bioinformatics Group, Interdisciplinary Center for Bioinformatics, Universität Leipzig
Bo Thomsen: Aarhus University
Rashmi Wali: Glasgow Caledonian University
Jian Wang: BGI-Shenzhen
Jun Wang: BGI-Shenzhen
Simon White: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Xun Xu: BGI-Shenzhen
Martine Yerle: INRA, Laboratoire de Génétique Cellulaire, Chemin de Borde-Rouge, Auzeville, 31320 Castanet Tolosan, France.
Guojie Zhang: BGI-Shenzhen
Jianguo Zhang: BGI-Shenzhen
Jie Zhang: Key Lab of Animal Genetics, Breeding, and Reproduction of Ministry Education, Huazhong Agricultural University, Wuhan 430070 PR China, Huazhong Agricultural University, Wuhan 430070, China.
Shuhong Zhao: Key Lab of Animal Genetics, Breeding, and Reproduction of Ministry Education, Huazhong Agricultural University, Wuhan 430070 PR China, Huazhong Agricultural University, Wuhan 430070, China.
Jane Rogers: The Genome Analysis Centre, Norwich Research Park
Carol Churcher: Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
Lawrence B. Schook: University of Illinois, Urbana, Illinois 61801, USA.

Nature, 2012, vol. 491, issue 7424, 393-398

Abstract: 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.

Date: 2012
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DOI: 10.1038/nature11622

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