14 Nov 2012

Analyses of pig genomes provide insight into porcine demography and evolution (Nature, abstract, edited)

[Source: Nature, full text: (LINK). Abstract, edited.]

Analyses of pig genomes provide insight into porcine demography and evolution

Martien A. M. Groenen,1, 56; Alan L. Archibald,2, 56; Hirohide Uenishi,3; Christopher K. Tuggle,4; Yasuhiro Takeuchi,5; Max F. Rothschild,4; Claire Rogel-Gaillard,6; Chankyu Park7; Denis Milan,8; Hendrik-Jan Megens,1; Shengting Li,9, 10; Denis M. Larkin,11; Heebal Kim,12; Laurent A. F. Frantz,1; Mario Caccamo,13; Hyeonju Ahn,12; Bronwen L. Aken,14; Anna Anselmo,15; Christian Anthon,16; Loretta Auvil,17; Bouabid Badaoui,15; Craig W. Beattie,18; Christian Bendixen,19; Daniel Berman,20; Frank Blecha,21; Jonas Blomberg,22; Lars Bolund,9, 10; Mirte Bosse,1; Sara Botti,15; Zhan Bujie,19; Megan Bystrom,4; Boris Capitanu,17; Denise Carvalho-Silva,23; Patrick Chardon,6; Celine Chen,24; Ryan Cheng,4; Sang-Haeng Choi,25; William Chow,14; Richard C. Clark,14; Christopher Clee,14; Richard P. M. A. Crooijmans,1; Harry D. Dawson,24; Patrice Dehais,8; Fioravante De Sapio,2; Bert Dibbits,1; Nizar Drou,13; Zhi-Qiang Du,4; Kellye Eversole,26; João Fadista,19, 55; Susan Fairley,14; Thomas Faraut,8; Geoffrey J. Faulkner,2, 55; Katie E. Fowler,27; Merete Fredholm,16; Eric Fritz,4; James G. R. Gilbert,14; Elisabetta Giuffra,6, 15; Jan Gorodkin,16; Darren K. Griffin,27; Jennifer L. Harrow,14; Alexander Hayward,28; Kerstin Howe,14; Zhi-Liang Hu,4; Sean J. Humphray,14, 55; Toby Hunt,14; Henrik Hornshøj,19; Jin-Tae Jeon,29, 57; Patric Jern,28; Matthew Jones,14; Jerzy Jurka,30; Hiroyuki Kanamori,3, 31; Ronan Kapetanovic,2; Jaebum Kim,7, 32; Jae-Hwan Kim,33; Kyu-Won Kim,34; Tae-Hun Kim,35; Greger Larson,36; Kyooyeol Lee,7; Kyung-Tai Lee,35; Richard Leggett,13; Harris A. Lewin,37; Yingrui Li,9; Wansheng Liu,38; Jane E. Loveland,14; Yao Lu,9; Joan K. Lunney,20; Jian Ma,39; Ole Madsen,1; Katherine Mann,20, 55; Lucy Matthews,14; Stuart McLaren,14; Takeya Morozumi,31; Michael P. Murtaugh,40; Jitendra Narayan,11; Dinh Truong Nguyen,7; Peixiang Ni,9; Song-Jung Oh,41; Suneel Onteru,4; Frank Panitz,19; Eung-Woo Park,35; Hong-Seog Park,25; Geraldine Pascal,42; Yogesh Paudel,1; Miguel Perez-Enciso,43; Ricardo Ramirez-Gonzalez,13; James M. Reecy,4; Sandra Rodriguez-Zas,44; Gary A. Rohrer,45; Lauretta Rund,44; Yongming Sang,21; Kyle Schachtschneider,44; Joshua G. Schraiber,46; John Schwartz,40; Linda Scobie,47; Carol Scott,14; Stephen Searle,14; Bertrand Servin,8; Bruce R. Southey,44; Goran Sperber,48; Peter Stadler,49; Jonathan V. Sweedler,50; Hakim Tafer,49; Bo Thomsen,19; Rashmi Wali,47; Jian Wang,9; Jun Wang,9, 51; Simon White,14; Xun Xu,9; Martine Yerle,8; Guojie Zhang,9, 52; Jianguo Zhang,9; Jie Zhang,53; Shuhong Zhao,53; Jane Rogers,13; Carol Churcher14; & Lawrence B. Schook54

Journal name: Nature Volume: 491, Pages: 393–398 - Date published: (15 November 2012)

DOI: doi:10.1038/nature11622

Received 16 June 2012  - Accepted 27 September 2012  - Published online 14 November 2012

 

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.

 

Primary authors

  1. These authors contributed equally to this work.
    • Martien A. M. Groenen &
    • Alan L. Archibald

Affiliations

  1. Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands.
    • Martien A. M. Groenen,
    • Hendrik-Jan Megens,
    • Laurent A. F. Frantz,
    • Mirte Bosse,
    • Richard P. M. A. Crooijmans,
    • Bert Dibbits,
    • Ole Madsen &
    • Yogesh Paudel
  2. The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK.
    • Alan L. Archibald,
    • Fioravante De Sapio,
    • Geoffrey J. Faulkner &
    • Ronan Kapetanovic
  3. National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan.
    • Hirohide Uenishi &
    • Hiroyuki Kanamori
  4. Department of Animal Science and Center for Integrated Animal Genomics, Iowa State University, 2255 Kildee Hall, Ames 50011, USA.
    • Christopher K. Tuggle,
    • Max F. Rothschild,
    • Megan Bystrom,
    • Ryan Cheng,
    • Zhi-Qiang Du,
    • Eric Fritz,
    • Zhi-Liang Hu,
    • Suneel Onteru &
    • James M. Reecy
  5. MRC/UCL Centre for Medical Molecular Virology and Wohl Virion Centre, Division of Infection & Immunity, University College London, Cruciform Building, Gower Street, London WC1E 6BT, UK.
    • Yasuhiro Takeuchi
  6. 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.
    • Claire Rogel-Gaillard,
    • Patrick Chardon &
    • Elisabetta Giuffra
  7. Department of Animal Biotechnology, Konkuk University, 1 Hwayang-dong, Kwangjin-gu, Seoul 143-701, South Korea.
    • Chankyu Park,
    • Jaebum Kim,
    • Kyooyeol Lee &
    • Dinh Truong Nguyen
  8. INRA, Laboratoire de Génétique Cellulaire, Chemin de Borde-Rouge, Auzeville, 31320 Castanet Tolosan, France.
    • Denis Milan,
    • Patrice Dehais,
    • Thomas Faraut,
    • Bertrand Servin &
    • Martine Yerle
  9. BGI-Shenzhen, Shenzhen 518083, China.
    • Shengting Li,
    • Lars Bolund,
    • Yingrui Li,
    • Yao Lu,
    • Peixiang Ni,
    • Jian Wang,
    • Jun Wang,
    • Xun Xu,
    • Guojie Zhang &
    • Jianguo Zhang
  10. Department of Biomedicine, Aarhus University, DK-8000 Aarhus C, Denmark.
    • Shengting Li &
    • Lars Bolund
  11. Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Penglais Campus, Aberystwyth, Ceredigion SY23 3DA, UK.
    • Denis M. Larkin &
    • Jitendra Narayan
  12. Department of Agricultural Biotechnology and C&K Genomics, Seoul National University, Gwanakgu, Seoul 151-742, South Korea.
    • Heebal Kim &
    • Hyeonju Ahn
  13. The Genome Analysis Centre, Norwich Research Park, Norwich NR4 7UH, UK.
    • Mario Caccamo,
    • Nizar Drou,
    • Richard Leggett,
    • Ricardo Ramirez-Gonzalez &
    • Jane Rogers
  14. Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK.
    • Bronwen L. Aken,
    • William Chow,
    • Richard C. Clark,
    • Christopher Clee,
    • Susan Fairley,
    • James G. R. Gilbert,
    • Jennifer L. Harrow,
    • Kerstin Howe,
    • Sean J. Humphray,
    • Toby Hunt,
    • Matthew Jones,
    • Jane E. Loveland,
    • Lucy Matthews,
    • Stuart McLaren,
    • Carol Scott,
    • Stephen Searle,
    • Simon White &
    • Carol Churcher
  15. Parco Tecnologico Padano, Via Einstein, Loc. C. Codazza, 26900 Lodi, Italy.
    • Anna Anselmo,
    • Bouabid Badaoui,
    • Sara Botti &
    • Elisabetta Giuffra
  16. Center for non-coding RNA in Technology and Health, IBHV University of Copenhagen, Frederiksberg, Denmark.
    • Christian Anthon,
    • Merete Fredholm &
    • Jan Gorodkin
  17. Illinois Informatics Institute, University of Illinois, Urbana, Illinois 61801, USA.
    • Loretta Auvil &
    • Boris Capitanu
  18. Department of Surgery, University of Illinois, Chicago, Illinois 60612, USA.
    • Craig W. Beattie
  19. Department of Molecular Biology and Genetics, Aarhus University, DK-8830 Tjele, Denmark.
    • Christian Bendixen,
    • Zhan Bujie,
    • João Fadista,
    • Henrik Hornshøj,
    • Frank Panitz &
    • Bo Thomsen
  20. USDA ARS BARC Animal Parasitic Diseases Laboratory, Beltsville, Maryland 20705, USA.
    • Daniel Berman,
    • Joan K. Lunney &
    • Katherine Mann
  21. Department of Anatomy and Physiology, College of Veterinary Medicine, Kansas State University, Manhattan, Kansas 66506, USA.
    • Frank Blecha &
    • Yongming Sang
  22. Clinical Virology, Department of Medical Sciences, Uppsala University, Building D1, Academic Hospital, 751 85 Uppsala, Sweden.
    • Jonas Blomberg
  23. European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SD, UK.
    • Denise Carvalho-Silva
  24. Diet, Genomics, Immunology Laboratory, Beltsville Human Nutrition Research Center, United States Department of Agriculture, BARC-East 10300 Baltimore Ave Beltsville, Maryland 20705, USA.
    • Celine Chen &
    • Harry D. Dawson
  25. Korean Research Institute of Bioscience and Biotechnology, 125 Gwahak ro, Yuseong gu, Daejeon 305-806, South Korea.
    • Sang-Haeng Choi &
    • Hong-Seog Park
  26. Eversole Associates and the Alliance for Animal Genome Research, 5207 Wyoming Road, Bethesda, Maryland 20816, USA.
    • Kellye Eversole
  27. School of Biosciences, The University of Kent, Giles Lane, Canterbury, Kent CT2 7NJ, UK.
    • Katie E. Fowler &
    • Darren K. Griffin
  28. Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, BMC, Box 582, SE75123 Uppsala, Sweden.
    • Alexander Hayward &
    • Patric Jern
  29. Department of Animal Sciences, College of Agriculture and Life Sciences, Gyeongsang National University, Jinju 660-701, South Korea.
    • Jin-Tae Jeon
  30. Genetic Information Research Institute, 1925 Landings Drive, Mountain View, California 94043, USA.
    • Jerzy Jurka
  31. Institute of Japan Association for Techno-innovation in Agriculture, Forestry and Fisheries, 446-1 Ippaizuka, Kamiyokoba, Tsukuba, Ibaraki 305-0854, Japan.
    • Hiroyuki Kanamori &
    • Takeya Morozumi
  32. Institute for Genomic Biology, University of Illinois, Urbana, Illinois 61801, USA.
    • Jaebum Kim
  33. Animal Genetic Resources Station, National Institute of Animal Science, RDA, San 4, Yongsanri, Unbong eup, Namwon 590-832, South Korea.
    • Jae-Hwan Kim
  34. C&K Genomics, Gwanakgu, Seoul 151-742, South Korea.
    • Kyu-Won Kim
  35. Animal Genomics and Bioinformatics Division, National Institute of Animal Science, RDA, 77 Chuksan gil, Kwonsun gu, Suwon 441-706, South Korea.
    • Tae-Hun Kim,
    • Kyung-Tai Lee &
    • Eung-Woo Park
  36. Durham Evolution and Ancient DNA, Department of Archaeology, Durham University, Durham DH1 3LE, UK.
    • Greger Larson
  37. Department of Evolution and Ecology, The UC Davis Genome Center, University of California, Davis, California 95618, USA.
    • Harris A. Lewin
  38. Department of Dairy and Animal Sciences, Center for Reproductive Biology and Health (CRBH), College of Agricultural Sciences, The Pennsylvania State University, 305 Henning Building, University Park, Pennsylvania 16802, USA.
    • Wansheng Liu
  39. Department of Bioengineering and Institute for Genomic Biology, University of Illinois, Urbana, Illinois 61801, USA.
    • Jian Ma
  40. Department of Veterinary and Biomedical Sciences, University of Minnesota, 1971 Commonwealth Avenue, St Paul, Minnesota 55108, USA.
    • Michael P. Murtaugh &
    • John Schwartz
  41. Jeju National University, 102 Jejudaehakno, Jeju 690-756, South Korea.
    • Song-Jung Oh
  42. INRA UMR85/CNRS UMR7247 Physiologie de la Reproduction et des Comportements/IFCE, F-37380 Nouzilly, France and Université François Rabelais de Tours, F-37041 Tours, France.
    • Geraldine Pascal
  43. ICREA, Centre for Research in Agricultural Genomics (CRAG) and Facultat de Veterinaria UAB, Campus Universitat Autonoma Barcelona, Bellaterra E-08193, Spain.
    • Miguel Perez-Enciso
  44. Department of Animal Sciences, University of Illinois, Urbana, Illinois 61801, USA.
    • Sandra Rodriguez-Zas,
    • Lauretta Rund,
    • Kyle Schachtschneider &
    • Bruce R. Southey
  45. USDA, ARS, US Meat Animal Research Center, Clay Center, Nebraska 68933, USA.
    • Gary A. Rohrer
  46. Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA.
    • Joshua G. Schraiber
  47. Department of Life Sciences, Glasgow Caledonian University, Glasgow G4 0BA, UK.
    • Linda Scobie &
    • Rashmi Wali
  48. Department of Neuroscience, Biomedical Centre, Uppsala University, PO Box 593, 751 24 Uppsala, Sweden.
    • Goran Sperber
  49. Bioinformatics Group, Department of Computer Science, Interdisciplinary Center for Bioinformatics, Universität Leipzig, Leipzig, Germany.
    • Peter Stadler &
    • Hakim Tafer
  50. Department of Chemistry, University of Illinois, Urbana, Illinois 61801, USA.
    • Jonathan V. Sweedler
  51. Novo Nordisk Foundation Center for Basic Metabolic Research and Department of Biology, University of Copenhagen, DK-2200 Copenhagen, Denmark.
    • Jun Wang
  52. BGI-Europe, DK-2200 Copenhagen N, Denmark.
    • Guojie Zhang
  53. Key Lab of Animal Genetics, Breeding, and Reproduction of Ministry Education, Huazhong Agricultural University, Wuhan 430070 PR China, Huazhong Agricultural University, Wuhan 430070, China.
    • Jie Zhang &
    • Shuhong Zhao
  54. Department of Animal Sciences and Institute for Genomic Biology, University of Illinois, Urbana, Illinois 61801, USA.
    • Lawrence B. Schook
  55. Present addresses: Lund University Diabetes Centre, CRC, Malmö University Hospital, SE-205 02 Malmö, Sweden (J.F.); Mater Medical Research Institute, and School of Biomedical Sciences, University of Queensland, Brisbane, 4072 Queensland, Australia (G.J.F.); Illumina Inc. Chesterford Research Park, Little Chesterford, Nr Saffron Walden, Essex CB10 1XL, UK (S.J.H.); Department of Molecular Microbiology, Washington University School of Medicine, Saint Louis, Missouri 63110, USA (K.M.).
    • João Fadista,
    • Geoffrey J. Faulkner,
    • Sean J. Humphray &
    • Katherine Mann
  56. Deceased.
    • Jin-Tae Jeon

Contributions

Manuscript main text: A.L.A., M.A.M.G., L.B.S., H.U., C.K.T., Y.T., M.F.R., C.P., S.L., D.M., H.-J.M., D.M.L., H.Ki., L.A.F.F., G.L.M.C.; project coordination: A.L.A., M.A.M.G., L.B.S., M.F.R., D.M., J.R., C.Chu., H.U., M.C., K.E.; project initiation: A.L.A., M.A.M.G., L.B.S., M.F.R., D.M., M.F., C.W.B., P.C., G.A.R., M.Y., J.R., L.B.; library preparation and sequencing: S.J.H., C.S., C.Cl., S.M., L.M., M.J., Y.Lu, X.X., P.N., Jia.Z., G.Z., A.L.A., R.C.C., T.M., H.Ka., K.-T.L., T.-H.K., H.-S.P., E.-W.P., J.-H.K., S.-H.C., S.-J.O., Ji.W., Ju.W., J.-T.J.; genome assembly: A.L.A., M.C., S.L., C.S., P.D., H.-J.M., H.U., D.M., B.S., T.F., Y.Li, N.D., R.R.-G., R.L., K.H., W.C.; repetitive DNA analysis: G.J.F. (leader), J.J., F.DeS., H.-J.M.; gene content and genome evolution: S.F., B.L.A., S.W., S.S.; conservation of synteny and evolutionary breakpoints: D.M.L. (leader), J.N., L.A., B.C., H.A.L., J.M., J.K., D.K.G., K.E.F.; speciation: L.A.F.F., M.A.M.G., O.M., H.-J.M., J.G.S.; divergence of Asian and European wild boar: H.-J.M., M.Bo., M.A.M.G., L.A.F.F.; annotation: S.S., B.L.A., T.M., C.K.T., Y.S., M.By., R.C., J.R., E.F., Z.-L.H., W.L., M.P.-E.; RNA analysis: O.M., R.P.M.A.C., H.U., C.A., H.T., B.T., P.S., M.F., J.G., C.B., F.P., H.H., Z.B., J.F.; neuropeptides: J.V.S., B.R.S., S.R.-Z.; pig domestication: L.A.F.F., R.P.M.A.C., H.-J.M., M.Bo., S.O., G.L., L.R., J.G.S.; population admixture: L.A.F.F., J.G.S.; biomedical models: B.D., L.R., K.S., M.A.M.G.; immune response: C.K.T., (co-leader) C.R.-G. (co-leader), H.D.D., J.E.L., A.A., B.B., J.S., D.B., F.B., M.By., S.B., C.Che., D.C.-S., R.C., E.F., E.G., J.G.R.G., J.L.H., T.H., Z.-L.H., R.K., J.K.L., K.M., M.P.M., T.M., G.P., J.M.R., J.S., H.U., Jie Z., S.Z.; olfactory and taste receptor analysis: C.P. (leader), D.T.N., K.L.; dN/dS analysis: H.Ki. (leader), H.A., K.-W.K.; PERV and retroviral insertions: C.R.-G., A.H., P.J., J.B., G.S., L.S., R.W., Y.T. (leader); segmental duplications: O.M., Y.P., Z.-Q.D., M.F.R.

Competing financial interests: The authors declare no competing financial interests.

The final assembly (Sscrofa10.2) has been deposited in the public sequence databases (GenBank/EMBL/DDBJ) under accession number AEMK01000000. The primary source of the Sscrofa10.2 assembly is the NCBI ftp site (ftp://ftp.ncbi.nih.gov/genbank/genomes/Eukaryotes/vertebrates_mammals/Sus_scrofa/Sscrofa10.2/). The chromosomes are CM000812–CM00830 and CM001155. They are built from 5,343 placed scaffolds, with GenBank accession numbers GL878569-GL882503 and JH114391-JH118402. The 4,562 unplaced scaffolds of Sscrofa10.2 have accessions in the ranges GL892100GL896682 and JH118403JH118999. Illumina sequences for the sequenced wild boars and individuals of the other breeds, aligned against build10.2, have been deposited in the European Nucleotide Archive (ENA) under project number ERP001813.

-

-------