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      Analyses of pig genomes provide insight into porcine demography and evolution

      research-article
      1 , 2 , 3 , 4 , 5 , 4 , 6 , 7 , 8 , 1 , 9 , 10 , 11 , 12 , 1 , 13 , 12 , 14 , 15 , 16 , 17 , 15 , 18 , 19 , 20 , 21 , 22 , 9 , 10 , 1 , 15 , 19 , 4 , 17 , 23 , 6 , 24 , 4 , 25 , 14 , 14 , 14 , 1 , 24 , 8 , 2 , 1 , 13 , 4 , 26 , 19 , 55 ,   14 , 8 , 2 , 55 , 27 , 16 , 4 , 14 , 6 , 15 , 16 , 27 , 14 , 28 ,   14 , 4 , 14 , 55 , 14 , 19 , 29 , 28 , 14 , 30 , 3 , 31 , 2 , 7 , 32 , 33 , 34 , 35 , 36 , 7 , 35 , 13 , 37 , 9 , 38 , 14 , 9 , 20 , 39 , 1 , 20 , 55 , 14 , 14 , 31 , 40 , 11 , 7 , 9 , 41 , 4 , 19 , 35 , 25 , 42 , 1 , 43 , 13 , 4 , 44 , 45 , 44 , 21 , 44 , 46 , 40 , 47 , 14 , 14 ,   8 , 44 , 48 , 49 , 50 , 49 , 19 , 47 , 9 , 9 , 51 , 14 , 9 , 8 , 9 , 52 , 9 , 53 , 53 , 13 , 14 , 54
      Nature
      Nature Publishing Group UK
      Sequencing, Genome evolution

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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.

          Supplementary information

          The online version of this article (doi:10.1038/nature11622) contains supplementary material, which is available to authorized users.

          Abstract

          This study presents the assembly and analysis of the genome sequence of a female domestic Duroc pig and a comparison with the genomes of wild and domestic pigs from Europe and Asia; the results shed light on the evolutionary relationship between European and Asian wild boars.

          Supplementary information

          The online version of this article (doi:10.1038/nature11622) contains supplementary material, which is available to authorized users.

          Bringing home the bacon: the pig genome

          The domestic pig ( Sus scrofa) is an important livestock species, its genome shaped by thousands of years of domestication and, latterly, sophisticated breeding practices. A high-quality draft genome sequence for a female domestic Duroc pig is published in this issue of Nature, under the auspices of the Swine Genome Sequencing Consortium. Comparisons of the genomes of wild and domestic pigs shed light on the evolutionary relationship between European and Asian wild boars, and reveal the rapid evolution of genes involved in the immune response and in olfaction. The authors identify many possible disease-causing gene variants, increasing the potential of the pig as a biomedical model, and present a detailed analysis of endogenous porcine retroviruses, knowledge of which is important for the possible use of pigs in xenotransplantation.

          Supplementary information

          The online version of this article (doi:10.1038/nature11622) contains supplementary material, which is available to authorized users.

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          Most cited references39

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          Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.

          DAVID bioinformatics resources consists of an integrated biological knowledgebase and analytic tools aimed at systematically extracting biological meaning from large gene/protein lists. This protocol explains how to use DAVID, a high-throughput and integrated data-mining environment, to analyze gene lists derived from high-throughput genomic experiments. The procedure first requires uploading a gene list containing any number of common gene identifiers followed by analysis using one or more text and pathway-mining tools such as gene functional classification, functional annotation chart or clustering and functional annotation table. By following this protocol, investigators are able to gain an in-depth understanding of the biological themes in lists of genes that are enriched in genome-scale studies.
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            Inference of Human Population History From Whole Genome Sequence of A Single Individual

            The history of human population size is important to understanding human evolution. Various studies 1-5 have found evidence for a founder event (bottleneck) in East Asian and European populations associated with the human dispersal out-of-Africa event around 60 thousand years ago (kya) before present. However, these studies have to assume simplified demographic models with few parameters and do not precisely date the start and stop times of the bottleneck. Here, with fewer assumptions on population size changes, we present a more detailed history of human population sizes between approximately ten thousand to a million years ago, using the pairwise sequentially Markovian coalescent (PSMC) model applied to the complete diploid genome sequences of a Chinese male (YH) 6 , a Korean male (SJK) 7 , three European individuals (Venter 8 , NA12891 and NA12878 9 ) and two Yoruba males (NA18507 10 and NA19239). We infer that European and Chinese populations had very similar population size histories before 10–20kya. Both populations experienced a severe bottleneck between 10–60kya while African populations experienced a milder bottleneck from which they recovered earlier. All three populations have an elevated effective population size between 60–250kya, possibly due to a population structure 11 . We also infer that the differentiation of genetically modern humans may have started as early as 100–120kya 12 , but considerable genetic exchanges may still have occurred until 20–40kya.
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              A draft sequence of the Neandertal genome.

              Neandertals, the closest evolutionary relatives of present-day humans, lived in large parts of Europe and western Asia before disappearing 30,000 years ago. We present a draft sequence of the Neandertal genome composed of more than 4 billion nucleotides from three individuals. Comparisons of the Neandertal genome to the genomes of five present-day humans from different parts of the world identify a number of genomic regions that may have been affected by positive selection in ancestral modern humans, including genes involved in metabolism and in cognitive and skeletal development. We show that Neandertals shared more genetic variants with present-day humans in Eurasia than with present-day humans in sub-Saharan Africa, suggesting that gene flow from Neandertals into the ancestors of non-Africans occurred before the divergence of Eurasian groups from each other.
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                Author and article information

                Journal
                Nature
                Nature
                Nature
                Nature Publishing Group UK (London )
                0028-0836
                1476-4687
                14 November 2012
                14 November 2012
                2012
                : 491
                : 7424
                : 393-398
                Affiliations
                [1 ]GRID grid.4818.5, ISNI 0000 0001 0791 5666, Animal Breeding and Genomics Centre, Wageningen University, De Elst 1, 6708 WD, Wageningen, The Netherlands., ; ,
                [2 ]GRID grid.4305.2, ISNI 0000 0004 1936 7988, The Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian EH25 9RG, UK., ; ,
                [3 ]GRID grid.410590.9, ISNI 0000 0001 0699 0373, National Institute of Agrobiological Sciences, 2-1-2 Kannondai, Tsukuba, Ibaraki 305-8602, Japan., ; ,
                [4 ]GRID grid.34421.30, ISNI 0000 0004 1936 7312, Department of Animal Science and Center for Integrated Animal Genomics, , Iowa State University, 2255 Kildee Hall, Ames 50011, USA., ; ,
                [5 ]GRID grid.83440.3b, ISNI 0000000121901201, Division of Infection & Immunity, , MRC/UCL Centre for Medical Molecular Virology and Wohl Virion Centre, University College London, Cruciform Building, Gower Street, London WC1E 6BT, UK., ; ,
                [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., ,
                [7 ]GRID grid.258676.8, ISNI 0000 0004 0532 8339, Department of Animal Biotechnology, , Konkuk University, 1 Hwayang-dong, Kwangjin-gu, Seoul 143-701, South Korea., ; ,
                [8 ]GRID grid.419081.5, ISNI 0000 0004 0427 456X, INRA, Laboratoire de Génétique Cellulaire, Chemin de Borde-Rouge, Auzeville, 31320 Castanet Tolosan, France., ; ,
                [9 ]GRID grid.21155.32, ISNI 0000 0001 2034 1839, BGI-Shenzhen, ; Shenzhen, 518083 China
                [10 ]GRID grid.7048.b, ISNI 0000 0001 1956 2722, Department of Biomedicine, , Aarhus University, ; Aarhus C, DK-8000 Denmark
                [11 ]GRID grid.8186.7, ISNI 0000000121682483, Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Penglais Campus, Aberystwyth, Ceredigion SY23 3DA, UK., ; ,
                [12 ]GRID grid.31501.36, ISNI 0000 0004 0470 5905, Department of Agricultural Biotechnology and C&K Genomics, , Seoul National University, Gwanakgu, Seoul 151-742, South Korea., ; ,
                [13 ]The Genome Analysis Centre, Norwich Research Park, Norwich, NR4 7UH UK
                [14 ]GRID grid.10306.34, ISNI 0000 0004 0606 5382, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridgeshire CB10 1SA, UK., ; ,
                [15 ]GRID grid.425375.2, ISNI 0000 0004 0604 0732, Parco Tecnologico Padano, Via Einstein, Loc. C. Codazza, 26900 Lodi, Italy., ; ,
                [16 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, Center for non-coding RNA in Technology and Health, IBHV University of Copenhagen, Frederiksberg, ; Denmark
                [17 ]GRID grid.35403.31, ISNI 0000 0004 1936 9991, Illinois Informatics Institute, University of Illinois, ; Urbana, 61801 Illinois USA
                [18 ]GRID grid.185648.6, ISNI 0000 0001 2175 0319, Department of Surgery, , University of Illinois, ; Chicago, 60612 Illinois USA
                [19 ]GRID grid.7048.b, ISNI 0000 0001 1956 2722, Department of Molecular Biology and Genetics, , Aarhus University, ; Tjele, DK-8830 Denmark
                [20 ]GRID grid.463419.d, ISNI 0000 0004 0404 0958, USDA ARS BARC Animal Parasitic Diseases Laboratory, ; Beltsville, 20705 Maryland USA
                [21 ]GRID grid.36567.31, ISNI 0000 0001 0737 1259, Department of Anatomy and Physiology, , College of Veterinary Medicine, Kansas State University, ; Manhattan, 66506 Kansas USA
                [22 ]Department of Medical Sciences, Clinical Virology, Uppsala University, Building D1, Academic Hospital, 751 85 Uppsala, Sweden., ,
                [23 ]GRID grid.225360.0, ISNI 0000 0000 9709 7726, European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, ; Cambridgeshire, CB10 1SD UK
                [24 ]GRID grid.463419.d, ISNI 0000 0004 0404 0958, United States Department of Agriculture, , Diet, Genomics, Immunology Laboratory, Beltsville Human Nutrition Research Center, BARC-East 10300 Baltimore Ave Beltsville, Maryland 20705, USA., ; ,
                [25 ]GRID grid.249967.7, ISNI 0000 0004 0636 3099, Korean Research Institute of Bioscience and Biotechnology, 125 Gwahak ro, Yuseong gu, Daejeon 305-806, South Korea., ; ,
                [26 ]GRID grid.498288.7, ISNI 0000 0004 0615 5951, Eversole Associates and the Alliance for Animal Genome Research, 5207 Wyoming Road, Bethesda, Maryland 20816, USA., ; ,
                [27 ]GRID grid.9759.2, ISNI 0000 0001 2232 2818, School of Biosciences, The University of Kent, Giles Lane, Canterbury, ; Kent, CT2 7NJ UK
                [28 ]Department of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, BMC, Box 582, SE75123 Uppsala, Sweden., ,
                [29 ]GRID grid.256681.e, ISNI 0000 0001 0661 1492, Department of Animal Sciences, , College of Agriculture and Life Sciences, Gyeongsang National University, Jinju 660-701, South Korea., ; ,
                [30 ]GRID grid.492326.8, ISNI 0000 0004 0444 3001, Genetic Information Research Institute, 1925 Landings Drive, ; Mountain View, 94043 California USA
                [31 ]Institute of Japan Association for Techno-innovation in Agriculture, Forestry and Fisheries, 446-1 Ippaizuka, Kamiyokoba, Tsukuba, Ibaraki 305-0854, Japan., ,
                [32 ]GRID grid.35403.31, ISNI 0000 0004 1936 9991, Institute for Genomic Biology, University of Illinois, ; Urbana, 61801 Illinois USA
                [33 ]GRID grid.420186.9, ISNI 0000 0004 0636 2782, Animal Genetic Resources Station, National Institute of Animal Science, RDA, San 4, Yongsanri, Unbong eup, Namwon 590-832, South Korea., ; ,
                [34 ]C&K Genomics, Gwanakgu, Seoul, 151-742 South Korea
                [35 ]GRID grid.420186.9, ISNI 0000 0004 0636 2782, Animal Genomics and Bioinformatics Division, , National Institute of Animal Science, RDA, 77 Chuksan gil, Kwonsun gu, Suwon 441-706, South Korea., ; ,
                [36 ]GRID grid.8250.f, ISNI 0000 0000 8700 0572, Department of Archaeology, , Durham Evolution and Ancient DNA, Durham University, ; Durham, DH1 3LE UK
                [37 ]GRID grid.27860.3b, ISNI 0000 0004 1936 9684, Department of Evolution and Ecology, , The UC Davis Genome Center, University of California, ; Davis, 95618 California USA
                [38 ]GRID grid.29857.31, ISNI 0000 0001 2097 4281, 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., ; ,
                [39 ]GRID grid.35403.31, ISNI 0000 0004 1936 9991, Department of Bioengineering and Institute for Genomic Biology, , University of Illinois, ; Urbana, 61801 Illinois USA
                [40 ]GRID grid.17635.36, ISNI 0000000419368657, Department of Veterinary and Biomedical Sciences, , University of Minnesota, 1971 Commonwealth Avenue, St Paul, Minnesota 55108, USA., ; ,
                [41 ]GRID grid.411277.6, ISNI 0000 0001 0725 5207, Jeju National University, 102 Jejudaehakno, Jeju 690-756, South Korea., ; ,
                [42 ]GRID grid.12366.30, ISNI 0000 0001 2182 6141, INRA UMR85/CNRS UMR7247 Physiologie de la Reproduction et des Comportements/IFCE, F-37380 Nouzilly, France and Université François Rabelais de Tours, ; Tours, F-37041 France
                [43 ]GRID grid.7080.f, ICREA, Centre for Research in Agricultural Genomics (CRAG) and Facultat de Veterinaria UAB, Campus Universitat Autonoma Barcelona, ; Bellaterra, E-08193 Spain
                [44 ]GRID grid.35403.31, ISNI 0000 0004 1936 9991, Department of Animal Sciences, , University of Illinois, ; Urbana, 61801 Illinois USA
                [45 ]GRID grid.417548.b, ISNI 0000 0004 0478 6311, USDA, ARS, US Meat Animal Research Center, Clay Center, ; Nebraska, 68933 USA
                [46 ]GRID grid.47840.3f, ISNI 0000 0001 2181 7878, Department of Integrative Biology, , University of California, ; Berkeley, 94720-3140 California USA
                [47 ]GRID grid.5214.2, ISNI 0000 0001 0669 8188, Department of Life Sciences, , Glasgow Caledonian University, ; Glasgow, G4 0BA UK
                [48 ]GRID grid.8993.b, ISNI 0000 0004 1936 9457, Department of Neuroscience, , Biomedical Centre, Uppsala University, PO Box 593, 751 24 Uppsala, Sweden., ; ,
                [49 ]Department of Computer Science, Bioinformatics Group, Interdisciplinary Center for Bioinformatics, Universität Leipzig, Leipzig, Germany
                [50 ]GRID grid.35403.31, ISNI 0000 0004 1936 9991, Department of Chemistry, , University of Illinois, ; Urbana, 61801 Illinois USA
                [51 ]GRID grid.5254.6, ISNI 0000 0001 0674 042X, Novo Nordisk Foundation Center for Basic Metabolic Research and Department of Biology, , University of Copenhagen, ; Copenhagen, DK-2200 Denmark
                [52 ]BGI-Europe, DK-2200 Copenhagen N, Denmark., ,
                [53 ]GRID grid.35155.37, ISNI 0000 0004 1790 4137, Key Lab of Animal Genetics, Breeding, and Reproduction of Ministry Education, Huazhong Agricultural University, Wuhan 430070 PR China, Huazhong Agricultural University, Wuhan 430070, China., ; ,
                [54 ]GRID grid.35403.31, ISNI 0000 0004 1936 9991, Department of Animal Sciences and Institute for Genomic Biology, , University of Illinois, Urbana, Illinois 61801, USA., ; ,
                [55 ]Present Address: 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.)., ,
                Article
                BFnature11622
                10.1038/nature11622
                3566564
                23151582
                9bc8563c-dd46-43c7-a2b4-c5e80f0b57ae
                © The Author(s) 2012

                This article is distributed under the terms of the Creative Commons Attribution-Non-Commercial-Share Alike licence ( http://creativecommons.org/licenses/by-nc-sa/3.0/).

                History
                : 16 June 2012
                : 27 September 2012
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                © Springer Nature Limited 2012

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                sequencing,genome evolution
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                sequencing, genome evolution

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