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      Worldwide Patterns of Ancestry, Divergence, and Admixture in Domesticated Cattle

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          Abstract

          The domestication and development of cattle has considerably impacted human societies, but the histories of cattle breeds and populations have been poorly understood especially for African, Asian, and American breeds. Using genotypes from 43,043 autosomal single nucleotide polymorphism markers scored in 1,543 animals, we evaluate the population structure of 134 domesticated bovid breeds. Regardless of the analytical method or sample subset, the three major groups of Asian indicine, Eurasian taurine, and African taurine were consistently observed. Patterns of geographic dispersal resulting from co-migration with humans and exportation are recognizable in phylogenetic networks. All analytical methods reveal patterns of hybridization which occurred after divergence. Using 19 breeds, we map the cline of indicine introgression into Africa. We infer that African taurine possess a large portion of wild African auroch ancestry, causing their divergence from Eurasian taurine. We detect exportation patterns in Asia and identify a cline of Eurasian taurine/indicine hybridization in Asia. We also identify the influence of species other than Bos taurus taurus and B. t. indicus in the formation of Asian breeds. We detect the pronounced influence of Shorthorn cattle in the formation of European breeds. Iberian and Italian cattle possess introgression from African taurine. American Criollo cattle originate from Iberia, and not directly from Africa with African ancestry inherited via Iberian ancestors. Indicine introgression into American cattle occurred in the Americas, and not Europe. We argue that cattle migration, movement and trading followed by admixture have been important forces in shaping modern bovine genomic variation.

          Author Summary

          The DNA of domesticated plants and animals contains information about how species were domesticated, exported, and bred by early farmers. Modern breeds were developed by lengthy and complex processes; however, our use of 134 breeds and new analytical models enabled us to reveal some of the processes that created modern cattle diversity. In Asia, Africa, North and South America, humpless ( Bos t. taurus or taurine) and humped ( Bos t. indicus or indicine) cattle were crossbred to produce hybrids adapted to the environment and local production systems. The history of Asian cattle involves the domestication and admixture of several species whereas African taurines arose through the introduction of domesticated Fertile Crescent taurines and their hybridization with wild African aurochs. African taurine genetic background is commonly observed among European Mediterranean breeds. The absence of indicine introgression within most European taurine breeds, but presence within three Italian breeds is consistent with at least two separate migration waves of cattle to Europe, one from the Middle East which captured taurines in which indicine introgression had already occurred and the second from western Africa into Spain with no indicine introgression. This second group seems to have radiated from Spain into the Mediterranean resulting in a cline of African taurine introgression into European taurines.

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          Most cited references 29

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          Development and Characterization of a High Density SNP Genotyping Assay for Cattle

          The success of genome-wide association (GWA) studies for the detection of sequence variation affecting complex traits in human has spurred interest in the use of large-scale high-density single nucleotide polymorphism (SNP) genotyping for the identification of quantitative trait loci (QTL) and for marker-assisted selection in model and agricultural species. A cost-effective and efficient approach for the development of a custom genotyping assay interrogating 54,001 SNP loci to support GWA applications in cattle is described. A novel algorithm for achieving a compressed inter-marker interval distribution proved remarkably successful, with median interval of 37 kb and maximum predicted gap of <350 kb. The assay was tested on a panel of 576 animals from 21 cattle breeds and six outgroup species and revealed that from 39,765 to 46,492 SNP are polymorphic within individual breeds (average minor allele frequency (MAF) ranging from 0.24 to 0.27). The assay also identified 79 putative copy number variants in cattle. Utility for GWA was demonstrated by localizing known variation for coat color and the presence/absence of horns to their correct genomic locations. The combination of SNP selection and the novel spacing algorithm allows an efficient approach for the development of high-density genotyping platforms in species having full or even moderate quality draft sequence. Aspects of the approach can be exploited in species which lack an available genome sequence. The BovineSNP50 assay described here is commercially available from Illumina and provides a robust platform for mapping disease genes and QTL in cattle.
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            Comprehensive polymorphism survey elucidates population structure of Saccharomyces cerevisiae.

            Comprehensive identification of polymorphisms among individuals within a species is essential both for studying the genetic basis of phenotypic differences and for elucidating the evolutionary history of the species. Large-scale polymorphism surveys have recently been reported for human, mouse and Arabidopsis thaliana. Here we report a nucleotide-level survey of genomic variation in a diverse collection of 63 Saccharomyces cerevisiae strains sampled from different ecological niches (beer, bread, vineyards, immunocompromised individuals, various fermentations and nature) and from locations on different continents. We hybridized genomic DNA from each strain to whole-genome tiling microarrays and detected 1.89 million single nucleotide polymorphisms, which were grouped into 101,343 distinct segregating sites. We also identified 3,985 deletion events of length >200 base pairs among the surveyed strains. We analysed the genome-wide patterns of nucleotide polymorphism and deletion variants, and measured the extent of linkage disequilibrium in S. cerevisiae. These results and the polymorphism resource we have generated lay the foundation for genome-wide association studies in yeast. We also examined the population structure of S. cerevisiae, providing support for multiple domestication events as well as insight into the origins of pathogenic strains.
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              Evidence for two independent domestications of cattle.

              The origin and taxonomic status of domesticated cattle are controversial. Zebu and taurine breeds are differentiated primarily by the presence or absence of a hump and have been recognized as separate species (Bos indicus and Bos taurus). However, the most widely held view is that both types of cattle derive from a single domestication event 8000-10,000 years ago. We have examined mtDNA sequences from representatives of six European (taurine) breeds, three Indian (zebu) breeds, and four African (three zebu, one taurine) breeds. Similar levels of average sequence divergence were observed among animals within each of the major continental groups: 0.41% (European), 0.38% (African), and 0.42% (Indian). However, the sequences fell into two very distinct geographic lineages that do not correspond with the taurine-zebu dichotomy: all European and African breeds are in one lineage, and all Indian breeds are in the other. There was little indication of breed clustering within either lineage. Application of a molecular clock suggests that the two major mtDNA clades diverged at least 200,000, and possibly as much as 1 million, years ago. This relatively large divergence is interpreted most simply as evidence for two separate domestication events, presumably of different subspecies of the aurochs, Bos primigenius. The clustering of all African zebu mtDNA sequences within the taurine lineage is attributed to ancestral crossbreeding with the earlier B. taurus inhabitants of the continent.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, USA )
                1553-7390
                1553-7404
                March 2014
                27 March 2014
                : 10
                : 3
                Affiliations
                [1 ]Division of Animal Sciences, University of Missouri, Columbia, Missouri, United States of America
                [2 ]Department of Animal Science, The University of Vermont, Burlington, Vermont, United States of America
                [3 ]Department of Animal Sciences, Oklahoma State University, Stillwater, Oklahoma, United States of America
                [4 ]Departamento de Genética, Facultad de Veterinaria, Universidad de Córdoba, Córdoba, Spain
                [5 ]USDA-ARS Bovine Functional Genomics Lab, Beltsville, Maryland, United States of America
                [6 ]Medicine & Health Sciences, The University of Nottingham, Nottingham, United Kingdom
                [7 ]Evolutionary Biology Centre, Uppsala Universitet, Uppsala, Sweden
                [8 ]Department of Veterinary Pathobiology, College of Veterinary Medicine, Texas A&M University, College Station, Texas, United States of America
                [9 ]Indonesian Research Institute for Animal Production, Ciawi, Bogor, Indonesia
                [10 ]Institute of Biochemistry & Biotechnology, University of Veterinary and Animal Sciences, Lahore, Pakistan
                [11 ]Animal Molecular Genetics, Embrapa Pecuaria Sudeste, Sao Carlos, Sao Paulo, Brasil
                [12 ]Animal Science, Biometry and Genetics, Ankara University, Diskapi, Ankara, Turkey
                [13 ]USDA, ARS, U.S. Meat Animal Research Center, Clay Center, Nebraska, United States of America
                [14 ]Department of Animal Science, Pennsylvania State University, University Park, Pennsylvania, United States of America
                [15 ]College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, China
                [16 ]Department of Animal Science, Iowa State University, Ames, Iowa, United States of America
                [17 ]Department of Animal Breeding and Genetics, University of Agriculture, Faisalabad, Pakistan
                University of Oxford, United Kingdom
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JED JFT. Performed the experiments: SDM MMR JK RDS. Analyzed the data: JED. Contributed reagents/materials/analysis tools: AMA TSS OH AG CMS LP MEB LCdAR MAY MPH WSL CZL JMR MSUR JFT. Wrote the paper: JED JFT.

                Article
                PGENETICS-D-13-02587
                10.1371/journal.pgen.1004254
                3967955
                24675901

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                Page count
                Pages: 14
                Funding
                This project was supported by National Research Initiative grants number 2008-35205-04687 and 2008-35205-18864 from the USDA Cooperative State Research, Education and Extension Service and National Research Initiative grants number 2009-65205-05635, 2011-68004-30214, 2011-68004-30367 and 2013-68004-20364 from the USDA National Institute of Food and Agriculture. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Agriculture
                Animal Management
                Animal Breeding
                Evolutionary Biology
                Evolutionary Processes
                Hybridization
                Introgression
                Evolutionary Systematics
                Phylogenetics
                Population Genetics
                Gene Flow
                Genetics
                Animal Genetics
                Population Biology

                Genetics

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