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      Domestication of cattle: Two or three events?

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          Abstract

          Cattle have been invaluable for the transition of human society from nomadic hunter‐gatherers to sedentary farming communities throughout much of Europe, Asia and Africa since the earliest domestication of cattle more than 10,000 years ago. Although current understanding of relationships among ancestral populations remains limited, domestication of cattle is thought to have occurred on two or three occasions, giving rise to the taurine ( Bos taurus) and indicine ( Bos indicus) species that share the aurochs ( Bos primigenius) as common ancestor ~250,000 years ago. Indicine and taurine cattle were domesticated in the Indus Valley and Fertile Crescent, respectively; however, an additional domestication event for taurine in the Western Desert of Egypt has also been proposed. We analysed medium density Illumina Bovine SNP array (~54,000 loci) data across 3,196 individuals, representing 180 taurine and indicine populations to investigate population structure within and between populations, and domestication and demographic dynamics using approximate Bayesian computation ( ABC). Comparative analyses between scenarios modelling two and three domestication events consistently favour a model with only two episodes and suggest that the additional genetic variation component usually detected in African taurine cattle may be explained by hybridization with local aurochs in Africa after the domestication of taurine cattle in the Fertile Crescent. African indicine cattle exhibit high levels of shared genetic variation with Asian indicine cattle due to their recent divergence and with African taurine cattle through relatively recent gene flow. Scenarios with unidirectional or bidirectional migratory events between European taurine and Asian indicine cattle are also plausible, although further studies are needed to disentangle the complex human‐mediated dispersion patterns of domestic cattle. This study therefore helps to clarify the effect of past demographic history on the genetic variation of modern cattle, providing a basis for further analyses exploring alternative migratory routes for early domestic populations.

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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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            Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds.

            The imprints of domestication and breed development on the genomes of livestock likely differ from those of companion animals. A deep draft sequence assembly of shotgun reads from a single Hereford female and comparative sequences sampled from six additional breeds were used to develop probes to interrogate 37,470 single-nucleotide polymorphisms (SNPs) in 497 cattle from 19 geographically and biologically diverse breeds. These data show that cattle have undergone a rapid recent decrease in effective population size from a very large ancestral population, possibly due to bottlenecks associated with domestication, selection, and breed formation. Domestication and artificial selection appear to have left detectable signatures of selection within the cattle genome, yet the current levels of diversity within breeds are at least as great as exists within humans.
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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
                orozco-terwengelpa@cardiff.ac.uk
                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                23 July 2018
                January 2019
                : 12
                : 1 , Genomics of Domestication ( doiID: 10.1111/eva.2019.12.issue-1 )
                : 123-136
                Affiliations
                [ 1 ] School of Biosciences Cardiff University Cardiff UK
                [ 2 ] Parco Tecnologico Padano (PTP) Lodi Italy
                [ 3 ] Animal Genomics Laboratory UCD School of Agriculture and Food Science, UCD College of Health and Agricultural Sciences University College Dublin Dublin Ireland
                [ 4 ] UCD Conway Institute of Biomolecular and Biomedical Research University College Dublin Dublin Ireland
                [ 5 ] IdentiGEN Ltd. Dublin Ireland
                [ 6 ] Istituto di Zootecnica e BioDNA Centro di Ricerca sulla Biodiversità e sul DNA Antico Università Cattolica del S. Cuore di Piacenza Piacenza Italy
                [ 7 ] Corporación Colombiana De Investigación Agropecuaria (Corpoica) Centro de investigaciones Tibaitatá Bogotá Colombia
                Author notes
                [*] [* ] Correspondence

                Pablo Orozco‐terWengel, School of Biosciences, Cardiff University, Cardiff, CF10 3AX, UK.

                Email: orozco-terwengelpa@ 123456cardiff.ac.uk

                Author information
                http://orcid.org/0000-0002-8429-2957
                http://orcid.org/0000-0003-4766-6291
                http://orcid.org/0000-0001-6357-6080
                http://orcid.org/0000-0002-7951-4148
                Article
                EVA12674
                10.1111/eva.12674
                6304694
                30622640
                e457e43b-34fa-433e-8e61-9e82c9ab0e82
                © 2018 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 October 2017
                : 19 March 2018
                : 10 June 2018
                Page count
                Figures: 7, Tables: 2, Pages: 14, Words: 9732
                Funding
                Funded by: BBSRC SWBio DTP PhD studentship
                Award ID: BB/M009122/1
                Funded by: FACCE‐JPI ERA‐NET Smart Agriculture Program
                Award ID: BB/M019276/1
                Funded by: H2020 Marie Skłodowska‐Curie Actions
                Award ID: DLV‐655100
                Categories
                Special Issue Original Article
                Special Issue Original Articles
                Custom metadata
                2.0
                eva12674
                January 2019
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.5.4 mode:remove_FC converted:24.12.2018

                Evolutionary Biology
                approximate bayesian computation,bos indicus,bos taurus,demographic modeling,domestication history,snp array

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