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Comparing genomic signatures of domestication in two Atlantic salmon (Salmo salar L.) populations with different geographical origins

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      Abstract

      Selective breeding and genetic improvement have left detectable signatures on the genomes of domestic species. The elucidation of such signatures is fundamental for detecting genomic regions of biological relevance to domestication and improving management practices. In aquaculture, domestication was carried out independently in different locations worldwide, which provides opportunities to study the parallel effects of domestication on the genome of individuals that have been selected for similar traits. In this study, we aimed to detect potential genomic signatures of domestication in two independent pairs of wild/domesticated Atlantic salmon populations of Canadian and Scottish origins, respectively. Putative genomic regions under divergent selection were investigated using a 200K SNP array by combining three different statistical methods based either on allele frequencies ( LFMM, Bayescan) or haplotype differentiation (Rsb). We identified 337 and 270 SNPs potentially under divergent selection in wild and hatchery populations of Canadian and Scottish origins, respectively. We observed little overlap between results obtained from different statistical methods, highlighting the need to test complementary approaches for detecting a broad range of genomic footprints of selection. The vast majority of the outliers detected were population‐specific but we found four candidate genes that were shared between the populations. We propose that these candidate genes may play a role in the parallel process of domestication. Overall, our results suggest that genetic drift may have override the effect of artificial selection and/or point toward a different genetic basis underlying the expression of similar traits in different domesticated strains. Finally, it is likely that domestication may predominantly target polygenic traits (e.g., growth) such that its genomic impact might be more difficult to detect with methods assuming selective sweeps.

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      Most cited references 117

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      PLINK: a tool set for whole-genome association and population-based linkage analyses.

      Whole-genome association studies (WGAS) bring new computational, as well as analytic, challenges to researchers. Many existing genetic-analysis tools are not designed to handle such large data sets in a convenient manner and do not necessarily exploit the new opportunities that whole-genome data bring. To address these issues, we developed PLINK, an open-source C/C++ WGAS tool set. With PLINK, large data sets comprising hundreds of thousands of markers genotyped for thousands of individuals can be rapidly manipulated and analyzed in their entirety. As well as providing tools to make the basic analytic steps computationally efficient, PLINK also supports some novel approaches to whole-genome data that take advantage of whole-genome coverage. We introduce PLINK and describe the five main domains of function: data management, summary statistics, population stratification, association analysis, and identity-by-descent estimation. In particular, we focus on the estimation and use of identity-by-state and identity-by-descent information in the context of population-based whole-genome studies. This information can be used to detect and correct for population stratification and to identify extended chromosomal segments that are shared identical by descent between very distantly related individuals. Analysis of the patterns of segmental sharing has the potential to map disease loci that contain multiple rare variants in a population-based linkage analysis.
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        The variant call format and VCFtools

        Summary: The variant call format (VCF) is a generic format for storing DNA polymorphism data such as SNPs, insertions, deletions and structural variants, together with rich annotations. VCF is usually stored in a compressed manner and can be indexed for fast data retrieval of variants from a range of positions on the reference genome. The format was developed for the 1000 Genomes Project, and has also been adopted by other projects such as UK10K, dbSNP and the NHLBI Exome Project. VCFtools is a software suite that implements various utilities for processing VCF files, including validation, merging, comparing and also provides a general Perl API. Availability: http://vcftools.sourceforge.net Contact: rd@sanger.ac.uk
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          A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3.

          We describe a new computer program, SnpEff, for rapidly categorizing the effects of variants in genome sequences. Once a genome is sequenced, SnpEff annotates variants based on their genomic locations and predicts coding effects. Annotated genomic locations include intronic, untranslated region, upstream, downstream, splice site, or intergenic regions. Coding effects such as synonymous or non-synonymous amino acid replacement, start codon gains or losses, stop codon gains or losses, or frame shifts can be predicted. Here the use of SnpEff is illustrated by annotating ~356,660 candidate SNPs in ~117 Mb unique sequences, representing a substitution rate of ~1/305 nucleotides, between the Drosophila melanogaster w(1118); iso-2; iso-3 strain and the reference y(1); cn(1) bw(1) sp(1) strain. We show that ~15,842 SNPs are synonymous and ~4,467 SNPs are non-synonymous (N/S ~0.28). The remaining SNPs are in other categories, such as stop codon gains (38 SNPs), stop codon losses (8 SNPs), and start codon gains (297 SNPs) in the 5'UTR. We found, as expected, that the SNP frequency is proportional to the recombination frequency (i.e., highest in the middle of chromosome arms). We also found that start-gain or stop-lost SNPs in Drosophila melanogaster often result in additions of N-terminal or C-terminal amino acids that are conserved in other Drosophila species. It appears that the 5' and 3' UTRs are reservoirs for genetic variations that changes the termini of proteins during evolution of the Drosophila genus. As genome sequencing is becoming inexpensive and routine, SnpEff enables rapid analyses of whole-genome sequencing data to be performed by an individual laboratory.
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            Author and article information

            Affiliations
            [ 1 ] Facultad de Ciencias Veterinarias y Pecuarias Universidad de Chile Santiago Chile
            [ 2 ] Facultad de Ciencias Agronómicas Universidad de Chile Santiago Chile
            [ 3 ] IBIS Institut de Biologie Intégrative et des Systèmes Université Laval Québec City Québec Canada
            [ 4 ] Centre d’Écologie Fonctionnelle et Évolutive Unité Mixte de Recherche CNRS 5175 Montpellier France
            [ 5 ] Marine Scotland Science Freshwater Fisheries Laboratory Faskally Pitlochry UK
            [ 6 ] Laboratory of Bioinformatics and Mathematics of the Genome Center for Mathematical Modeling (UMI 2807 CNRS) and Center for Genome Regulation (Fondap 15090007) Universidad de Chile Santiago Chile
            [ 7 ] Aquainnovo Puerto Montt Chile
            [ 8 ] Núcleo Milenio INVASAL Concepción Chile
            Author notes
            [* ] Correspondence

            José M. Yáñez, Facultad de Ciencias Agronómicas, Universidad de Chile, Santiago, Chile.

            Email: jmayanez@ 123456uchile.cl

            [†]

            Both authors contributed equally to the manuscript.

            Contributors
            ORCID: http://orcid.org/0000-0002-6612-4087, jmayanez@uchile.cl
            Journal
            Evol Appl
            Evol Appl
            10.1111/(ISSN)1752-4571
            EVA
            Evolutionary Applications
            John Wiley and Sons Inc. (Hoboken )
            1752-4571
            07 December 2018
            January 2019
            : 12
            : 1 , Genomics of Domestication ( doiID: 10.1111/eva.2019.12.issue-1 )
            : 137-156
            6304691 10.1111/eva.12689 EVA12689
            © 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.

            Counts
            Figures: 5, Tables: 5, Pages: 20, Words: 15691
            Product
            Funding
            Funded by: Corporación de Fomento de la Producción
            Award ID: 11IEI‐12843
            Award ID: 12PIE‐17669
            Funded by: CONICYT
            Award ID: 21120382
            Funded by: Canada–Chile Leadership Exchange Scholarship
            Funded by: Ministerio de Economía, Fomento y Turismo
            Categories
            Special Issue Original Article
            Special Issue Original Articles
            Custom metadata
            2.0
            eva12689
            January 2019
            Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.5.4 mode:remove_FC converted:24.12.2018

            Evolutionary Biology

            single nucleotide polymorphisms, salmo salar, selective sweeps

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