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      Polygenic and sex specific architecture for two maturation traits in farmed Atlantic salmon

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          Abstract

          Background

          A key developmental transformation in the life of all vertebrates is the transition to sexual maturity, whereby individuals are capable of reproducing for the first time. In the farming of Atlantic salmon, early maturation prior to harvest size has serious negative production impacts.

          Results

          We report genome wide association studies (GWAS) using fish measured for sexual maturation in freshwater or the marine environment. Genotypic data from a custom 50 K single nucleotide polymorphism (SNP) array was used to identify 13 significantly associated SNP for freshwater maturation with the most strongly associated on chromosomes 10 and 11. A higher number of associations (48) were detected for marine maturation, and the two peak loci were found to be the same for both traits. The number and broad distribution of GWAS hits confirmed a highly polygenetic nature, and GWAS performed separately within males and females revealed sex specific genetic behaviour for loci co-located with positional candidate genes phosphatidylinositol-binding clathrin assembly protein-like ( picalm) and membrane-associated guanylate kinase, WW and PDZ domain-containing protein 2 ( magi2).

          Conclusions

          The results extend earlier work and have implications for future applied breeding strategies to delay maturation in this important aquaculture species.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-019-5525-4) contains supplementary material, which is available to authorized users.

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          Most cited references28

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          Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon.

          Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific loci underlying sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here we identify a large effect locus controlling age at maturity in Atlantic salmon (Salmo salar), an important fitness trait in which selection favours earlier maturation in males than females, and show it is a clear example of sex-dependent dominance that reduces intralocus sexual conflict and maintains adaptive variation in wild populations. Using high-density single nucleotide polymorphism data across 57 wild populations and whole genome re-sequencing, we find that the vestigial-like family member 3 gene (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39% of phenotypic variation, an unexpectedly large proportion for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal allowing greater optimization of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.
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            Genomic analyses identify hundreds of variants associated with age at menarche and support a role for puberty timing in cancer risk

            John Perry, Ken Ong and colleagues analyze genotype data on ∼370,000 women and identify 389 independent signals that associate with age at menarche, implicating ∼250 genes. Their analyses suggest causal inverse associations, independent of BMI, between puberty timing and risks for breast and endometrial cancers in women and prostate cancer in men.
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              Permutation tests for multiple loci affecting a quantitative character.

              The problem of detecting minor quantitative trait loci (QTL) responsible for genetic variation not explained by major QTL is of importance in the complete dissection of quantitative characters. Two extensions of the permutation-based method for estimating empirical threshold values are presented. These methods, the conditional empirical threshold (CET) and the residual empirical threshold (RET), yield critical values that can be used to construct tests for the presence of minor QTL effects while accounting for effects of known major QTL. The CET provides a completely nonparametric test through conditioning on markers linked to major QTL. It allows for general nonadditive interactions among QTL, but its practical application is restricted to regions of the genome that are unlinked to the major QTL. The RET assumes a structural model for the effect of major QTL, and a threshold is constructed using residuals from this structural model. The search space for minor QTL is unrestricted, and RET-based tests may be more powerful than the CET-based test when the structural model is approximately true.
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                Author and article information

                Contributors
                amin.esmail@csiro.au
                Klara.Verbyla@data61.csiro.au
                Hawlader.Almamun@data61.csiro.au
                Sean.McWilliam@csiro.au
                bradley.evans@tassal.com.au
                Harry.King@csiro.au
                Peter.Kube@csiro.au
                james.kijas@csiro.au
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                15 February 2019
                15 February 2019
                2019
                : 20
                : 139
                Affiliations
                [1 ]GRID grid.1016.6, Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, ; Queensland Bioscience Precinct, St Lucia Brisbane, 4067 Australia
                [2 ]GRID grid.1016.6, Commonwealth Scientific and Industrial Research Organisation Data 61, ; Canberra, Australian Capital Territory 2601 Australia
                [3 ]Tassal Operations Pty Ltd, Hobart, Tasmania 7001 Australia
                [4 ]Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Hobart, Tasmania 7004 Australia
                [5 ]ISNI 0000 0004 0621 2741, GRID grid.411660.4, Zoology Department, Faculty of Science, , Benha University, ; Benha, 13518 Egypt
                Article
                5525
                10.1186/s12864-019-5525-4
                6377724
                30770720
                d873454b-b22f-43d8-9c0d-69a84e1c08b4
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 17 April 2018
                : 11 February 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000943, Commonwealth Scientific and Industrial Research Organisation;
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Genetics
                atlantic salmon (salmo salar),sexual maturation,genetic architecture,gwas,snp,picalm
                Genetics
                atlantic salmon (salmo salar), sexual maturation, genetic architecture, gwas, snp, picalm

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