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      Genomic signatures and correlates of widespread population declines in salmon

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          Abstract

          Global losses of biodiversity are occurring at an unprecedented rate, but causes are often unidentified. Genomic data provide an opportunity to isolate drivers of change and even predict future vulnerabilities. Atlantic salmon ( Salmo salar) populations have declined range-wide, but factors responsible are poorly understood. Here, we reconstruct changes in effective population size ( N e) in recent decades for 172 range-wide populations using a linkage-based method. Across the North Atlantic, N e has significantly declined in >60% of populations and declines are consistently temperature-associated. We identify significant polygenic associations with decline, involving genomic regions related to metabolic, developmental, and physiological processes. These regions exhibit changes in presumably adaptive diversity in declining populations consistent with contemporary shifts in body size and phenology. Genomic signatures of widespread population decline and associated risk scores allow direct and potentially predictive links between population fitness and genotype, highlighting the power of genomic resources to assess population vulnerability.

          Abstract

          The Atlantic salmon has suffered widespread population declines over the last century. Here, Lehnert et al. reconstruct changes in effective population size of 172 populations based on genomic linkage information revealing mostly temperature-associated population declines with over 60% of populations in decline since 1975.

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          A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish

          Barrier structures (e.g. epithelia around tissues, plasma membranes around cells) are required for internal homeostasis and protection from pathogens. Wound detection and healing represent a dormant morphogenetic program that can be rapidly executed to restore barrier integrity and tissue homeostasis. In animals, initial steps include recruitment of leukocytes to the site of injury across distances of hundreds of micrometers within minutes of wounding. The spatial signals that direct this immediate tissue response are unknown. Due to their fast diffusion and versatile biological activities, reactive oxygen species (ROS), including hydrogen peroxide (H2O2), are interesting candidates for wound-to-leukocyte signalling. We probed the role of H2O2 during the early events of wound responses in zebrafish larvae expressing a genetically encoded H2O2 sensor1. This reporter revealed a sustained rise in H2O2 concentration at the wound margin, starting ∼3 min after wounding and peaking at ∼20 min, which extended ∼100−200 μm into the tail fin epithelium as a decreasing concentration gradient. Using pharmacological and genetic inhibition, we show that this gradient is created by Dual oxidase (Duox), and that it is required for rapid recruitment of leukocytes to the wound. This is the first observation of a tissue-scale H2O2 pattern, and the first evidence that H2O2 signals to leukocytes in tissues, in addition to its known antiseptic role.
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            A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci*

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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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                Author and article information

                Contributors
                sarah.lehnert@dfo-mpo.gc.ca
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                5 July 2019
                5 July 2019
                2019
                : 10
                : 2996
                Affiliations
                [1 ]ISNI 0000 0004 0449 2129, GRID grid.23618.3e, Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, ; 80 E White Hills Rd, St. John’s, Newfoundland, A1C 5X1 Canada
                [2 ]ISNI 0000 0004 1936 8200, GRID grid.55602.34, Biology Department, , Dalhousie University, ; 6050 University Avenue, Halifax, NS B3H 4R2 Canada
                [3 ]ISNI 0000 0004 0607 975X, GRID grid.19477.3c, Centre for Integrative Genetics (CIGENE), Department of Animal and Aquacultural Sciences, Faculty of Biosciences, , Norwegian University of Life Sciences, ; Ås, 1430 Norway
                [4 ]ISNI 0000 0000 9697 5734, GRID grid.438570.d, Marine Scotland Science, Freshwater Fisheries Laboratory, ; Faskally, Pitlochry PH16 5LB UK
                [5 ]ISNI 0000 0000 9130 6822, GRID grid.25055.37, Centre for Fisheries Ecosystems Research, , Fisheries and Marine Institute of Memorial University of Newfoundland, ; 155 Ridge Rd, St. John’s, NL A1C 5R3 Canada
                [6 ]ISNI 0000 0000 9130 6822, GRID grid.25055.37, Labrador Institute, , Memorial University of Newfoundland, ; 219 Hamilton River Rd, Happy Valley-Goose Bay, NL A0P 1E0 Canada
                [7 ]ISNI 0000 0001 2173 5688, GRID grid.418256.c, Fisheries and Oceans Canada, Bedford Institute of Oceanography, ; 1 Challenger Dr, Dartmouth, NS B2Y 4A2 Canada
                [8 ]ISNI 0000 0001 1502 9269, GRID grid.420104.3, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, ; Seattle, WA 98112 USA
                Author information
                http://orcid.org/0000-0002-3569-8299
                http://orcid.org/0000-0003-3362-7590
                Article
                10972
                10.1038/s41467-019-10972-w
                6611788
                31278264
                814e336b-0b2e-4a1c-9483-3b906810a81d
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 22 November 2018
                : 11 June 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100000041, Gouvernement du Canada | Fisheries and Oceans Canada (Pêches et Océans Canada);
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                evolutionary genetics,population genetics,biodiversity,conservation genomics
                Uncategorized
                evolutionary genetics, population genetics, biodiversity, conservation genomics

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