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      Genomics and conservation units: The genetic basis of adult migration timing in Pacific salmonids

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          Abstract

          It is now routinely possible to generate genomics‐scale datasets for nonmodel species; however, many questions remain about how best to use these data for conservation and management. Some recent genomics studies of anadromous Pacific salmonids have reported a strong association between alleles at one or a very few genes and a key life history trait (adult migration timing) that has played an important role in defining conservation units. Publication of these results has already spurred a legal challenge to the existing framework for managing these species, which was developed under the paradigm that most phenotypic traits are controlled by many genes of small effect, and that parallel evolution of life history traits is common. But what if a key life history trait can only be expressed if a specific allele is present? Does the current framework need to be modified to account for the new genomics results, as some now propose? Although this real‐world example focuses on Pacific salmonids, the issues regarding how genomics can inform us about the genetic basis of phenotypic traits, and what that means for applied conservation, are much more general. In this perspective, we consider these issues and outline a general process that can be used to help generate the types of additional information that would be needed to make informed decisions about the adequacy of existing conservation and management frameworks.

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          Most cited references28

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          Adaptive evolutionary conservation: towards a unified concept for defining conservation units.

          Recent years have seen a debate over various methods that could objectively prioritize conservation value below the species level. Most prominent among these has been the evolutionarily significant unit (ESU). We reviewed ESU concepts with the aim of proposing a more unified concept that would reconcile opposing views. Like species concepts, conflicting ESU concepts are all essentially aiming to define the same thing: segments of species whose divergence can be measured or evaluated by putting differential emphasis on the role of evolutionary forces at varied temporal scales. Thus, differences between ESU concepts lie more in the criteria used to define the ESUs themselves rather than in their fundamental essence. We provide a context-based framework for delineating ESUs which circumvents much of this situation. Rather than embroil in a befuddled debate over an optimal criterion, the key to a solution is accepting that differing criteria will work more dynamically than others and can be used alone or in combination depending on the situation. These assertions constitute the impetus behind adaptive evolutionary conservation.
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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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              The genetic architecture of adaptation under migration-selection balance.

              Many ecologically important traits have a complex genetic basis, with the potential for mutations at many different genes to shape the phenotype. Even so, studies of local adaptation in heterogeneous environments sometimes find that just a few quantitative trait loci (QTL) of large effect can explain a large percentage of observed differences between phenotypically divergent populations. As high levels of gene flow can swamp divergence at weakly selected alleles, migration-selection-drift balance may play an important role in shaping the genetic architecture of local adaptation. Here, we use analytical approximations and individual-based simulations to explore how genetic architecture evolves when two populations connected by migration experience stabilizing selection toward different optima. In contrast to the exponential distribution of allele effect sizes expected under adaptation without migration (Orr 1998), we find that adaptation with migration tends to result in concentrated genetic architectures with fewer, larger, and more tightly linked divergent alleles. Even if many small alleles contribute to adaptation at the outset, they tend to be replaced by a few large alleles under prolonged bouts of stabilizing selection with migration. All else being equal, we also find that stronger selection can maintain linked clusters of locally adapted alleles over much greater map distances than weaker selection. The common empirical finding of QTL of large effect is shown to be expected with migration in a heterogeneous landscape, and these QTL may often be composed of several tightly linked alleles of smaller effect. © 2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.
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                Author and article information

                Contributors
                robin.waples@noaa.gov
                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                28 August 2018
                October 2018
                : 11
                : 9 ( doiID: 10.1111/eva.2018.11.issue-9 )
                : 1518-1526
                Affiliations
                [ 1 ] NOAA Fisheries Northwest Fisheries Science Center Seattle Washington
                [ 2 ] NOAA Fisheries Southwest Fisheries Science Center Santa Cruz California
                Author notes
                [*] [* ] Correspondence

                Robin Waples, NOAA Fisheries, Northwest Fisheries Science Center, Seattle, WA.

                Email: robin.waples@ 123456noaa.gov

                Author information
                http://orcid.org/0000-0003-3362-7590
                Article
                EVA12687
                10.1111/eva.12687
                6183503
                30344624
                eb25f052-9c91-4e79-aaac-bbcbb9ed044c
                Published 2018. This article is a U.S. Government work and is in the public domain in the USA. 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
                : 19 April 2018
                : 18 July 2018
                : 20 July 2018
                Page count
                Figures: 2, Tables: 0, Pages: 9, Words: 7751
                Categories
                Perspective
                Perspectives
                Custom metadata
                2.0
                eva12687
                October 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.5.0.1 mode:remove_FC converted:12.10.2018

                Evolutionary Biology
                adaptation,conservation genetics,fisheries management,genomics,life history evolution,natural selection,population genetics

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