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.
Farm Atlantic salmon escape and invade rivers throughout the North Atlantic annually, which has generated growing concern about their impacts on native salmon populations. A large-scale experiment was therefore undertaken in order to quantify the lifetime success and interactions of farm salmon invading a Norwegian river. Sexually mature farm and native salmon were genetically screened, radio tagged and released into the River Imsa where no other salmon had been allowed to ascend. The farm ¢shes were competitively and reproductively inferior, achieving less than one-third the breeding success of the native ¢shes. Moreover, this inferiority was sex biased, being more pronounced in farm males than females, resulting in the principal route of gene £ow involving native males mating with farm females. There were also indications of selection against farm genotypes during early survival but not thereafter. However, evidence of resource competition and competitive displacement existed as the productivity of the native population was depressed by more than 30%. Ultimately, the lifetime reproductive success (adult to adult) of the farm ¢shes was 16% that of the native salmon. Our results indicate that such annual invasions have the potential for impacting on population productivity, disrupting local adaptations and reducing the genetic diversity of wild salmon populations.
This paper addresses the genetic consequences of aquaculture on natural fish populations. The study is motivated by rapidly increasing numbers of intentionally and accidentally released fish and is based on empirical observations reported in the literature. A wide variety of outcomes, ranging from no detectable effect to complete introgression or displacement, has been observed following releases of cultured fish into natural settings. Where genetic effects on performance traits have been documented, they always appear to be negative in comparison with the unaffected native populations. These findings are consistent with theoretical considerations of the implications of elevated levels of gene flow between cultured and locally adapted natural populations; they raise concerns over the genetic future of many natural populations in the light of increasing numbers of released fish. Strategies for the genetic protection of native populations from the effects of aquaculture are outlined including more secure containment, the use of sterilized fish, and modifying the points of rearing and release. We recommend strong restrictions on gene flow from cultured to wild populations and effective monitoring of such gene flow.
Atlantic salmon (Salmo salar) is one of the best researched fishes, and its aquaculture plays a global role in the blue revolution. However, since the 1970s, tens of millions of farmed salmon have escaped into the wild. We review current knowledge of genetic interactions and identify the unanswered questions. Native salmon populations are typically genetically distinct from each other and potentially locally adapted. Outside Norway, introgression remains unquantified, and in all regions, biological changes and the mechanisms driving population-specific impacts remain poorly documented. Nevertheless, existing knowledge shows that the long-term consequences of introgression is expected to lead to changes in life-history traits, reduced population productivity and decreased resilience to future challenges. Only a major reduction in the number of escapees and/or sterility of farmed salmon can eliminate further impacts. K E Y W O R D Saquaculture, evolution, fish farming, fitness, genetic, hybrid
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