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
Atlantic salmon (Salmo salar) is one of the most extensively studied fish species in the world due to its significance in aquaculture, fisheries and ongoing conservation efforts to protect declining populations. Yet, limited genomic resources have hampered our understanding of genetic architecture in the species and the genetic basis of adaptation to the wide range of natural and artificial environments it occupies. In this study, we describe the development of a medium-density Atlantic salmon single nucleotide polymorphism (SNP) array based on expressed sequence tags (ESTs) and genomic sequencing. The array was used in the most extensive assessment of population genetic structure performed to date in this species. A total of 6176 informative SNPs were successfully genotyped in 38 anadromous and freshwater wild populations distributed across the species natural range. Principal component analysis clearly differentiated European and North American populations, and within Europe, three major regional genetic groups were identified for the first time in a single analysis. We assessed the potential for the array to disentangle neutral and putative adaptive divergence of SNP allele frequencies across populations and among regional groups. In Europe, secondary contact zones were identified between major clusters where endogenous and exogenous barriers could be associated, rendering the interpretation of environmental influence on potentially adaptive divergence equivocal. A small number of markers highly divergent in allele frequencies (outliers) were observed between (multiple) freshwater and anadromous populations, between northern and southern latitudes, and when comparing Baltic populations to all others. We also discuss the potential future applications of the SNP array for conservation, management and aquaculture.
The extensive phenotypic polymorphism in the European whitefish has triggered evolutionary research in order to disentangle mechanisms underlying diversification. To illuminate the ecological distinctiveness in polymorphic whitefish, and evaluate taxonomic designations, we studied nine Norwegian lakes in three watercourses, which each harboured pairs of divergent whitefish morphs. We compared the morphology and life history of these morphs, documented the extent of genetic differentiation between them, and contrasted the niche use of sympatric morphs along both the habitat and resource axes. In all cases, sympatric morphs differed in the number of gill rakers, a highly heritable trait related to trophic utilization. Individual growth rate, age and size at maturity, diet and habitat use also differed between morphs within lakes, but were remarkably similar across lakes within the same morph. Microsatellite analyses confirmed for all but one pair that sympatric morphs were significantly genetically different, and that similar morphs from different lakes likely have a polyphyletic origin. These results are most compatible with the process of parallel evolution through recurrent postglacial divergence into pelagic and benthic niches in each of these lakes. We propose that sparsely and densely rakered whitefish sympatric pairs may be a likely case of ecological speciation, mediated in oligotrophic lakes with few trophic competitors.
O. 2006. Genetic and ecological effects of salmon farming on wild salmon: modelling from experimental results. À ICES Journal of Marine Science, 63: 1234e1247. Cultured salmonids are released or escape into the wild in large numbers and may make up significant proportions of wild salmonid populations in fresh-and saltwater, causing considerable concern for the fitness and productivity of these populations. This paper focuses on the effects of escaped farmed Atlantic salmon (Salmo salar) on wild salmon. Farmed salmon have been under artificial selection for growth and other economically important traits for 30 years and are genetically different in their origin at the molecular and quantitative genetic levels. Escaped farmed salmon spawn in the wild with limited success. Their offspring outgrow those of wild origin but suffer higher mortality. Whole-river experiments in Ireland and Norway have shown that the lifetime success of farmed salmon is reduced relative to wild salmon. Based on data from these experiments, we model the future of wild salmon populations experiencing invasions of escaped farmed salmon. Simulations with a fixed intrusion rate of 20% escaped farmed salmon at spawning suggest that substantial changes take place in wild salmon populations within ten salmon generations (w40 years). Low-invasion scenarios suggest that farmed offspring are unlikely to become established in the population, whereas high-invasion scenarios suggest that populations are eventually mixtures of hybrid and farmed descendants. Recovery of the wild population is not likely under all circumstances, even after many decades without further intrusion. Managers of wild salmon will have difficulty in obtaining broodstock of the original wild population after a few generations of high intrusion. We conclude that further measures to reduce escapes of farmed salmon and their spawning in wild populations are urgently needed.
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