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.
The genes of the major histocompatibility complex (MHC) code for proteins involved in antigen recognition and triggering of the adaptive immune response, and are therefore likely to be under selection from parasites. These selection regimes may vary in space and time. Here we report a strong geographical structure in MHC class II B genes of a migrating bird, the great snipe (Gallinago media). Genetic differentiation in the MHC between two ecologically distinct distributional regions (Scandinavian mountain populations vs. East European lowland populations) was still present after statistically controlling for the effect of selectively neutral variation (microsatellites) using partial Mantel tests. This suggests a role for selection in generating this spatial structure and that it represents local adaptation to different environments. Differentiation between populations within the two regions was negligible. Overall, we found a high number of MHC alleles (50, from 175 individuals). This, together with a tendency for a higher rate of nonsynonymous than synonymous substitutions in the peptide binding sites, and high Tajima's D in certain regions of the gene, suggests a history of balancing selection. MHC variation is often thought to be maintained by some form of balancing selection, but the nature of this selection remains unclear. Our results support the hypothesis that spatial variation in selection regimes contributes to the high polymorphism.
Atlantic salmon (Salmo salar) is an economically and culturally important species. Norway has more than 400 watercourses with Atlantic salmon and supports a large proportion of the world's wild Atlantic salmon. Atlantic salmon are structured into numerous genetically differentiated populations, and are therefore managed at the population level. Long-distance migrations between freshwater and ocean habitats expose Atlantic salmon to multiple threats, and a number of anthropogenic factors have contributed to the decline of Atlantic salmon during the last decades. Knowledge on the relative importance of the different anthropogenic factors is vital for prioritizing management measures. We developed a semi-quantitative 2D classification system to rank the different anthropogenic factors and used this to assess the major threats to Norwegian Atlantic salmon. Escaped farmed salmon and salmon lice from fish farms were identified as expanding population threats, with escaped farmed salmon being the largest current threat. These two factors affect populations to the extent that they may be critically endangered or lost, with a large likelihood of causing further reductions and losses in the future. The introduced parasite Gyrodactylus salaris, freshwater acidification, hydropower regulation and other habitat alterations were identified as stabilized population threats, which have contributed to populations becoming critically endangered or lost, but with a low likelihood of causing further loss. Other impacts were identified as less influential, either as stabilized or expanding factors that cause loss in terms of number of returning adults, but not to the extent that populations become threatened. Management based on population specific reference points (conservation limits) has reduced exploitation in Norway, and overexploitation was therefore no longer regarded an important impact factor. The classification system may be used as a template for ranking of anthropogenic impact factors in other countries and as a support for national and international conservation efforts.
Farmed Atlantic salmon (Salmo salar) escape from net pens and enter rivers to spawn, potentially resulting in genetic introgression and reduced fitness of wild salmon. Here, we quantify genetic introgression of farmed to wild salmon, using molecular genetic markers, in populations from 147 salmon rivers, representing three-quarters of the total wild salmon spawning population in Norway. For 109 rivers with adult modern samples and sample sizes of 20 or more, the average level of farmed genetic introgression was 6.4% (median = 2.3%), with a range between 0.0% and 42.2%. Fifty-one of these rivers showed significant farmed genetic introgression when compared with historical reference samples. We observed a highly significant correlation between estimated farmed introgression and average proportion of escaped farmed salmon. We quantify levels of introgression as unweighted averages or weighted by population sizes, to compare geographical regions and to compare levels of introgression in rivers and fjords designated as locations deserving a high level of protection. We found a generally lower level of introgression in National Salmon Rivers and National Salmon Fjords subjected to formal protection by parliament. We conclude that farmed to wild genetic introgression is high in a large proportion of Norwegian salmon rivers, with the highest levels found in the most intensive areas of salmon farming. The extensive genetic introgression documented here poses a serious challenge to the management of farmed and wild Atlantic salmon in Norway and, in all likelihood, in other regions where farmed-salmon escape events occur with regularity
We applied a phenotypic QST (PST) vs. FST approach to study spatial variation in selection among great snipe (Gallinago media) populations in two regions of northern Europe. Morphological divergence between regions was high despite low differentiation in selectively neutral genetic markers, whereas populations within regions showed very little neutral divergence and trait differentiation. QST > FST was robust against altering assumptions about the additive genetic proportions of variance components. The homogenizing effect of gene flow (or a short time available for neutral divergence) has apparently been effectively counterbalanced by differential natural selection, although one trait showed some evidence of being under uniform stabilizing selection. Neutral markers can hence be misleading for identifying evolutionary significant units, and adopting the PST–FST approach might therefore be valuable when common garden experiments is not an option. We discuss the statistical difficulties of documenting uniform selection as opposed to divergent selection, and the need for estimating measurement error. Instead of only comparing overall QST and FST values, we advocate the use of partial matrix permutation tests to analyse pairwise QST differences among populations, while statistically controlling for neutral differentiation.
Interbreeding between domesticated and wild animals occurs in several species. This gene flow has long been anticipated to induce genetic changes in life-history traits of wild populations, thereby influencing population dynamics and viability. Here, we show that individuals with high levels of introgression (domesticated ancestry) have altered age and size at maturation in 62 wild Atlantic salmon Salmo salar populations, including seven ancestral populations to breeding lines of the domesticated salmon. This study documents widespread changes to life-history traits in wild animal populations following gene flow from selectively bred, domesticated conspecifics. The continued high abundance of escaped, domesticated Atlantic salmon thus threatens wild Atlantic salmon populations by inducing genetic changes in fitness-related traits. Our results represent key evidence and a timely warning concerning the potential ecological impacts of the globally increasing use of domesticated animals.
In 2017, Norway experienced an invasion of the Pacific salmonid pink salmon (Oncorhynchus gorbuscha) in numbers never before seen in rivers all along the coast. Significant numbers were also caught in other parts of northwestern Europe. Pink salmon has been observed in variable numbers in Norwegian waters in the summer and autumn of most years since 1960, after the first successful Russian introduction of pink salmon fry in rivers draining to the White Sea in northwest Russia in 1959. With the exception of 1960, pink salmon have been most abundant in odd years, based on the odd-year broodline of the 2-year life salmonid. Even-year fish has generally been less abundant, but in recent years, significant numbers of this broodline have also been caught. In this paper we review the available information on pink salmon in Norwegian rivers and discuss (1) to what extent the presence of this species in Norway has been driven by Russian introductions and natural reproduction in Russian, and lately in Norwegian, rivers, and (2) the likelihood of reproducing populations of pink salmon being established in more Norwegian rivers. Considering the continued propagule pressure in terms of adult pink salmon entering and spawning in Electronic supplementary material The online version of this article (
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