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.
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.
Ecological regime shifts are abrupt changes in the structure and function of ecosystems that persist over time, but evidence of contemporary regime shifts are rare. Historical scale data from 52,384 individual wild Atlantic salmon caught in 180 rivers from 1989 to 2017 reveal that growth of Atlantic salmon across the Northeast Atlantic Ocean abruptly decreased following the year 2004. At the same time, the proportion of early maturing Atlantic salmon decreased. These changes occurred after a marked decrease in the extent of Arctic water in the Norwegian Sea, a subsequent warming of spring water temperature before Atlantic salmon entering the sea, and an approximately 50% reduction of zooplankton across large geographic areas of the Northeast Atlantic Ocean. A sudden decrease in growth was also observed among Atlantic mackerel in the Norwegian Sea. Our results point toward an ecosystem-scale regime shift in the Northeast Atlantic Ocean.
The impact of salmon lice on the survival of migrating Atlantic salmon smolts was studied by comparing the adult returns of sea-ranched smolts treated for sea lice using emamectin benzoate or substance EX with untreated control groups in the River Dale in western Norway. A total of 143 500 smolts were released in 35 release groups in freshwater from 1997 to 2009 and in the fjord system from 2007 to 2009. The adult recaptures declined gradually with release year and reached minimum levels in 2007. This development corresponded with poor marine growth and increased age at maturity of ranched salmon and in three monitored salmon populations and indicated unfavourable conditions in the Norwegian Sea. The recapture rate of treated smolts was significantly higher than the controls in three of the releases performed: the only release in 1997, one of three in 2002 and the only group released in sea water in 2007. The effect of treating the smolts against salmon lice was smaller than the variability in return rates between release groups, and much smaller that variability between release years, but its overall contribution was still significant (P < 0.05) and equivalent to an odds ratio of the probability of being recaptured of 1.17 in favour of the treated smolts. Control fish also tended to be smaller as grilse (P = 0.057), possibly due to a sublethal effect of salmon lice.
Norway is the world’s largest producer of farmed Atlantic salmon and is home to ∼400 rivers containing wild salmon populations. Farmed escapees, a reoccurring challenge of all cage-based marine aquaculture, pose a threat to the genetic integrity, productivity, and evolutionary trajectories of wild populations. Escapees have been monitored in Norwegian rivers since 1989, and, a second-generation programme was established in 2014. The new programme includes data from summer angling, autumn angling, broodstock sampling, and snorkelling surveys in >200 rivers, and >25 000 scale samples are analysed annually. In 2014–2017, escapees were observed in two-thirds of rivers surveyed each year, and between 15 and 30 of the rivers had >10% recorded escapees annually. In the period 1989–2017, a reduction in the proportion of escapees in rivers was observed, despite a >6-fold increase in aquaculture production. This reflected improved escape prevention, and possibly changes in production methods that influence post-escape behaviour. On average, populations estimated to experience the greatest genetic introgression from farmed salmon up to 2014 also had the largest proportions of escapees in 2014–2017. Thus, populations already most affected are those at greatest risk of further impacts. These data feed into the annual risk-assessment of Norwegian aquaculture and form the basis for directing mitigation efforts.
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