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.

Ecological regime shift in the Northeast Atlantic Ocean revealed from the unprecedented reduction in marine growth of Atlantic salmon.

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.

Time series covering up to four decades reveals major changes and drivers of marine growth and proportion of repeat spawners in an Atlantic salmon population.

Wild Atlantic salmon populations have declined in many regions and are affected by diverse natural and anthropogenic factors. To facilitate management guidelines, precise knowledge of mechanisms driving population changes in demographics and life history traits is needed.Our analyses were conducted on (a) age and growth data from scales of salmon caught by angling in the river Etneelva, Norway, covering smolt year classes from 1980 to 2018, (b) extensive sampling of the whole spawning run in the fish trap from 2013 onwards, and (c) time series of sea surface temperature, zooplankton biomass, and salmon lice infestation intensity.Marine growth during the first year at sea displayed a distinct stepwise decline across the four decades. Simultaneously, the population shifted from predominantly 1SW to 2SW salmon, and the proportion of repeat spawners increased from 3 to 7%. The latter observation is most evident in females and likely due to decreased marine exploitation. Female repeat spawners tended to be less catchable than males by anglers.Depending on the time period analyzed, marine growth rate during the first year at sea was both positively and negatively associated with sea surface temperature. Zooplankton biomass was positively associated with growth, while salmon lice infestation intensity was negatively associated with growth.Collectively, these results are likely to be linked with both changes in oceanic conditions and harvest regimes. Our conflicting results regarding the influence of sea surface temperature on marine growth are likely to be caused by long-term increases in temperature, which may have triggered (or coincided with) ecosystem shifts creating generally poorer growth conditions over time, but within shorter datasets warmer years gave generally higher growth. We encourage management authorities to expand the use of permanently monitored reference rivers with complete trapping facilities, like the river Etneelva, generating valuable long-term data for future analyses.

Introgression from farmed escapees affects the full life cycle of wild Atlantic salmon.

After a half a century of salmon farming, we have yet to understand how the influx of genes from farmed escapees affects the full life history of Atlantic salmon (Salmo salar L.) in the wild. Using scale samples of over 6900 wild adult salmon from 105 rivers, we document that increased farmed genetic ancestry is associated with increased growth throughout life and a younger age at both seaward migration and sexual maturity. There was large among-population variation in the effects of introgression. Most saliently, the increased growth at sea following introgression declined with the population's average growth potential. Variation at two major-effect loci associated with age at maturity was little affected by farmed genetic ancestry and could not explain the observed phenotypic effects of introgression. Our study provides knowledge crucial for predicting the ecological and evolutionary consequences of increased aquaculture production worldwide.

Gene flow from domesticated escapes alters the life history of wild Atlantic salmon.

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.