Overruled by nature: A plastic response to environmental change disconnects a gene and its trait.

In Atlantic salmon, age at maturation is a life history trait governed by a sex-specific trade-off between reproductive success and survival. Following environmental changes across large areas of the Northeast Atlantic, many populations currently display smaller size at age and higher age at maturation. However, whether these changes reflect rapid evolution or plasticity is unknown. Approximately 1500 historical and contemporary salmon from the river Etne in Western Norway, genotyped at 50,000 SNPs, revealed three loci associated with age at maturation. These included vgll3 and six6 which collectively explained 36%-50% of the age at maturation variation in the 1983-1984 period. These two loci also displayed sex-specific epistasis, as the effect of six6 was only detected in males bearing two copies of the late maturation allele for vgll3. Strikingly, despite allelic frequencies at vgll3 remaining unchanged, the combined influence of these genes was nearly absent in all samples from 2013 to 2016, and genome-wide heritability strongly declined between the two time-points. The difference in age at maturation between males and females was upheld in the population despite the loss of effect from the candidate loci, which strongly points towards additional causative mechanisms resolving the sexual conflict. Finally, because admixture with farmed escaped salmon was excluded as the origin of the observed disconnection between gene(s) and maturation age, we conclude that the environmental changes observed in the North Atlantic during the past decades have led to bypassing of the influence of vgll3 and six6 on maturation through growth-driven plasticity.

DNA and scale reading to identify repeat spawning in Atlantic salmon: Unique insights into patterns of iteroparity.

Iteroparity represents an important but often overlooked component of life history in anadromous Atlantic salmon. Here, we combined individual DNA profiling and scale reading to identify repeat spawners among ~8000 adult salmon captured in a fish trap in the river Etne, Norway, in the period 2015-2019. Additionally, 171 outward migrating kelts were captured in the spring of 2018-2020 and identified using molecular methods to estimate weight loss since ascending the river to spawn. The overall frequency of repeat spawners identified using molecular methods and scale reading combined was 7% in females and 3% in males (5% in total). Most of these (83%) spent one full year reconditioning at sea before returning for their second spawning, with a larger body size compared with their size at first spawning, gaining on average 15.9 cm. A single female migrating back into the river for a fifth breeding season was also identified. On average, kelts lost 40% bodyweight in the river, and more female than male kelts were captured during outward migration. The date of arrival in the upstream fish trap was significantly but moderately correlated between maiden and second entry to the river for alternate and consecutive spawners. The estimated contribution from repeat spawners to the total number of eggs deposited in the river each year varied between 2% and 17% (average 12%). Molecular-based methods marginally underestimated the number of repeat spawners compared with scale reading (5% vs 7%) likely due to a small number of returning spawners not being trapped and sampled. Differences between the methods were most evident when classifying the spawning strategy (alternate or consecutive-year repeat spawners), where the scale method identified proportionally more consecutive-year repeat spawners than the molecular method. This unique data set reveals previously unstudied components of this life history strategy and demonstrates the importance of repeat spawners in population recruitment.

Introgression of domesticated salmon changes life history and phenology of a wild salmon population.

The release of domesticated conspecifics into the natural environment, whether deliberate or accidental, has the potential to alter the genetic integrity and evolutionary trajectory of wild populations. This widespread challenge is of particular concern for wild Atlantic salmon. By investigating phenotypic differences between the offspring of domesticated, hybrid, and wild Atlantic salmon released into the natural environment, earlier studies have documented the short-term consequences of introgression from domesticated fish into wild salmon populations. However, few studies have investigated the joined product of introgression and natural selection after several generations. Here, we investigated the phenotypic response of an Atlantic salmon population that has been subjected to an average of 24% genetic admixture by domesticated conspecifics escaping from fish farms over three decades (approximately 6-7 generations). Individual levels of admixture were positively correlated with increased size at the smolt and adult stages for both sexes, a decrease in the age of male smolts, and a decrease in the age at maturity for males. These life history changes are presumably the consequence of the well-documented directional selection for increased growth in domesticated salmon and are likely maladaptive. However, the most novel result of this study is that admixture was positively linked with delayed date of return to the river, with highly admixed fish arriving up to 26 days later than nonadmixed fish. Potentially, this phenological change provides admixed individuals with a survival advantage in the later phase of the life cycle as it reduces their period of exposure to selection through rod and line angling. We, therefore, conclude that while gene flow from domesticated conspecifics changes life history and phenological traits of wild Atlantic salmon populations, most of which are likely to be maladaptive, when pressured by additional anthropogenic challenges, some changes may confer a fitness advantage for a short part of the life cycle.

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.