Sex-specific overdominance at the maturation vgll3 gene for reproductive fitness in wild Atlantic salmon.

Linking reproductive fitness with adaptive traits at the genomic level can shed light on the mechanisms that produce and maintain sex-specific selection. Here, we construct a multigenerational pedigree to investigate sex-specific selection on a maturation gene, vgll3, in a wild Atlantic salmon population. The vgll3 locus is responsible for ~40% of the variation in maturation (sea age at first reproduction). Genetic parentage analysis was conducted on 18,265 juveniles (parr) and 685 adults collected at the same spawning ground over eight consecutive years. A high proportion of females (26%) were iteroparous and reproduced two to four times in their lifetime. A smaller proportion of males (9%) spawned at least twice in their lifetime. Sex-specific patterns of reproductive fitness were related to vgll3 genotype. Females showed a pattern of overdominance where vgll3*EL genotypes had three-fold more total offspring than homozygous females. In contrast, males demonstrated that late-maturing vgll3*LL individuals had two-fold more offspring than either vgll3*EE or vgll3*EL males. Taken together, these data suggest that balancing selection in females contributes to the maintenance of variation at this locus via increased fitness of iteroparous vgll3*EL females. This study demonstrates the utility of multigenerational pedigrees for uncovering complex patterns of reproduction, sex-specific selection and the maintenance of genetic variation.

Active feeding of downstream migrating juvenile pink salmon (Oncorhynchus gorbuscha) revealed in a large Barents Sea river using diet and stable isotope analysis.

The recent, rapid spreading of non-native pink salmon Oncorhynchus gorbuscha in the North Atlantic area has raised concerns about their possible negative impacts on native salmonid species. Potential interactions include competition for food resources during the short freshwater phase of juvenile O. gorbuscha, but little is known about their feeding behavior in the newly occupied North Atlantic rivers. Using stable isotope and stomach content analyses, patterns of freshwater feeding of non-native O. gorbuscha fry were studied in a large Fennoscandian river, the Teno, that discharges to the Barents Sea. Changes in stable isotope values (δ13 C, δ15 N, δ34 S) and stomach contents from the period of emergence (April to mid-May) to estuarine entry (late May/June) were examined and provided both temporally integrated and short-term indicators of freshwater feeding dependency. In addition, the occurrence of juvenile O. gorbuscha and changes in their length and weight during their emergence/migration period were investigated. Juvenile O. gorbuscha were at the spawning grounds from April through to mid-May with abundance peaking in mid-May. Fish moved to the estuary by late May and their abundance decreased toward June, and their body size increased concurrently. Stomach analyses indicated no feeding activity in April-early May in the spawning areas, but the stomach fullness indices increased markedly in fish sampled in the estuary in May and June. The most important prey items in stomachs were Chironomidae and Ephemeroptera larvae. Significant changes in all analysed stable isotopes were detected among sample periods, with a peak in mid-May and June showing significantly lower values than other sample periods. A change from the higher values reflective of parental marine feeding to the lower values reflective of freshwater feeding indicated active in-river feeding by juveniles during the study period. The documented active freshwater feeding of non-native juvenile O. gorbuscha suggests potential resource competition with native fluvial fishes, particularly salmonids.

Spawning migration behaviour of sea trout (Salmo trutta L.) in a boreal river system: effects of flow conditions and obstacles on migratory activity.

In this study, radio telemetry was used to examine the upstream spawning migration behaviour of anadromous brown trout (sea trout), Salmo trutta L., in a boreal river system, the River Isojoki, western Finland. The aim was to study the movement activity and migration characteristics of trout during the upstream spawning migration, as well as to locate the important spawning habitats and study the spawning characteristics. Furthermore, the authors analysed how flow conditions and a hydropower dam, with adjacent fishways, affected the upstream spawning migration. Tagged trout spawned in both the main stem and four tributaries, with spawning taking place from early October to November. The movement activity of radio-tagged trout was influenced by a hydropower dam (Perus dam), with spring migrators spending prolonged periods at the dam area, postponing the migration upstream. Flow conditions affected the total time spent at the dam area, as well as the movement activity in the free-flowing sections above the dam, with increasing flow stimulating activity. In addition, time of river ascent and location of spawning area had a significant effect on the movement activity of tagged trout. These results are further evidence that synergistic effects of flow and migratory obstacles can negatively influence migrations of anadromous fish, regardless of constructed fishways. The management of flow regimes and the efficiency of fishways are vital, as climate change will likely influence the flow and increase the water temperature of boreal river systems, further aggravating issues caused by obstacles.

Development of invasive pink salmon (Oncorhynchus gorbuscha Walbaum) eggs in a large Barents Sea river.

The spawning and egg development of invasive pink salmon Oncorhynchus gorbuscha were investigated in the large River Teno in the Barents Sea area where they spawned for the first time on a large scale in 2021. The spawning period started in early August and egg development was rapid. All eggs were eyed by mid-September and the first juveniles hatched in late September. In early October most eggs had hatched. Degree-days in water temperature suggested that egg deposition had mostly taken place in early August. Early egg development is discussed in relation to possible consequences for survival.

Time spent in distinct life history stages has sex-specific effects on reproductive fitness in wild Atlantic salmon.

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4-year pedigree to investigate if time spent in two distinct life history stages has sex-specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: -33.9% offspring/FW and -32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex-specific consequence on female reproductive fitness, demonstrating a life history trade-off between maturation and reproduction in wild Atlantic salmon.

Home ground advantage: Local Atlantic salmon have higher reproductive fitness than dispersers in the wild.

A long-held, but poorly tested, assumption in natural populations is that individuals that disperse into new areas for reproduction are at a disadvantage compared to individuals that reproduce in their natal habitat, underpinning the eco-evolutionary processes of local adaptation and ecological speciation. Here, we capitalize on fine-scale population structure and natural dispersal events to compare the reproductive success of local and dispersing individuals captured on the same spawning ground in four consecutive parent-offspring cohorts of wild Atlantic salmon (Salmo salar). Parentage analysis conducted on adults and juvenile fish showed that local females and males had 9.6 and 2.9 times higher reproductive success than dispersers, respectively. Our results reveal how higher reproductive success in local spawners compared to dispersers may act in natural populations to drive population divergence and promote local adaptation over microgeographic spatial scales without clear morphological differences between populations.

Co-inheritance of sea age at maturity and iteroparity in the Atlantic salmon vgll3 genomic region.

Co-inheritance in life-history traits may result in unpredictable evolutionary trajectories if not accounted for in life-history models. Iteroparity (the reproductive strategy of reproducing more than once) in Atlantic salmon (Salmo salar) is a fitness trait with substantial variation within and among populations. In the Teno River in northern Europe, iteroparous individuals constitute an important component of many populations and have experienced a sharp increase in abundance in the last 20 years, partly overlapping with a general decrease in age structure. The physiological basis of iteroparity bears similarities to that of age at first maturity, another life-history trait with substantial fitness effects in salmon. Sea age at maturity in Atlantic salmon is controlled by a major locus around the vgll3 gene, and we used this opportunity demonstrate that these two traits are co-inherited around this genome region. The odds ratio of survival until second reproduction was up to 2.4 (1.8-3.5 90% CI) times higher for fish with the early-maturing vgll3 genotype (EE) compared to fish with the late-maturing genotype (LL). The L allele was dominant in individuals remaining only one year at sea before maturation, but the dominance was reversed, with the E allele being dominant in individuals maturing after two or more years at sea. Post hoc analysis indicated that iteroparous fish with the EE genotype had accelerated growth prior to first reproduction compared to first-time spawners, across all age groups, whereas this effect was not detected in fish with the LL genotype. These results broaden the functional link around the vgll3 genome region and help us understand constraints in the evolution of life-history variation in salmon. Our results further highlight the need to account for genetic correlations between fitness traits when predicting demographic changes in changing environments.

Rapid sex-specific evolution of age at maturity is shaped by genetic architecture in Atlantic salmon.

Understanding the mechanisms by which populations adapt to their environments is a fundamental aim in biology. However, it remains challenging to identify the genetic basis of traits, provide evidence of genetic changes and quantify phenotypic responses. Age at maturity in Atlantic salmon represents an ideal trait to study contemporary adaptive evolution as it has been associated with a single locus in the vgll3 region and has also strongly changed in recent decades. Here, we provide an empirical example of contemporary adaptive evolution of a large-effect locus driving contrasting sex-specific evolutionary responses at the phenotypic level. We identified an 18% decrease in the vgll3 allele associated with late maturity in a large and diverse salmon population over 36 years, induced by sex-specific selection during sea migration. Those genetic changes resulted in a significant evolutionary response only in males, due to sex-specific dominance patterns and vgll3 allelic effects. The vgll3 allelic and dominance effects differed greatly in a second population and were likely to generate different selection and evolutionary patterns. Our study highlights the importance of knowledge of genetic architecture to better understand fitness trait evolution and phenotypic diversity. It also emphasizes the potential role of adaptive evolution in the trend towards earlier maturation observed in numerous Atlantic salmon populations worldwide.

Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes.

Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine-scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene-environment association and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci could be adaptively important in Atlantic salmon at subdrainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis and immune defence. These included the large-effect age-at-maturity gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations and that is also a candidate for local selection over the global range of Atlantic salmon. This region colocalized with a haplotype strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to upstream catchment area and covaries with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research.

Single nucleotide polymorphisms to discriminate different classes of hybrid between wild Atlantic salmon and aquaculture escapees.

Many wild Atlantic salmon (Salmo salar) populations are threatened by introgressive hybridization from domesticated fish that have escaped from aquaculture facilities. A detailed understanding of the hybridization dynamics between wild salmon and aquaculture escapees requires discrimination of different hybrid classes; however, markers currently available to discriminate the two types of parental genome have limited power to do this. Using a high-density Atlantic salmon single nucleotide polymorphism (SNP) array, in combination with pooled-sample allelotyping and an Fst outlier approach, we identified 200 SNPs that differentiated an important Atlantic salmon stock from the escapees potentially hybridizing with it. By simulating multiple generations of wild-escapee hybridization, involving wild populations in two major phylogeographic lineages and a genetically diverse set of escapees, we showed that both the complete set of SNPs and smaller subsets could reliably assign individuals to different hybrid classes up to the third hybrid (F3) generation. This set of markers will be a useful tool for investigating the genetic interactions between native wild fish and aquaculture escapees in many Atlantic salmon populations.

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.

Low but significant genetic differentiation underlies biologically meaningful phenotypic divergence in a large Atlantic salmon population.

Despite decades of research assessing the genetic structure of natural populations, the biological meaning of low yet significant genetic divergence often remains unclear due to a lack of associated phenotypic and ecological information. At the same time, structured populations with low genetic divergence and overlapping boundaries can potentially provide excellent models to study adaptation and reproductive isolation in cases where high-resolution genetic markers and relevant phenotypic and life history information are available. Here, we combined single nucleotide polymorphism (SNP)-based population inference with extensive phenotypic and life history data to identify potential biological mechanisms driving fine-scale subpopulation differentiation in Atlantic salmon (Salmo salar) from the Teno River, a major salmon river in Europe. Two sympatrically occurring subpopulations had low but significant genetic differentiation (FST  = 0.018) and displayed marked differences in the distribution of life history strategies, including variation in juvenile growth rate, age at maturity and size within age classes. Large, late-maturing individuals were virtually absent from one of the two subpopulations, and there were significant differences in juvenile growth rates and size at age after oceanic migration between individuals in the respective subpopulations. Our findings suggest that different evolutionary processes affect each subpopulation and that hybridization and subsequent selection may maintain low genetic differentiation without hindering adaptive divergence.

Genome-wide SNP analysis reveals a genetic basis for sea-age variation in a wild population of Atlantic salmon (Salmo salar).

Delaying sexual maturation can lead to larger body size and higher reproductive success, but carries an increased risk of death before reproducing. Classical life history theory predicts that trade-offs between reproductive success and survival should lead to the evolution of an optimal strategy in a given population. However, variation in mating strategies generally persists, and in general, there remains a poor understanding of genetic and physiological mechanisms underlying this variation. One extreme case of this is in the Atlantic salmon (Salmo salar), which can show variation in the age at which they return from their marine migration to spawn (i.e. their 'sea age'). This results in large size differences between strategies, with direct implications for individual fitness. Here, we used an Illumina Infinium SNP array to identify regions of the genome associated with variation in sea age in a large population of Atlantic salmon in Northern Europe, implementing individual-based genome-wide association studies (GWAS) and population-based FST outlier analyses. We identified several regions of the genome which vary in association with phenotype and/or selection between sea ages, with nearby genes having functions related to muscle development, metabolism, immune response and mate choice. In addition, we found that individuals of different sea ages belong to different, yet sympatric populations in this system, indicating that reproductive isolation may be driven by divergence between stable strategies. Overall, this study demonstrates how genome-wide methodologies can be integrated with samples collected from wild, structured populations to understand their ecology and evolution in a natural context.

Fish scales and SNP chips: SNP genotyping and allele frequency estimation in individual and pooled DNA from historical samples of Atlantic salmon (Salmo salar).

BACKGROUND: DNA extracted from historical samples is an important resource for understanding genetic consequences of anthropogenic influences and long-term environmental change. However, such samples generally yield DNA of a lower amount and quality, and the extent to which DNA degradation affects SNP genotyping success and allele frequency estimation is not well understood. We conducted high density SNP genotyping and allele frequency estimation in both individual DNA samples and pooled DNA samples extracted from dried Atlantic salmon (Salmo salar) scales stored at room temperature for up to 35 years, and assessed genotyping success, repeatability and accuracy of allele frequency estimation using a high density SNP genotyping array. RESULTS: In individual DNA samples, genotyping success and repeatability was very high (> 0.973 and > 0.998, respectively) in samples stored for up to 35 years; both increased with the proportion of DNA of fragment size > 1000 bp. In pooled DNA samples, allele frequency estimation was highly repeatable (Repeatability = 0.986) and highly correlated with empirical allele frequency measures (Mean Adjusted R2 = 0.991); allele frequency could be accurately estimated in > 95% of pooled DNA samples with a reference group of at least 30 individuals. SNPs located in polyploid regions of the genome were more sensitive to DNA degradation: older samples had lower genotyping success at these loci, and a larger reference panel of individuals was required to accurately estimate allele frequencies. CONCLUSIONS: SNP genotyping was highly successful in degraded DNA samples, paving the way for the use of degraded samples in SNP genotyping projects. DNA pooling provides the potential for large scale population genetic studies with fewer assays, provided enough reference individuals are also genotyped and DNA quality is properly assessed beforehand. We provide recommendations for future studies intending to conduct high-throughput SNP genotyping and allele frequency estimation in historical samples.