Temporal allele frequency changes in large-effect loci reveal potential fishing impacts on salmon life-history diversity.

Fishing has the potential to influence the life-history traits of exploited populations. However, our understanding of how fisheries can induce evolutionary genetic changes remains incomplete. The discovery of large-effect loci linked with ecologically important life-history traits, such as age at maturity in Atlantic salmon (Salmo salar), provides an opportunity to study the impacts of temporally varying fishing pressures on these traits. A 93-year archive of fish scales from wild Atlantic salmon catches from the northern Baltic Sea region allowed us to monitor variation in adaptive genetic diversity linked with age at maturity of wild Atlantic salmon populations. The dataset consisted of samples from both commercial and recreational fisheries that target salmon on their spawning migration. Using a genotyping-by-sequencing approach (GT-seq), we discovered strong within-season allele frequency changes at the vgll3 locus linked with Atlantic salmon age at maturity: fishing in the early season preferentially targeted the vgll3 variant linked with older maturation. We also found within-season temporal variation in catch proportions of different wild Atlantic salmon subpopulations. Therefore, selective pressures of harvesting may vary depending on the seasonal timing of fishing, which has the potential to cause evolutionary changes in key life-history traits and their diversity. This knowledge can be used to guide fisheries management to reduce the effects of fishing practices on salmon life-history diversity. Thus, this study provides a tangible example of using genomic approaches to infer, monitor and help mitigate human impacts on adaptively important genetic variation in nature.

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.

Genetic gradient of a host-parasite pair along a river persisted ten years against physical mobility: Baltic Salmo salar vs. Gyrodactylus salaris.

The Atlantic salmon, Salmo salar L., in the Tornio River in the Northern Baltic Sea basin accommodates a monogenean ectoparasite, Gyrodactylus salaris. The aim of the study was to understand the population structure of apparently co-adapted host-parasite system: no parasite-associated mortality has been reported. The parasite burden among salmon juveniles (parr) was monitored along 460km of the river in 2000-2009. Among the parr, 33.0% were infected (nfish=1913). The genetic structure of the parasite population was studied by sequencing an anonymous nuclear DNA marker (ADNAM1, three main genotypes) and mitochondrial CO1 (three clades, six haplotypes). During the ten years, the parasite population was strongly and stably genetically differentiated among up- and downstream nurseries (nADNAM1=411, FST=0.579; nCO1=443, FST=0.534). Infection prevalence among the smolts migrating to sea was higher than in the sedentary parr populations (82.2%, nfish=129). The spatial differentiation observed among the sedentary juveniles was reflected temporally in the smolt run: parasite genotypes dominating the upper part of the river arrived later than downstream dwellers (medians June 4 and June 2) to the trap 7km from the river mouth. The nuclear and mitochondrial markers were in stable disequilibrium which was not relaxed in the contact zone or among the smolts where the parasite clones often met on individual fish. Only five parasite specimens on smolts (nworms=217) were putative recent sexual recombinants. The contribution of extant salmon hatcheries into the infection was negligible. The host salmon population in Tornio River is known to show significant spatial differentiation (FST=0.022). The stable spatial genetic structure of the parasite against the high physical mobility suggested a possibility of local co-adaptation of the host-parasite subpopulations.

Small Tails Tell Tall Tales--Intra-Individual Variation in the Stable Isotope Values of Fish Fin.

BACKGROUND: Fish fin is a widely used, non-lethal sample material in studies using stable isotopes to assess the ecology of fishes. However, fish fin is composed of two distinct tissues (ray and membrane) which may have different stable isotope values and are not homogeneously distributed within a fin. As such, estimates of the stable isotope values of a fish may vary according to the section of fin sampled. METHODS: To assess the magnitude of this variation, we analysed carbon (δ13C), nitrogen (δ15N), hydrogen (δ2H) and oxygen (δ18O) stable isotopes of caudal fin from juvenile, riverine stages of Atlantic salmon (Salmo salar) and brown trout (Salmo trutta). Individual fins were sub-sectioned into tip, mid and base, of which a further subset were divided into ray and membrane. FINDINGS: Isotope variation between fin sections, evident in all four elements, was primarily related to differences between ray and membrane. Base sections were13C depleted relative to tip (~1‰) with equivalent variation evident between ray and membrane. A similar trend was evident in δ2H, though the degree of variation was far greater (~10‰). Base and ray sections were 18O enriched (~2‰) relative to tip and membrane, respectively. Ray and membrane sections displayed longitudinal variation in 15N mirroring that of composite fin (~1‰), indicating that variation in15N values was likely related to ontogenetic variation. CONCLUSIONS: To account for the effects of intra-fin variability in stable isotope analyses we suggest that researchers sampling fish fin, in increasing priority, 1) also analyse muscle (or liver) tissue from a subsample of fish to calibrate their data, or 2) standardize sampling by selecting tissue only from the extreme tip of a fin, or 3) homogenize fins prior to analysis.

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.

Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar).

Migrations between different habitats are key events in the lives of many organisms. Such movements involve annually recurring travel over long distances usually triggered by seasonal changes in the environment. Often, the migration is associated with travel to or from reproduction areas to regions of growth. Young anadromous Atlantic salmon (Salmo salar) emigrate from freshwater nursery areas during spring and early summer to feed and grow in the North Atlantic Ocean. The transition from the freshwater ('parr') stage to the migratory stage where they descend streams and enter salt water ('smolt') is characterized by morphological, physiological and behavioural changes where the timing of this parr-smolt transition is cued by photoperiod and water temperature. Environmental conditions in the freshwater habitat control the downstream migration and contribute to within- and among-river variation in migratory timing. Moreover, the timing of the freshwater emigration has likely evolved to meet environmental conditions in the ocean as these affect growth and survival of the post-smolts. Using generalized additive mixed-effects modelling, we analysed spatio-temporal variations in the dates of downstream smolt migration in 67 rivers throughout the North Atlantic during the last five decades and found that migrations were earlier in populations in the east than the west. After accounting for this spatial effect, the initiation of the downstream migration among rivers was positively associated with freshwater temperatures, up to about 10 °C and levelling off at higher values, and with sea-surface temperatures. Earlier migration occurred when river discharge levels were low but increasing. On average, the initiation of the smolt seaward migration has occurred 2.5 days earlier per decade throughout the basin of the North Atlantic. This shift in phenology matches changes in air, river, and ocean temperatures, suggesting that Atlantic salmon emigration is responding to the current global climate changes.