Autumn outmigrants in brown trout (Salmo trutta) are not a demographic dead-end.

Genetic identity analysis and PIT (passive integrated transponder) tagging were used to examine the freshwater return rates and phenotypic characteristics of n = 1791 downstream migrating juvenile Salmo trutta in the Burrishoole catchment (northwest Ireland) across the period September 2017 to December 2020. In this system, juveniles out-migrate (move from freshwater into brackish or marine habitats) in every month of the year, with distinct seasonal peaks in spring (March through June; mostly silvered smolts) and autumn (September through December; mostly younger, unsilvered fry or parr). Both types exhibited a sex-bias towards females, which was stronger in spring (78% females) than in autumn outmigrants (67%). Sixty-nine returning fish were matched back to previous juvenile outmigrants, and similar return rates were found for spring outmigrants (5.0%), autumn outmigrants (3.3%) and fish that out-migrated outside of spring or autumn (2.8%). Spring and autumn outmigrants returned at similar dates (typically mid to late July), but autumn fish were away for longer periods (median = 612 days; spring outmigrants = 104 days). Autumn outmigrants were 25% smaller than spring outmigrants at outmigration and 6% smaller on their return, and within both groups smaller/younger outmigrants spent longer away than larger/older outmigrants. Autumn outmigrants were more likely to return unsilvered as "slob" trout (84%) than spring outmigrants (31%), suggesting they make greater use of brackish habitats that might be safer, but less productive, than fully marine habitats. Nonetheless, both types also produced silvered "sea trout" (≥1+ sea-age), implying neither is locked into a single life-history strategy. The findings emphasise that autumn outmigrants and the transitional habitats that support their persistence should not be overlooked in salmonid management and conservation.

Alternative migratory tactics in brown trout (Salmo trutta) are underpinned by divergent regulation of metabolic but not neurological genes.

The occurrence of alternative morphs within populations is common, but the underlying molecular mechanisms remain poorly understood. Many animals, for example, exhibit facultative migration, where two or more alternative migratory tactics (AMTs) coexist within populations. In certain salmonid species, some individuals remain in natal rivers all their lives, while others (in particular, females) migrate to sea for a period of marine growth. Here, we performed transcriptional profiling ("RNA-seq") of the brain and liver of male and female brown trout to understand the genes and processes that differentiate between migratory and residency morphs (AMT-associated genes) and how they may differ in expression between the sexes. We found tissue-specific differences with a greater number of genes expressed differentially in the liver (n = 867 genes) compared with the brain (n = 10) between the morphs. Genes with increased expression in resident livers were enriched for Gene Ontology terms associated with metabolic processes, highlighting key molecular-genetic pathways underlying the energetic requirements associated with divergent migratory tactics. In contrast, smolt-biased genes were enriched for biological processes such as response to cytokines, suggestive of possible immune function differences between smolts and residents. Finally, we identified evidence of sex-biased gene expression for AMT-associated genes in the liver (n = 12) but not the brain. Collectively, our results provide insights into tissue-specific gene expression underlying the production of alternative life histories within and between the sexes, and point toward a key role for metabolic processes in the liver in mediating divergent physiological trajectories of migrants versus residents.

Domestication-induced reduction in eye size revealed in multiple common garden experiments: The case of Atlantic salmon (Salmo salar L.).

Domestication leads to changes in traits that are under directional selection in breeding programmes, though unintentional changes in nonproduction traits can also arise. In offspring of escaping fish and any hybrid progeny, such unintentionally altered traits may reduce fitness in the wild. Atlantic salmon breeding programmes were established in the early 1970s, resulting in genetic changes in multiple traits. However, the impact of domestication on eye size has not been studied. We measured body size corrected eye size in 4000 salmon from six common garden experiments conducted under artificial and natural conditions, in freshwater and saltwater environments, in two countries. Within these common gardens, offspring of domesticated and wild parents were crossed to produce 11 strains, with varying genetic backgrounds (wild, domesticated, F1 hybrids, F2 hybrids and backcrosses). Size-adjusted eye size was influenced by both genetic and environmental factors. Domesticated fish reared under artificial conditions had smaller adjusted eye size when compared to wild fish reared under identical conditions, in both the freshwater and marine environments, and in both Irish and Norwegian experiments. However, in parr that had been introduced into a river environment shortly after hatching and sampled at the end of their first summer, differences in adjusted eye size observed among genetic groups were of a reduced magnitude and were nonsignificant in 2-year-old sea migrating smolts sampled in the river immediately prior to sea entry. Collectively, our findings could suggest that where natural selection is present, individuals with reduced eye size are maladapted and consequently have reduced fitness, building on our understanding of the mechanisms that underlie a well-documented reduction in the fitness of the progeny of domesticated salmon, including hybrid progeny, in the wild.

Genetic stock identification of Atlantic salmon (Salmo salar) populations in the southern part of the European range.

BACKGROUND: Anadromous migratory fish species such as Atlantic salmon (Salmo salar) have significant economic, cultural and ecological importance, but present a complex case for management and conservation due to the range of their migration. Atlantic salmon exist in rivers across the North Atlantic, returning to their river of birth with a high degree of accuracy; however, despite continuing efforts and improvements in in-river conservation, they are in steep decline across their range. Salmon from rivers across Europe migrate along similar routes, where they have, historically, been subject to commercial netting. This mixed stock exploitation has the potential to devastate weak and declining populations where they are exploited indiscriminately. Despite various tagging and marking studies, the effect of marine exploitation and the marine element of the salmon lifecycle in general, remain the "black-box" of salmon management. In a number of Pacific salmonid species and in several regions within the range of the Atlantic salmon, genetic stock identification and mixed stock analysis have been used successfully to quantify exploitation rates and identify the natal origins of fish outside their home waters - to date this has not been attempted for Atlantic salmon in the south of their European range. RESULTS: To facilitate mixed stock analysis (MSA) of Atlantic salmon, we have produced a baseline of genetic data for salmon populations originating from the largest rivers from Spain to northern Scotland, a region in which declines have been particularly marked. Using 12 microsatellites, 3,730 individual fish from 57 river catchments have been genotyped. Detailed patterns of population genetic diversity of Atlantic salmon at a sub-continent-wide level have been evaluated, demonstrating the existence of regional genetic signatures. Critically, these appear to be independent of more commonly recognised terrestrial biogeographical and political boundaries, allowing reporting regions to be defined. The implications of these results on the accuracy of MSA are evaluated and indicate that the success of MSA is not uniform across the range studied; our findings indicate large differences in the relative accuracy of stock composition estimates and MSA apportioning across the geographical range of the study, with a much higher degree of accuracy achieved when assigning and apportioning to populations in the south of the area studied. This result probably reflects the more genetically distinct nature of populations in the database from Spain, northwest France and southern England. Genetic stock identification has been undertaken and validation of the baseline microsatellite dataset with rod-and-line and estuary net fisheries of known origin has produced realistic estimates of stock composition at a regional scale. CONCLUSIONS: This southern European database and supporting phylogeographic and mixed-stock analyses of net samples provide a unique tool for Atlantic salmon research and management, in both their natal rivers and the marine environment. However, the success of MSA is not uniform across the area studied, with large differences in the relative accuracy of stock composition estimates and MSA apportioning, with a much higher degree of accuracy achieved when assigning and apportioning to populations in the south of the region. More broadly, this study provides a basis for long-term salmon management across the region and confirms the value of this genetic approach for fisheries management of anadromous species.

Telemetry and genetics reveal asymmetric dispersal of a lake-feeding salmonid between inflow and outflow spawning streams at a microgeographic scale.

The degree of natal philopatry relative to natal dispersal in animal populations has important demographic and genetic consequences and often varies substantially within species. In salmonid fishes, lakes have been shown to have a strong influence on dispersal and gene flow within catchments; for example, populations spawning in inflow streams are often reproductively isolated and genetically distinct from those spawning in relatively distant outflow streams. Less is known, however, regarding the level of philopatry and genetic differentiation occurring at microgeographic scales, for example, where inflow and outflow streams are separated by very small expanses of lake habitat. Here, we investigated the interplay between genetic differentiation and fine-scale spawning movements of brown trout between their lake-feeding habitat and two spawning streams (one inflow, one outflow, separated by <100 m of lake habitat). Most (69.2%) of the lake-tagged trout subsequently detected during the spawning period were recorded in just one of the two streams, consistent with natal fidelity, while the remainder were detected in both streams, creating an opportunity for these individuals to spawn in both natal and non-natal streams. The latter behavior was supported by genetic sibship analysis, which revealed several half-sibling dyads containing one individual that was sampled as a fry in the outflow and another that was sampled as fry in the inflow. Genetic clustering analyses in conjunction with telemetry data suggested that asymmetrical dispersal patterns were occurring, with natal fidelity being more common among individuals originating from the outflow than the inflow stream. This was corroborated by Bayesian analysis of gene flow, which indicated significantly higher rates of gene flow from the inflow into the outflow than vice versa. Collectively, these results reveal how a combination of telemetry and genetics can identify distinct reproductive behaviors and associated asymmetries in natal dispersal that produce subtle, but nonetheless biologically relevant, population structuring at microgeographic scales.

Natural selection acts on Atlantic salmon major histocompatibility (MH) variability in the wild.

Pathogen-driven balancing selection is thought to maintain polymorphism in major histocompatibility (MH) genes. However, there have been few empirical demonstrations of selection acting on MH loci in natural populations. To determine whether natural selection on MH genes has fitness consequences for wild Atlantic salmon in natural conditions, we compared observed genotype frequencies of Atlantic salmon (Salmo salar) surviving in a river six months after their introduction as eggs with frequencies expected from parental crosses. We found significant differences between expected and observed genotype frequencies at the MH class II alpha locus, but not at a MH class I-linked microsatellite or at seven non-MH-linked microsatellite loci. We therefore conclude that selection at the MH class II alpha locus was a result of disease-mediated natural selection, rather than any demographic event. We also show that survival was associated with additive allelic effects at the MH class II alpha locus. Our results have implications for both the conservation of wild salmon stocks and the management of disease in hatchery fish. We conclude that natural or hatchery populations have the best chance of dealing with episodic and variable disease challenges if MH genetic variation is preserved both within and among populations.

The signature of fine scale local adaptation in Atlantic salmon revealed from common garden experiments in nature.

Understanding the extent, scale and genetic basis of local adaptation (LA) is important for conservation and management. Its relevance in salmonids at microgeographic scales, where dispersal (and hence potential gene flow) can be substantial, has however been questioned. Here, we compare the fitness of communally reared offspring of local and foreign Atlantic salmon Salmo salar from adjacent Irish rivers and reciprocal F1 hybrid crosses between them, in the wild 'home' environment of the local population. Experimental groups did not differ in wild smolt output but a catastrophic flood event may have limited our ability to detect freshwater performance differences, which were evident in a previous study. Foreign parr exhibited higher, and hybrids intermediate, emigration rates from the natal stream relative to local parr, consistent with genetically based behavioural differences. Adult return rates were lower for the foreign compared to the local group. Overall lifetime success of foreigners and hybrids relative to locals was estimated at 31% and 40% (mean of both hybrid groups), respectively. The results imply a genetic basis to fitness differences among populations separated by only 50 km, driven largely by variation in smolt to adult return rates. Hence even if supplementary stocking programs obtain broodstock from neighbouring rivers, the risk of extrinsic outbreeding depression may be high.

Varying disease-mediated selection at different life-history stages of Atlantic salmon in fresh water.

Laboratory studies on associations between disease resistance and susceptibility and major histocompatibility (MH) genes in Atlantic salmon Salmo salar have shown the importance of immunogenetics in understanding the capacity of populations to fight specific diseases. However, the occurrence and virulence of pathogens may vary spatially and temporally in the wild, making it more complicated to predict the overall effect that MH genes exert on fitness of natural populations and over several life-history stages. Here we show that MH variability is a significant determinant of salmon survival in fresh water, by comparing observed and expected genotype frequencies at MH and control microsatellite loci at parr and migrant stages in the wild. We found that additive allelic effects at immunogenetic loci were more likely to determine survival than dominance deviation, and that selection on certain MH alleles varied with life stage, possibly owing to varying pathogen prevalence and/or virulence over time. Our results highlight the importance of preserving genetic diversity (particularly at MH loci) in wild populations, so that they have the best chance of adapting to new and increased disease challenges as a result of projected climate warming and increasing aquaculture.