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Migration in animals and associated adaptations to contrasting environments are underpinned by complex genetic architecture. Here, we explore the genomic basis of facultative anadromy in brown trout (Salmo trutta), wherein some individuals migrate to sea while others remain resident in natal rivers, to better understand how alternative migratory tactics (AMTs) are maintained evolutionarily. To identify genomic variants associated with AMTs, we sequenced whole genomes for 194 individual trout from five anadromous–resident population pairs, situated above and below waterfalls, in five different Irish rivers. These waterfalls act as natural barriers to upstream migration and hence we predicted that loci underpinning AMTs should be under similar divergent selection across these replicate pairs. A sliding windows based analysis revealed a highly polygenic adaptive divergence between anadromous and resident populations, encompassing 329 differentiated genomic regions. These regions were associated with 292 genes involved in various processes crucial for AMTs, including energy homeostasis, reproduction, osmoregulation, immunity, circadian rhythm and neural function. Furthermore, examining patterns of diversity we were able to link specific genes and biological processes to putative AMT trait classes: migratory‐propensity, migratory‐lifestyle and residency. Importantly, AMT outlier regions possessed higher genetic diversity than the background genome, particularly in the anadromous group, suggesting balancing selection may play a role in maintaining genetic variation. Overall, the results from this study provide important insights into the genetic architecture of migration and the evolutionary mechanisms shaping genomic diversity within and across populations. [ABSTRACT FROM AUTHOR]

The deliberate release of captive‐bred individuals, the accidental escape of domesticated strains, or the invasion of closely related conspecifics into wild populations can all lead to introgressive hybridization, which poses a challenge for conservation and wildlife management. Rates of introgression and the magnitude of associated demographic impacts vary widely across ecological contexts. However, the reasons for this variation remain poorly understood. One rarely considered phenomenon in this context is soft selection, wherein relative trait values determine success in intraspecific competition for a limiting resource. Here we develop an eco‐genetic model explicitly focussed on understanding the influence of such competitive interactions on the eco‐evolutionary dynamics of wild populations experiencing an influx of foreign/domesticated individuals. The model is applicable to any taxon that experiences natural or human‐mediated inputs of locally maladapted genotypes ('intrusion'), in addition to phenotype‐dependent competition for a limiting resource (e.g. breeding sites, feeding territories). The effects of both acute and chronic intrusion depended strongly on the relative competitiveness of intruders versus locals. When intruders were competitively inferior, density‐dependent regulation limited their reproductive success (ability to compete for limited spawning sites), which prevented strong introgression or population declines from occurring. In contrast, when intruders were competitively superior, this amplified introgression and led to increased maladaptation of the admixed population. This had negative consequences for population size and population viability. The results were sensitive to the intrusion level, the magnitude of reproductive excess, trait heritability and the extent to which intruders were maladapted relative to locals. Our findings draw attention to under‐appreciated interactions between phenotype‐dependent competitive interactions and maladaptive hybridization, which may be critical to determining the impact captive breeding programmes and domesticated escapees can have on otherwise self‐sustaining wild populations. [ABSTRACT FROM AUTHOR]

Global warming has been implicated in widespread demographic changes in Atlantic salmon Salmo salar populations, but projections of life‐history responses to future climate change are lacking. Here, we first exploit multiple decades of climate and biological data from the Burrishoole catchment in the west of Ireland to model statistical relationships between atmospheric variables, water temperature, and freshwater growth of juvenile Atlantic salmon. We then use this information to project potential changes in juvenile growth and life‐history scheduling under three shared socioeconomic pathway and representative concentration pathway scenarios from 1961 to 2100, based on an ensemble of five climate models. Historical water temperatures were well predicted with a recurrent neural network, using observation‐based atmospheric forcing data. Length‐at‐age was in turn also well predicted by cumulative growing degree days calculated from these water temperatures. Most juveniles in the Burrishoole population migrated to sea as 2‐year‐old smolts, but our future projections indicate that the system should start producing a greater proportion of 1‐year‐old smolts, as increasingly more juveniles cross a size‐based threshold in their first summer for smoltification the following spring. Those failing to cross the size‐based threshold will instead become 2‐year‐old smolts, but at a larger length relative to 2‐year‐old smolts observed currently, owing to greater overall freshwater growth opportunity. These changes in age‐ and size‐at‐seaward migration could have cascading effects on age‐ and size‐at‐maturity and reproductive output. Consequently, the seemingly small changes that our results demonstrate have the potential to cause significant shifts in population dynamics over the full life cycle. This workflow is highly applicable across the range of the Atlantic salmon, as well as to other anadromous species, as it uses openly accessible climate data and a length‐at‐age model with minimal input requirements, fostering improved general understanding of phenotypic and demographic responses to climate change and management implications. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Males and females are often subject to different and even opposing selection pressures. When a given trait has a shared genetic basis between the sexes, sexual conflict (antagonism) can arise. This can result in significant individual‐level fitness consequences that might also affect population performance, whilst anthropogenic environmental change can further exacerbate maladaptation in one or both sexes driven by sexual antagonism. Here, we develop a genetically explicit eco‐evolutionary model using an agent‐based framework to explore how a population of a facultatively migratory fish species (brown trout Salmo trutta) adapts to environmental change across a range of intersex genetic correlations for migration propensity, which influence the magnitude of sexual conflict. Our modelled focal trait represents a condition threshold governing whether individuals adopt a resident or anadromous (sea migration) tactic. Anadromy affords potential size‐mediated reproductive advantages to both males and females due to improved feeding opportunities at sea, but these can be undermined by high background marine mortality and survival/growth costs imposed by marine parasites (sea lice). We show that migration tactic frequency for a given set of environmental conditions is strongly influenced by the intersex genetic correlation, such that one sex can be dragged off its optimum more than the other. When this occurred in females in our model, population productivity was substantially reduced, but eco‐evolutionary outcomes were altered by allowing for sneaking behaviour in males. We discuss real‐world implications of our work given that anadromous salmonids are regularly challenged by sea lice infestations, which might act synergistically with other stressors such as climate change or fishing that impact marine performance, driving populations towards residency and potentially reduced resilience. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

With rapid global change, organisms in natural systems are exposed to a multitude of stressors that likely co‐occur, with uncertain impacts. We explored individual and cumulative effects of co‐occurring environmental stressors on the striking, yet poorly understood, phenomenon of facultative migration. We reared offspring of a brown trout population that naturally demonstrates facultative anadromy (sea migration), under different environmental stressor treatments and measured life history responses in terms of migratory tactics and freshwater maturation rates. Juvenile fish were exposed to reduced food availability, temperatures elevated to 1.8°C above natural conditions or both treatments in combination over 18 months of experimental tank rearing. When considered in isolation, reduced food had negative effects on the size, mass and condition of fish across the experiment. We detected variable effects of warm temperatures (negative effects on size and mass, but positive effect on lipids). When combined with food restriction, temperature effects on these traits were less pronounced, implying antagonistic stressor effects on morphological traits. Stressors combined additively, but had opposing effects on life history tactics: migration increased and maturation rates decreased under low food conditions, whereas the opposite occurred in the warm temperature treatment. Not all fish had expressed maturation or migration tactics by the end of the study, and the frequency of these 'unassigned' fish was higher in food deprivation treatments, but lower in warm treatments. Fish showing migration tactics were smaller and in poorer condition than fish showing maturation tactics, but were similar in size to unassigned fish. We further detected effects of food restriction on hypo‐osmoregulatory function of migrants that may influence the fitness benefits of the migratory tactic at sea. We also highlight that responses to multiple stressors may vary depending on the response considered. Collectively, our results indicate contrasting effects of environmental stressors on life history trajectories in a facultatively migratory species. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

We report the first application of CRISPR‐Cas technology to single species detection from environmental DNA (eDNA). Organisms shed and excrete DNA into their environment such as in skin cells and faeces, referred to as environmental DNA (eDNA). Utilising eDNA allows noninvasive monitoring with increased specificity and sensitivity. Current methods primarily employ PCR‐based techniques to detect a given species from eDNA samples, posing a logistical challenge for on‐site monitoring and potential adaptation to biosensor devices. We have developed an alternative method; coupling isothermal amplification to a CRISPR‐Cas12a detection system. This utilises the collateral cleavage activity of Cas12a, a ribonuclease guided by a highly specific single CRISPR RNA. We used the target species Salmo salar as a proof‐of‐concept test of the specificity of the assay among closely related species and to show the assay is successful at a single temperature of 37°C with signal detection at 535 nM. The specific assay, detects at attomolar sensitivity with rapid detection rates (<2.5 hr). This approach simplifies the challenge of building a biosensor device for rapid target species detection in the field and can be easily adapted to detect any species from eDNA samples from a variety of sources enhancing the capabilities of eDNA as a tool for monitoring biodiversity. [ABSTRACT FROM AUTHOR]

Brown trout Salmo trutta is endemic to Europe, western Asia and north‐western Africa; it is a prominent member of freshwater and coastal marine fish faunas. The species shows two resident (river‐resident, lake‐resident) and three main facultative migratory life histories (downstream–upstream within a river system, fluvial–adfluvial potamodromous; to and from a lake, lacustrine–adfluvial (inlet) or allacustrine (outlet) potamodromous; to and from the sea, anadromous). River‐residency v. migration is a balance between enhanced feeding and thus growth advantages of migration to a particular habitat v. the costs of potentially greater mortality and energy expenditure. Fluvial–adfluvial migration usually has less feeding improvement, but less mortality risk, than lacustrine–adfluvial or allacustrine and anadromous, but the latter vary among catchments as to which is favoured. Indirect evidence suggests that around 50% of the variability in S. trutta migration v. residency, among individuals within a population, is due to genetic variance. This dichotomous decision can best be explained by the threshold‐trait model of quantitative genetics. Thus, an individual's physiological condition (e.g., energy status) as regulated by environmental factors, genes and non‐genetic parental effects, acts as the cue. The magnitude of this cue relative to a genetically predetermined individual threshold, governs whether it will migrate or sexually mature as a river‐resident. This decision threshold occurs early in life and, if the choice is to migrate, a second threshold probably follows determining the age and timing of migration. Migration destination (mainstem river, lake, or sea) also appears to be genetically programmed. Decisions to migrate and ultimate destination result in a number of subsequent consequential changes such as parr–smolt transformation, sexual maturity and return migration. Strong associations with one or a few genes have been found for most aspects of the migratory syndrome and indirect evidence supports genetic involvement in all parts. Thus, migratory and resident life histories potentially evolve as a result of natural and anthropogenic environmental changes, which alter relative survival and reproduction. Knowledge of genetic determinants of the various components of migration in S. trutta lags substantially behind that of Oncorhynchus mykiss and other salmonines. Identification of genetic markers linked to migration components and especially to the migration–residency decision, is a prerequisite for facilitating detailed empirical studies. In order to predict effectively, through modelling, the effects of environmental changes, quantification of the relative fitness of different migratory traits and of their heritabilities, across a range of environmental conditions, is also urgently required in the face of the increasing pace of such changes. [ABSTRACT FROM AUTHOR]

Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree‐derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so‐called "paradox of stasis." To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies—which have largely been limited to birds and mammals—to study evolutionary processes on contemporary timescales. [ABSTRACT FROM AUTHOR]

Aim Most animal species live in spatially and temporally heterogeneous landscapes where resources are unevenly distributed. Consequently, individuals must adapt their migratory behaviour to optimize feeding and breeding opportunities. Here, we assess the role of life-history (anadromy) and seascape (a derivation of the concept of landscape) heterogeneity on the genetic connectivity of coastal brown trout populations ( Salmo trutta L., 1758). Location English Channel. Methods A causal modelling approach, combining geographical data with inferences on gene flow among 20 populations, deploying neutral microsatellite markers, was used to identify environmental factors influencing brown trout genetic dispersal between rivers. Alternative models of landscape permeability combining least-cost path and transect analysis were employed. The model selection procedure was based on a multiple regression analysis on distance matrices analysis ( MRDM) and a linear mixed modelling approach using maximum likelihood population effects ( MLPE). Results Landscape genetic analyses showed a hierarchical genetic structure with two main genetic units corresponding to the eastern and western marine ecoregions of the English Channel delineated by the Cotentin peninsula. Within these two regions, a model, which included parameters for depth and seabed substrate habitat features, explained significantly more variance in genetic differentiation than simple isolation-by-distance models alone. Main conclusions The genetic structure of brown trout populations within the English Channel appears to be shaped by the spatial arrangement and quality (with respect to feeding opportunities) of marine habitats, which promotes a clinal variation in migratory behaviour, which in turn determines the level of gene flow among neighbouring streams. Genetic structure thus partly reflects microgeographical responses to spatial variation in foraging conditions at sea. These results show that the marine environment, rarely considered previously, has an important role in combination with variation in freshwater environments in the evolution of life history in migratory aquatic animals. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Domestication can have adverse genetic consequences, which may reduce the fitness of individuals once released back into the wild. Many wild Atlantic salmon ( Salmo salar L.) populations are threatened by anthropogenic influences, and they are supplemented with captively bred fish. The Atlantic salmon is also widely used in selective breeding programs to increase the mean trait values for desired phenotypic traits. We analyzed a genomewide set of SNPs in three domesticated Atlantic salmon strains and their wild conspecifics to identify loci underlying domestication. The genetic differentiation between domesticated strains and wild populations was low ( FST < 0.03), and domesticated strains harbored similar levels of genetic diversity compared to their wild conspecifics. Only a few loci showed footprints of selection, and these loci were located in different linkage groups among the different wild population/hatchery strain comparisons. Simulated scenarios indicated that differentiation in quantitative trait loci exceeded that in neutral markers during the early phases of divergence only when the difference in the phenotypic optimum between populations was large. This study indicates that detecting selection using standard approaches in the early phases of domestication might be challenging unless selection is strong and the traits under selection show simple inheritance patterns. [ABSTRACT FROM AUTHOR]

We present a new R package, diveRsity, for the calculation of various diversity statistics, including common diversity partitioning statistics (θ, GST) and population differentiation statistics ( D Jost [ABSTRACT FROM AUTHOR]

Atlantic salmon ( Salmo salar) is one of the most extensively studied fish species in the world due to its significance in aquaculture, fisheries and ongoing conservation efforts to protect declining populations. Yet, limited genomic resources have hampered our understanding of genetic architecture in the species and the genetic basis of adaptation to the wide range of natural and artificial environments it occupies. In this study, we describe the development of a medium-density Atlantic salmon single nucleotide polymorphism ( SNP) array based on expressed sequence tags ( ESTs) and genomic sequencing. The array was used in the most extensive assessment of population genetic structure performed to date in this species. A total of 6176 informative SNPs were successfully genotyped in 38 anadromous and freshwater wild populations distributed across the species natural range. Principal component analysis clearly differentiated European and North American populations, and within Europe, three major regional genetic groups were identified for the first time in a single analysis. We assessed the potential for the array to disentangle neutral and putative adaptive divergence of SNP allele frequencies across populations and among regional groups. In Europe, secondary contact zones were identified between major clusters where endogenous and exogenous barriers could be associated, rendering the interpretation of environmental influence on potentially adaptive divergence equivocal. A small number of markers highly divergent in allele frequencies (outliers) were observed between (multiple) freshwater and anadromous populations, between northern and southern latitudes, and when comparing Baltic populations to all others. We also discuss the potential future applications of the SNP array for conservation, management and aquaculture. [ABSTRACT FROM AUTHOR]

Domesticated animals provide a unique opportunity to identify genomic targets of artificial selection to the captive environment. Here, we screened three independent domesticated/captive Atlantic salmon (Salmo salar) strains and their wild progenitor populations in an effort to detect potential signals of domestication selection by typing of 261 SNPs and 70 microsatellite loci. By combining information from four different neutrality tests, in total ten genomic regions showed signs of directional selection based on multiple sources of evidence. Most of the identified candidate regions were rather small ranging from zero to a few centimorgans (cM) in the female Atlantic salmon linkage map. We also evaluated how adaptation from standing variation affects adjacent SNP and microsatellite variation along the chromosomes and, by using forward simulations with strong selection, we were able to generate genetic differentiation patterns comparable to the observed data. This study highlights the significance of standing genetic variation during the early stages of adaptation and represents a useful step towards identifying functional variants involved in domestication of Atlantic salmon. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]