Abstract Rapid environmental change is exposing organisms to conditions that do not match those under which they evolved, making it increasingly important to understand how genetic variation shapes phenotypic responses to environmental stress. Since most phenotypic traits arise from interactions between genetic variation and the environments experienced throughout an organism’s lifetime, understanding the genetic architecture of these interactions is central to predicting how populations will respond to novel environments. While genotype-by-environment interactions (G×E) are well studied in quantitative genetics, identifying specific loci that contribute to environmentally dependent trait expression remains rare. Salmonids already exhibit a wide portfolio of plastic life-history strategies, reflecting adaptation to highly heterogeneous environments, yet it remains unclear whether known major-effect loci involved in life-history regulation also contribute to variation in plastic responses to environmental change. One such major-effect locus is the transcription factor six6 , which has been repeatedly associated with variation in age at maturity across multiple populations of rainbow trout ( Oncorhynchus mykiss ). Since maturation timing is closely linked to growth trajectories and patterns of energetic allocation during early development, allelic variation at this locus may also influence growth responses to warming conditions. Here, we test this hypothesis using a common-garden experiment in which 6 months old juvenile rainbow trout were reared under current and warming (+2°C) temperature regimes. By quantifying genotype-specific reaction norms across environments, we show that six6 genotype contributes to environmentally dependent variation in growth and body composition, with individuals heterozygous for the six6 locus showing a distinct and steeper response to warming relative to homozygotes. These findings provide evidence that a major life-history gene shapes plastic responses to thermal stress in juvenile rainbow trout, with novel implications for how standing genetic variation at in large-effect loci may influence population-level responses to climate warming.

Intraspecific competition due to for example, density, has substantial influence on fitness dynamics and life histories, but the underlying physiological mechanisms are often complex and the molecular basis unclear. Further, designing laboratory experiments to measure physiological responses that reflect natural conditions is challenging. Here, we reared Atlantic salmon juveniles in semi-wild conditions in two densities to investigate the molecular mechanism of density-related changes in the hypothalamus, a key brain region regulating stress and energy homeostasis. We measured density-dependent changes in the expression of 12 genes involved in appetite and stress regulation and 16 genes involved in post-transcriptional regulation of gene expression via m6A RNA methylation. We also quantified genotype-environment interactions between density and two major life-history loci, vgll3 and six6. We found significant density-related differences in the expression of genes coding for corticotropin-releasing factors, appetite stimulators and inhibitors and m6A RNA methylation actors. Moreover, a paralogue of an appetite inhibitor showed a density-dependent pattern that was the opposite of what was expected. Six6 locus was also associated with changes in the expression of epitranscriptomic markers, including two writers and one eraser. Our results highlight that individuals' response to density in natural conditions is shaped by a complex interplay between stress, appetite and epitranscriptomic pathways in the hypothalamus. In addition, the functional divergence of paralogs indicates a potential role of genome duplication shaping such a response. We emphasise the value of integrating different physiological responses at the molecular level to better understand ecological processes affected by environmental change.

Background Pubertal timing is a key life history trait, shaped by ecological pressures to balance reproductive success and survival. Emerging evidence suggests a link between adiposity and early maturation, potentially through hormonal signaling pathways governing puberty timing. The timing of sexual maturation in Atlantic salmon has a strong genetic basis in addition to being linked with environmental shifts and lipid reserves. A gene encoding a co-factor of the Hippo pathway, vgll3 , is a major determinant of maturation timing in salmon. The Hippo pathway is known for its evolutionary conserved molecular signal role in both sexual maturation and adipogenesis. Results In this study, we tested the expression of Hippo pathway genes in the brain of immature and mature male Atlantic salmon carrying either the early or the late maturation genotype of vgll3. We found increased brain expression of a major Hippo pathway kinase ( lats1b ) in individuals with early maturation genotypes of vgll3 before maturation development of testes was evident. Moreover, we found components and regulating partners of the Hippo pathway showing differential expression in brain of individuals with early and late vgll3 genotypes prior to maturation. This may suggest a role for the Hippo pathway in central nervous system processes that regulate the preparation for maturation. Conclusions This study characterizes transcriptional changes in components of the Hippo pathway in the brain in relation to vgll3 -mediated early maturation in Atlantic salmon, highlighting the potential involvement of this pathway in the central regulation of maturation prior to gonadal development.

Many species are currently experiencing range shifts in response to changing environmental conditions with potentially serious genetic consequences. Repeated founder events and strong genetic drift are expected to erode genetic variation at the range front, reducing adaptive potential and slowing or even halting the expansion. However, the severity of these consequences for common and highly mobile species undergoing environment-driven range shifts (c.f. invasions) is less clear. Here, we combined historical observations and contemporary movement data of the common reed warbler (Acrocephalus scirpaceus) with genomic evidence from across its European breeding range to (1) infer the origin and (2) quantify the genetic consequences of a recent and rapid northward range expansion. Although there were no reductions in levels of nucleotide diversity or allelic richness, nor a signal of founder effect in the directionality index (ψ), our combined dataset approach was able to infer an expansion origin from the southwest. Furthermore, we found that private allelic richness retained a slight but significant linear decline along the colonisation route. These results suggest that high dispersal capabilities can allow even philopatric species to avoid the loss of genetic diversity during rapid range expansions. Nevertheless, if multiple lines of evidence enable identification of an expansion pathway, we may still detect genetic signals of expansion.

Understanding the molecular basis of plasticity and physiological tolerance to environmental changes is crucially important in the era of global change. Salmonids, a diverse family of fishes that includes salmon, trout, and charr, are emerging as powerful models for studying molecular responses to such changes. These species inhabit a wide range of aquatic environments, including freshwater and marine ecosystems, and are known for their remarkable adaptability to varying environmental conditions and for their variety of life history strategies. This review synthesizes current research on some of the major molecular mechanisms underlying transcriptional responses to important environmental changes. We discuss key studies that have applied state-of-the-art genomic tools in salmonids to uncover some of the gene expression changes underpinning plastic or acclimatory responses due to changes in temperature, salinity, oxygen levels or pH. By presenting examples of genes involved in these processes in salmonids, this review aims to provide insights into the broader implications of these findings, namely for conservation strategies and management. We also consider the potential of salmonids as emerging model species for monitoring the impacts of climate change on aquatic ecosystems, and their capacity to cope with rapid and inevitable environmental change. Finally, we outline future research directions to further elucidate the molecular pathways underlying plastic responses to environmental changes, with potential implications for evolutionary adaptation in these species.

Heterochrony, or shifts in developmental timing, drives phenotypic diversity within and between species and shapes life history traits that can be selected for in changing environments, which in turn promotes population resilience. Mutations in heterochronic genes that regulate these processes can induce stable timing shifts, impacting important life history traits such as pubertal timing. Age at maturity is a key adaptive trait across species, with vestigial-like family member 3 (vgll3), a Hippo pathway cofactor, as a main determinant in Atlantic salmon. Recent studies show that early (E) and late (L) vgll3 alleles affect reproductive gene expression in salmon, reinforcing its role in regulating developmental timing. This study examines whether vgll3 influences testicular heterochrony in Atlantic salmon by analyzing gene expression related to the Hippo pathway. We observed heterochronic divergence in Hippo pathway gene transcription, indicating accelerated changes linked to spermatogenesis in vgll3*EE individuals. Our results position vgll3 as a heterochronic gene with a key role in regulating developmental timing in salmon.

To improve our understanding and management of species’ response to environmental and anthropogenic changes, there is a critical need for integrative modeling approaches that encompass demographic, ecological and evolutionary processes in a unified framework. This is especially crucial for anadromous salmonid fishes that hold significant socio-economic value. Mechanistic models, particularly Demo-Genetic Agent-Based Models (DG-ABMs), are promising tools to address this challenge. Building on previous work, we present IBASAM, an Individual Based Anadromous SAlmonids Model. It incorporates significant advancements, including new processes such as dispersal and in-river movement, enhanced flexibility for simulating diverse spatial configurations- from river dendritic networks to metapopulations and multiple marine areas- and the integration of variation in life history phenology and the genetic architecture of traits. Additionally, a user-friendly interface has been developed to facilitate broader application. This improved versatility enables IBASAM application to a number of populations and species of anadromous salmonids, making it well-suited for a wide range of ecological and evolutionary studies. The model is particularly suited for investigating (meta)population eco-evolutionary dynamics, persistence, and adaptation to environmental changes, as well as exploring management options including fisheries regulation and river connectivity restoration. We summarize the model’s structure and illustrate some of its novelties, parameterization, and emerging patterns with the case study of a naturally reproducing Atlantic salmon population simulated over 100 years, with constant fishing rates and no climatic trend. Our simulations successfully reproduced 30 variables observed over 30 years in the Scorff population. IBASAM opens up new opportunities for research on the response of salmonid meta-populations to environmental changes, the exploration of management practices, with further developments possible.

Understanding pleiotropic architectures of phenotypes is instrumental for identifying the functional basis of adaptive genetic variation in the wild. Life-history variation may have a morphological basis that mediates resource acquisition allocation pathways, but identifying the underlying genetic basis of such traits is challenging. Using Atlantic salmon (Salmo salar) juveniles reared in common garden conditions, we test if 2 life-history associated loci, six6 and vgll3, are also associated with functional morphological traits. These loci had previously shown to exhibit strong signals of adaptation and are highly correlated with sea age at maturity. We show that genetic variation at the vgll3 locus is linked to variation in morphological traits that underlie swimming performance, along a tradeoff axis between efficient cruising and maneuvering, while the genetic variation at the six6 locus was linked to variation in body-head proportions suggesting the potential functional importance of these traits for resource acquisition efficiency. However, the direction of changes in morphological traits associated with late- vs early maturing alleles was not always consistent with the expected direction of an effect to maturation timing. Our results reveal a complex morphological landscape associated with the genetic variation in these loci, possibly as a result of pleiotropy or linkage across these genomic regions.

Sexual maturation in Atlantic salmon entails a transition in energy utilization, regulated by genes and environmental stimuli in sex-specific manner. Males require less energy, in the form of adiposity, to mature and typically mature younger than females. Maturation age is also influenced in a sex-dependent fashion by the vgll3 genotype (vestigial-like 3), a co-factor in the Hippo pathway. The underlying molecular processes of sex-dependent maturation age, and their interplay with adiposity and vgll3 genotypes, remain unclear. To elucidate the mechanisms underlying sex- and genotype-specific maturation differences, we investigated the association of early (E) and late (L) maturation vgll3 alleles with the transcription of > 330 genes involved in the regulation of the Hippo pathway and sexual maturation, and related molecular signals in brain, adipose, and gonads. The strongest effect of vgll3 genotype was observed in adipose for females and in brain for males, highlighting sex-specific expression differences in association with vgll3 genotype. Genes related to ovarian development showed increased expression in vgll3*EE compared to vgll3*LL females. Moreover, vgll3*EE females compared to vgll3*EE males exhibited reduced markers of pre-adipocyte differentiation and lipolysis yet enhanced expression of genes related to adipocyte maturation and lipid storage. Brain gene expression further showed sex-specific expression signals for genes related to hormones and lipids, as well as tight junction assembly. Overall, these sex-specific patterns point towards a greater lipid storage and slower energy utilization in females compared to males. These results suggest Hippo-dependent mechanisms may be important mediators of sex differences in maturation age in salmon.

A new single nucleotide polymorphism (SNP) panel for genetic stock identification in the Teno river Atlantic salmon, Salmo salar L., fishery was developed, with a view to improving on an existing microsatellite panel. Twenty-two genetically differentiated reporting units were proposed based on population genetic analyses of 1212 individuals collected at 37 locations in the river and genotyped for >33,000 genome-wide SNPs. A small subset of these SNPs was selected for genetic stock identification (GSI) using an iterative process that considered their diversity and differentiation across reporting units. A genotyping-by-sequencing assay was developed to simultaneously genotype 180 of these GSI SNPs plus a sexing marker. This new SNP panel showed comparative GSI power to the microsatellite panel, with anticipated improvements in terms of cost, speed and robustness, and transferability across laboratories and genotyping platforms. Mixed-stock analysis of the 2018 Teno river salmon catch using the new panel inferred that all 22 reporting units contributed to the fishery. Estimated catch proportions positively scaled with an independent estimate of reporting unit productivity: target spawning female biomass. This demonstrates the usefulness and efficiency of the 180 SNP panel for Atlantic salmon GSI in the Teno river system. If conducted on a regular basis, GSI can enable fine-tuning of management strategies to promote sustainable fishing.

Many species are currently experiencing range shifts in response to climate change. The colonisation of new regions can have serious genetic consequences for the shifting population, given that repeated founder events and strong genetic drift are expected to erode genetic variation along the expansion axis. Such a loss of genetic diversity could reduce adaptive potential, slowing or even halting the expansion. These genetic consequences are known to be particularly acute in species with low dispersal capabilities and therefore low levels of gene flow. Whether highly mobile species experience similar genetic bottlenecks as they undergo environment-driven range shifts is, however, less clear. Here we combined ecological and genomic evidence to (1) infer the origin and (2) quantify the genetic consequences of a recent and rapid northward range expansion of the common reed warbler (Acrocephalus scirpaceus), a philopatric long-distance migratory passerine capable of high dispersal. Together, historical observations, ringing data, and genomic RAD-seq data covering the species' European breeding range support an expansion origin from southwest. There were no reductions in levels of nucleotide diversity or allelic richness along the colonisation route, and no detectable allele frequency clines persisting from potential past founder effects. The genomic dataset confirmed the occurrence of low but significant levels of geographically continuous population structure across the European range. These results suggest that high dispersal capabilities can help even strongly philopatric species to escape the genetic costs of rapid range expansions. The lack of genetic patterns also highlights the value of combining multiple lines of evidence to reveal range shifts as genomic data alone was not sufficient to detect the occurrence of this large-scale range expansion. ### Competing Interest Statement The authors have declared no competing interest.

The Näätämö River, in the far north of Europe, hosts a large Atlantic salmon (Salmo salar) stock with high socio-economic value. The catchment has near-pristine environmental conditions, although there are recent signs of stock declines. It nevertheless offers a good opportunity to monitor the status of a near pristine wild salmon system. This study aimed to characterize the fine-scale genetic structure of Atlantic salmon in the Näätämö River and evaluated the possibility to assign individuals to their population of origin. We genotyped juveniles sampled from eight locations using a 60 K single nucleotide polymorphism (SNP) panel to characterize within-river genetic diversity and structure. We also tested the performance of a previously designed 180 SNP panel to assign individuals to their population of origin. The genetic structure of the Näätämö River salmon population appears weak (FST ranging from 0.001–0.035), possibly due to natural straying. The performance of the predesigned panel in assigning individuals to their population of origin was moderate to high (82–85

Heterochrony, or shifts in developmental timing, drives phenotypic diversity within and between species and shapes life history traits that can be selected for in changing environments which in turn promotes population resilience. Despite its importance, the molecular basis of heterochrony remains largely unknown. Mutations in heterochronic genes that regulate these processes can induce stable timing shifts, impacting important life history traits like pubertal timing. Heterochronic shifts in gene transcription are often tissue-specific and in mammals, for example, the testis shows the most pronounced heterochrony across species, especially during spermatogenesis. Age at maturity is a key adaptive trait across species, with vgll3, a Hippo pathway co-factor, as a main determinant in Atlantic salmon. The roles of vgll3 in maturation timing, adiposity, and energy storage are evolutionarily conserved across fish and mammals. Recent studies in salmon show vgll3 alleles; early (E) and late (L), affect reproductive gene expression, reinforcing its role in regulating developmental timing. This study examines whether vgll3 influences testicular heterochrony in Atlantic salmon by analyzing Hippo pathway-related gene expression in E and L genotypes. We observed heterochronic divergence in Hippo pathway gene transcription, indicating accelerated spermatogenesis-linked changes in the testes of vgll3*EE individuals. Since maturation in Atlantic salmon is closely tied to environmental changes, and the Hippo pathway acts as an environmental sensor, these findings suggest that Hippo-vgll3 shifts may also respond to environmental signals. This positions vgll3 as a heterochronic gene which is potentially affected by environmental changes (heterokairic), making it an ideal target for studying ecological adaptation linked to heterochrony. ### Competing Interest Statement The authors have declared no competing interest.

Seasonality can influence many physiological traits requiring optimal energetic capacity for life-history stage transitions. In Atlantic salmon, high-energy status is essential for the initiation of maturation. Earlier studies have linked a genomic region encoding vgll3 to maturation age, potentially mediated via body condition. Vgll3 has also been shown to act as an inhibitor of adipogenesis in mice. Here we investigate the influence of season and vgll3 genotypes associating with early (EE) and late (LL) maturation on lipid profiles in the muscle and liver of juvenile Atlantic salmon. We reared Atlantic salmon for two years from fertilization and sampled muscle and liver during the spring and autumn of the second year (at which time some males were sexually mature). We found no seasonal or genotype effect in the muscle lipid profiles of immature males or females. However, in the liver we detected a triacylglycerol enrichment and a genotype specific direction of change in membrane lipids, phosphatidylcholine and phosphatidylethanolamine, from spring to autumn. Specifically, from spring to autumn membrane lipid concentrations increased in vgll3*EE individuals but decreased in vgll3*LL individuals. This could be explained by 1) a seasonally more stable capacity of endoplasmic reticulum (ER) functions in vgll3*EE individuals compared to vgll3*LL individuals or 2) vgll3*LL individuals storing larger lipid droplets from spring to autumn in the liver compared to vgll3*EE individuals at the expense of ER capacity. This genotype specific seasonal direction of change in membrane lipid concentrations provides more indirect evidence of a potential mechanism linking vgll3 with lipid metabolism and storage.

Sexual maturation in many fishes requires a major physiological change that involves a rapid transition between energy storage and usage. In Atlantic salmon, this transition for the initiation of maturation is tightly controlled by seasonality and requires a high-energy status. Lipid metabolism is at the heart of this transition since lipids are the main energy storing molecules. The balance between lipogenesis (lipid accumulation) and lipolysis (lipid use) determines energy status transitions. A genomic region containing a transcription co-factor of the Hippo pathway, vgll3, is the main determinant of maturation timing in Atlantic salmon. Interestingly, vgll3 acts as an inhibitor of adipogenesis in mice and its genotypes are potentially associated with seasonal heterochrony in lipid storage and usage in juvenile Atlantic salmon. Here, we explored changes in expression of more than 300 genes directly involved in the processes of adipogenesis, lipogenesis and lipolysis, as well as the Hippo pathway in the adipose tissue of immature and mature Atlantic salmon with distinct vgll3 genotypes. We found molecular evidence consistent with a scenario in which immature males with different vgll3 genotypes exhibit contrasting seasonal dynamics in their lipid profiles. We also identified components of the Hippo signalling pathway as potential major drivers of vgll3 genotype-specific differences in adipose tissue gene expression. This study demonstrates the importance of adipose gene expression patterns for directly linking environmental changes with energy balance and age at maturity through genetic factors bridging lipid metabolism, seasonality and sexual maturation.

Genetic monitoring of populations currently attracts interest in the context of the Convention on Biological Diversity but needs long-term planning and investments. However, genetic diversity has been largely neglected in biodiversity monitoring, and when addressed, it is treated separately, detached from other conservation issues, such as habitat alteration due to climate change. We report an accounting of efforts to monitor population genetic diversity in Europe (genetic monitoring effort, GME), the evaluation of which can help guide future capacity building and collaboration towards areas most in need of expanded monitoring. Overlaying GME with areas where the ranges of selected species of conservation interest approach current and future climate niche limits helps identify whether GME coincides with anticipated climate change effects on biodiversity. Our analysis suggests that country area, financial resources and conservation policy influence GME, high values of which only partially match species' joint patterns of limits to suitable climatic conditions. Populations at trailing climatic niche margins probably hold genetic diversity that is important for adaptation to changing climate. Our results illuminate the need in Europe for expanded investment in genetic monitoring across climate gradients occupied by focal species, a need arguably greatest in southeastern European countries. This need could be met in part by expanding the European Union's Birds and Habitats Directives to fully address the conservation and monitoring of genetic diversity.

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.

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.

Age at maturity is an important factor contributing to life-history diversity. In Atlantic salmon, this trait often shows sex-specific variation, but female salmon are seldom included in experimental studies of maturation. As a result, there is a gap in our knowledge of how different genetic and environmental factors affect female maturation. Using a 4-year common-garden experiment, we assessed the influence of diet (low-fat vs. control) and vgll3 (a candidate gene in a genomic region known to influence age at maturity in Atlantic salmon) on maturation and related phenotypic traits of female Atlantic salmon from two 2nd-generation hatchery populations. We found the early-maturation-associated vgll3*E allele to be associated with higher probability of maturation. Heritability of maturation was estimated to be 0.295 with vgll3's contribution to phenotypic variance being ~2%. In addition, both body size and body condition measured in the spring prior to spawning influenced maturation. Body condition, in turn, was influenced by population and diet. The northern Oulu population and the low-fat diet were associated with lower body condition compared to the southern Neva population and the control diet. Moreover, there was an interaction between population and diet on body condition, suggesting that populations may respond differently to nutrient availability. These results broaden our understanding of the processes underlying maturation and demonstrate that genes and environment interact to shape age at maturity in female Atlantic salmon. ### Competing Interest Statement The authors have declared no competing interest.