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Adipose tissue is essential for energy homeostasis, with mitochondria having a central role in its function. Mitochondria-mediated white adipose tissue dysfunction has been linked to several metabolic disorders in humans but surprisingly little is known about natural variation in mitochondrial function in wild animal populations, and its evolutionary significance. Early sexual maturation (low age-at-maturity) in Atlantic salmon (Salmo salar) is promoted by higher adiposity and has a strong genetic association with thevgll3locus. This makes Atlantic salmon a convenient wild model to study the potential role of mitochondria-mediated adipose tissue processes in relation to the timing of maturation. Yet, mitochondrial respiration has not been measured in the adipose tissue in fish, and the lack of data is restricting the development of informed hypotheses. Here, using 13 Atlantic salmon individuals reared in common-garden conditions, we first verified the feasibility of measuring mitochondrial respiration in the adipose tissue. As expected, the respiration level was generally low, but nonetheless we successfully quantified its biological variation in the adipose tissue. Next, we analysed the potential association of mitochondrial respiration with mitochondrial DNA (mtDNA) content, adipocyte size, sex, and thevgll3genotype. Despite low samples sizes, mitochondrial respiration, leak respiration, and coupling capacity (P/E ratio) were marginally significantly decreased in immature females carrying with thevgll3early maturation compared to the alternative genotype. Based on these results, we suggested two new hypotheses on how the coupling capacity of oxidative phosphorylation could be linked with the timing of maturation via adiposity and pave the way to study the mechanistic relationships between life-history variation and mitochondrial bioenergetics in wild populations.

There is a general paucity of knowledge regards spatial variation in marine resource use for many taxa, even those of high socio-economic importance such as Atlantic salmon. While it is known that the oceans around the Faroe Islands support a salmon feeding ground, the relative use of this feeding ground by different age classes across different stocks remains largely unexplored. Using a combination of genetic stock assignment and run-reconstruction models, we observed a consistent pattern whereby the proportion of multi-sea winter (MSW) salmon for a given reporting group was substantially greater around the Faroes than the MSW proportion for that reporting groups among the prefisheries abundance. Surprisingly, MSW fish from Ireland and UK were as likely to occur around the Faroes as were MSW fish from more north-eastern regions such as the Teno river and the Barents and White Seas. MSW fish from Southern Norway were the most likely to be caught at the Faroes. While 1SW salmon from Ireland and UK as well as from Southern Norway occurred at similar rates around the Faroes, 1SW fish from more north-eastern reporting groups were nearly entirely absent from the same feeding ground. In combination with previous studies that examine the marine distribution of Atlantic salmon, our results strongly indicate that the oceans around the Faroes play host to a predominantly MSW salmon feeding ground and that use of this resource varies both within the age classes of a given stock as well as between different stocks. Furthermore, these results suggest that MSW fish from certain stocks might preferentially undertake migrations to the Faroes. Variation in spatial resource use may help to buffer salmon stocks against localised negative changes in marine conditions.

Understanding the drivers of evolution is a fundamental aim in biology. However, identifying the evolutionary impacts of human activities is challenging because of a lack of temporal data and limited knowledge of the genetic basis of most traits. Here, we identify the drivers of evolution toward maturity at an earlier age in Atlantic salmon through two types of fisheries-induced evolution acting in opposing directions: an indirect effect linked with harvest of a salmon prey species (capelin) at sea (selection against late maturation) and a direct effect due to net fishing in rivers (selection against early maturation). Because capelin are harvested as an aquaculture feed protein source, we hereby determine an indirect path by which salmon aquaculture may influence wild salmon populations.

Efforts to understand the genetic underpinnings of phenotypic variation are becoming more and more frequent in molecular ecology. Such efforts often lead to the identification of candidate regions showing signals of association and/or selection. These regions may contain multiple genes and therefore validation of which genes are actually responsible for the signal is required. In Atlantic salmon (Salmo salar), a large-effect locus for maturation timing, an ecologically important trait, occurs in a genomic region including two genes, vgll3 and akap11, but data for clearly determining which of the genes (or both) contribute to the association have been lacking. Here, we take advantage of natural recombination events detected between the two candidate genes in a salmon broodstock to reduce linkage disequilibrium at the locus, thus enabling delineation of the influence of variation at these two genes on early maturation. By rearing 5,895 males to maturation age, of which 81% had recombinant vgll3/akap11 allelic combinations, we found that vgll3 single nucleotide polymorphism (SNP) variation was strongly associated with early maturation, whereas there was little or no association between akap11 SNP variation and early maturation. These findings provide strong evidence supporting vgll3 as the primary candidate gene in the chromosome 25 locus for influencing early maturation. This will help guide future research for understanding the genetic processes controlling early maturation. This also exemplifies the utility of natural recombinants to more precisely map causal variation underlying ecologically important phenotypic diversity.

A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of the relationship and its dependence on ecological conditions have rarely been demonstrated. The strong genetic determination of age-at-maturity by two unlinked genomic regions ( vgll3 and six6 ) makes Atlantic salmon ( Salmo salar ) an ideal model to address these questions. Using more than 250 juveniles in common garden conditions, we quantified the covariation between metabolic phenotypes—standard and maximum metabolic rates (SMR and MMR), and aerobic scope (AS)—and the life-history genomic regions, and tested if food availability modulates the relationships. We found that the early maturation genotype in vgll3 was associated with higher MMR and consequently AS. Additionally, MMR exhibited physiological epistasis; it was decreased when late maturation genotypes co-occurred in both genomic regions. Contrary to our expectation, the life-history genotypes had no effects on SMR. Furthermore, food availability had no effect on the genetic covariation, suggesting a lack of genotype-by-environment interactions. Our results provide insights on the key organismal processes that link energy use at the juvenile stage to age-at-maturity, indicating potential mechanisms by which metabolism and life-history can coevolve.

Sexual maturation timing is a life-history trait central to the balance between mortality and reproduction. Maturation may be triggered when an underlying compound trait, called liability, exceeds a threshold. In many different species and especially fishes, this liability is approximated by growth and body condition. However, environmental vs. genetic contributions either directly or via growth and body condition to maturation timing remain unclear. Uncertainty exists also because the maturation process can reverse this causality and itself affect growth and body condition. In addition, disentangling the contributions of polygenic and major loci can be important. In many fishes, males mature before females, enabling the study of associations between male maturation and maturation-unbiased female liability traits. Using 40 Atlantic salmon families, longitudinal common-garden experimentation, and quantitative genetic analyses, we disentangled environmental from polygenic and major locus (vgll3) effects on male maturation, and sex-specific growth and condition. We detected polygenic heritabilities for maturation, growth, and body condition, and vgll3 effects on maturation and body condition but not on growth. Longitudinal patterns for sex-specific phenotypic liability, and for genetic variances and correlations between sexes suggested that early growth and condition indeed positively affected maturation initiation. However, towards spawning time, causality appeared reversed for males whereby maturation affected growth negatively and condition positively via both the environmental and genetic effects. Altogether, the results indicate that growth and condition are useful traits to study liability for maturation initiation, but only until maturation alters their expression, and that vgll3 contributes to maturation initiation via condition.

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.

Efforts to understand the genetic underpinnings of phenotypic variation are becoming more and more frequent in molecular ecology. Such efforts often lead to the identification of candidate regions showing signals of association and/or selection. These regions may contain multiple genes and therefore validation of which genes are actually responsible for the signal is required. In Atlantic salmon (Salmo salar), a large-effect locus for maturation timing, an ecologically important trait, occurs in a genomic region including two genes, vgll3 and akap11, but data for clearly determining which of the genes (or both) contribute to the association have been lacking. Here, we take advantage of natural recombination events detected between the two candidate genes in a salmon broodstock to reduce linkage disequilibrium at the locus, and thus enabling delineation of the influence of variation at these two genes on maturation timing. By rearing 5895 males to maturation age, of which 81% had recombinant vgll3/akap11 allelic combinations, we found that vgll3 SNP variation was strongly associated with maturation timing, whereas there was little or no association between akap11 SNP variation and maturation timing. These findings provide strong evidence supporting vgll3 as the primary candidate gene in the chromosome 25 locus for influencing maturation timing. This will help guide future research for understanding the genetic processes controlling maturation timing. This also exemplifies the utility of natural recombinants to more precisely map causal variation underlying ecologically important phenotypic diversity.

Understanding the drivers of evolution is a fundamental aim in biology. However, identifying the evolutionary impacts of human activities, both direct and indirect, is challenging because of lack of temporal data and limited knowledge of the genetic basis of most traits1. Atlantic salmon is a species exposed to intense anthropogenic pressures during its anadromous life cycle2. Previous research has shown that salmon age at maturity has evolved towards earlier maturation over the last 40 years, with an 18% decrease3 in the allele associated with late maturation at the large-effect vgll3 locus4; but the drivers of this change remain unknown. Here, we link genetic and phenotypic changes in a large Atlantic salmon population with salmon prey species biomass in the Barents Sea, temperature, and fishing effort in order to identify drivers of age at maturity evolution. We show that age at maturity evolution is associated with two different types of fisheries induced evolution acting in opposing directions: an indirect effect linked with commercial harvest of a salmon prey species (capelin) at sea (selection against late maturation), and a direct effect due to temporal changes in net fishing pressure in the river (surprisingly, selection against early maturation). Although the potential for direct and indirect evolutionary effects of fishing have been acknowledged, empirical evidence for induced changes at the genetic level has been lacking5. As capelin are primarily harvested to produce fish meal and oil for aquaculture6, we hereby identify an indirect path by which Atlantic salmon aquaculture may negatively affect wild populations.

Over the past decades, Atlantic salmon (Salmo salar, Salmonidae) has emerged as a model system for sexual maturation research, owing to the high diversity of life history strategies, knowledge of trait genetic architecture, and their high economic value. The aim of this synthesis is to summarize the current state of knowledge concerning maturation in Atlantic salmon, outline knowledge gaps, and provide a roadmap for future work. We summarize the current state of knowledge: 1) maturation in Atlantic salmon takes place over the entire life cycle, starting as early as embryo development, 2) variation in the timing of maturation promotes diversity in life history strategies, 3) ecological and genetic factors influence maturation, 4) maturation processes are sex-specific and may have fitness consequences for each sex, 5) genomic studies have identified large-effect loci that influence maturation, 6) the brain-pituitary–gonadal axis regulates molecular and physiological processes of maturation, 7) maturation is a key component of fisheries, aquaculture, conservation, and management, and 8) climate change, fishing pressure, and other anthropogenic stressors likely have major effects on salmon maturation. In the future, maturation research should focus on a broader diversity of life history stages, including early embryonic development, the marine phase and return migration. We recommend studies combining ecological and genetic approaches will help disentangle the relative contributions of effects in different life history stages to maturation. Functional validation of large-effect loci should reveal how these genes influence maturation. Finally, continued research in maturation will improve our predictions concerning how salmon may adapt to fisheries, climate change, and other future challenges. Keywords Brain-pituitary–gonadal axis Genomewide association mapping Life history stage Life history traits Puberty Reproduction

Understanding the genetic basis of repeated evolution of the same phenotype across taxa is a fundamental aim in evolutionary biology and has applications in conservation and management. However, the extent to which interspecific life-history trait polymorphisms share evolutionary pathways remains underexplored. Here, we address this gap by studying the genetic basis of a key life-history trait, age at maturity, in four species of Pacific salmonids (genus Oncorhynchus) that exhibit intra- and interspecific variation in this trait-Chinook Salmon, Coho Salmon, Sockeye Salmon, and Steelhead Trout. We tested for associations in all four species between age at maturity and two genome regions, six6 and vgll3, that are strongly associated with the same trait in Atlantic Salmon (Salmo salar). We also conducted a genome-wide association analysis in Steelhead to assess whether additional regions were associated with this trait. We found the genetic basis of age at maturity to be heterogeneous across salmonid species. Significant associations between six6 and age at maturity were observed in two of the four species, Sockeye and Steelhead, with the association in Steelhead being particularly strong in both sexes (p = 4.46 x 10(-9) after adjusting for genomic inflation). However, no significant associations were detected between age at maturity and the vgll3 genome region in any of the species, despite its strong association with the same trait in Atlantic Salmon. We discuss possible explanations for the heterogeneous nature of the genetic architecture of this key life-history trait, as well as the implications of our findings for conservation and management.

This is the peer reviewed version of the following article: Aykanat, T., Rasmussen, M., Ozerov, M., Niemelä, E., Paulin, L., Vähä, J.-P., ...Primmer, C. R. (2020). Life‐history genomic regions explain differences in Atlantic salmon marine diet specialization. Journal of Animal Ecology, ?(?), 1-15., which has been published in final form at https://doi.org/10.1111/1365-2656.13324. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. 1. Animals employ various foraging strategies along their ontogeny to acquire energy, and with varying degree of efficiencies, to support growth, maturation and subsequent reproduction events. Individuals that can efficiently acquire energy early are more likely to mature at an earlier age, as a result of faster energy gain which can fuel maturation and reproduction. 2. We aimed to test the hypothesis that heritable resource acquisition variation that covaries with efficiency along the ontogeny would influence maturation timing of individuals. 3. To test this hypothesis, we utilized Atlantic salmon as a model which exhibits a simple, hence trackable, genetic control of maturation age. We then monitored the variation in diet acquisition (quantified as stomach fullness and composition) of individuals with different ages, and linked it with genomic regions (haploblocks) that were previously identified to be associated with age‐at‐maturity. 4. Consistent with the hypothesis, we demonstrated that one of the life‐history genomic regions tested (six6) was indeed associated with age‐dependent differences in stomach fullness. Prey composition was marginally linked to six6, and suggestively (but non‐significantly) to vgll3 genomic regions. We further showed Atlantic salmon switched to the so‐called ‘feast and famine’ strategy along the ontogeny, where older age groups exhibited heavier stomach content, but that came at the expense of running on empty more often. 5. These results suggest genetic variation underlying resource utilization may explain the genetic basis of age structure in Atlantic salmon. Given that ontogenetic diet has a genetic component and the strong spatial diversity associated with these genomic regions, we predict populations with diverse maturation age will have diverse evolutionary responses to future changes in marine food web structures.

The release of captive-bred animals into the wild is commonly practised to restore or supplement wild populations but comes with a suite of ecological and genetic consequences. Vast numbers of hatchery-reared fish are released annually, ostensibly to restore/enhance wild populations or provide greater angling returns. While previous studies have shown that captive-bred fish perform poorly in the wild relative to wild-bred conspecifics, few have measured individual lifetime reproductive success (LRS) and how this affects population productivity. Here, we analyse data on Atlantic salmon from an intensely studied catchment into which varying numbers of captive-bred fish have escaped/been released and potentially bred over several decades. Using a molecular pedigree, we demonstrate that, on average, the LRS of captive-bred individuals was only 36% that of wild-bred individuals. A significant LRS difference remained after excluding individuals that left no surviving offspring, some of which might have simply failed to spawn, consistent with transgenerational effects on offspring survival. The annual productivity of the mixed population (wild-bred plus captive-bred) was lower in years where captive-bred fish comprised a greater fraction of potential spawners. These results bolster previous empirical and theoretical findings that intentional stocking, or non-intentional escapees, threaten, rather than enhance, recipient natural populations.

Understanding the genetic basis of repeated evolution of the same phenotype across taxa is a fundamental aim in evolutionary biology and has applications to conservation and management. However, the extent to which interspecific life-history trait polymorphisms share evolutionary pathways remains under-explored. We address this gap by studying the genetic basis of a key life-history trait, age at maturity, in four species of Pacific salmon (genus Oncorhynchus) that exhibit intra- and interspecific variation in this trait – Chinook Salmon, Coho Salmon, Sockeye Salmon, and Steelhead Trout. We tested for associations in all four species between age at maturity and two genome regions, six6 and vgll3, that are strongly associated with the same trait in Atlantic Salmon (Salmo salar). We also conducted a genome-wide association analysis in Steelhead to assess whether additional regions were associated with this trait. We found the genetic basis of age at maturity to be heterogeneous across salmonid species. Significant associations between six6 and age at maturity were observed in two of the four species, Sockeye and Steelhead, with the association in Steelhead being particularly strong in both sexes (p = 4.46×10−9 after adjusting for genomic inflation). However, no significant associations were detected between age at maturity and the vgll3 genome region in any of the species, despite its strong association with the same trait in Atlantic Salmon. We discuss possible explanations for the heterogeneous nature of the genetic architecture of this key life-history trait, as well as the implications of our findings for conservation and management.

A major goal in biology is to understand how evolution shapes variation in individual life histories. Genome-wide association studies have been successful in uncovering genome regions linked with traits underlying life history variation in a range of species. However, lack of functional studies of the discovered genotype-phenotype associations severely restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here, we report a cis-regulatory mechanism whereby expression of alternative isoforms of the transcription co-factor vestigial-like 3 (vgll3) associate with variation in a key life history trait, age at maturity, in Atlantic salmon (Salmo salar). Using a common-garden experiment, we first show that vgll3 genotype associates with puberty timing in one-year-old salmon males. By way of temporal sampling of vgll3 expression in ten tissues across the first year of salmon development, we identify a pubertal transition in vgll3 expression where maturation coincided with a 66% reduction in testicular vgll3 expression. The late maturation allele was not only associated with a tendency to delay puberty, but also with expression of a rare transcript isoform of vgll3 pre-puberty. By comparing absolute vgll3 mRNA copies in heterozygotes we show that the expression difference between the early and late maturity alleles is largely cis-regulatory. We propose a model whereby expression of a rare isoform from the late allele shifts the liability of its carriers towards delaying puberty. These results exemplify the potential importance of regulatory differences as a mechanism for the evolution of life history traits., Author summary Alternative life history strategies are an important source of diversity within populations and promote the maintenance of adaptive capacity and population resilience. However, in many cases the molecular basis of different life history strategies remains elusive. Age at maturity is a key adaptive life history trait in Atlantic salmon and has a relatively simple genetic basis. Using salmon age at maturity as a model, we report a mechanism whereby different transcript isoforms of the key age at maturity gene, vestigial-like 3 (vgll3), associate with variation in the timing of male puberty. Our results show how gene regulatory differences in conjunction with variation in gene transcript structure can encode for complex alternative life histories.

Sexual maturation is a pivotal life-history trait that balances the probabilities between mortality and reproduction. Environmental vs. genetic contributions to maturation component traits, such as somatic growth and body condition, remain uncertain because of difficulties in determining causality. In Atlantic salmon, maturation timing associates with a large-effect locus around vgll3, which also links with growth, condition, and maturation in mammals. We investigate environmental vs. genetic contributions to maturation and its component traits by combining controlled breeding with common-garden experimentation in two temperatures. We test whether vgll3 associates with first-year maturation of male salmon and, to avoid reverse causality, whether vgll3 effects express via growth or condition in the males’ non-maturing female relatives. Across 41 families, 4% of males matured in the cold vs. 39% in the warm environment. Maturation rate differed 3.3- to 4.6-fold between vgll3 genotypes, which also explained around 30% of maturation heritability. Female condition differed up to 2% between vgll3 genotypes, which also explained 6-17% of condition heritability. Non-significant vgll3 effects on female length were antagonistic to those for condition but of equal proportional size. When accounting for vgll3 effects, positive genetic correlations between male maturation and female growth increased, whereas those between male maturation and condition decreased, supporting an antagonistic effect of vgll3 on growth and condition. The results indicate that large vgll3 effects on maturation are mediated via large condition effects and suggest vgll3 as a candidate locus for controlling the resource allocation trade-off between somatic growth and body condition. Significance Statement Identifying traits that affect sexual maturation timing and quantifying their relative environmental and genetic importance is a major goal in evolutionary research because of their strong links to fitness. However, cause and effect between maturation timing and such traits often remain unknown. We conducted a common-garden quantitative genetic study using Atlantic salmon to test for genetic contributions of body length and body condition expressed in immature females on maturation of their male relatives. We show that the detection of genetic associations between maturation and length or condition depends on both genetic and environmental factors and suggest that the genetic association with condition chiefly underlies a candidate gene with large effect on maturation that is mediated via variation in body condition.

Despite recent taxonomic diversification in studies linking genotype with phenotype, follow-up studies aimed at understanding the molecular processes of such genotype-phenotype associations remain rare. The age at which an individual reaches sexual maturity is an important fitness trait in many wild species. However, the molecular mechanisms regulating maturation timing processes remain obscure. A recent genome-wide association study in Atlantic salmon (Salmo salar) identified large-effect age-at-maturity-associated chromosomal regions including genesvgll3,akap11andsix6, which have roles in adipogenesis, spermatogenesis and the hypothalamic-pituitary-gonadal (HPG) axis, respectively. Here, we determine expression patterns of these genes during salmon development and their potential molecular partners and pathways. Using Nanostring transcription profiling technology, we show development- and tissue-specific mRNA expression patterns forvgll3,akap11andsix6. Correlated expression levels ofvgll3andakap11, which have adjacent chromosomal location, suggests they may have shared regulation. Further,vgll3correlating witharhgap6andyap1, andakap11withlats1andyap1suggests that Vgll3 and Akap11 take part in actin cytoskeleton regulation. Tissue-specific expression results indicate thatvgll3andakap11paralogs have sex-dependent expression patterns in gonads. Moreover,six6correlating withslc38a6andrtn1, and Hippo signaling genes suggests that Six6 could have a broader role in the HPG neuroendrocrine and cell fate commitment regulation, respectively. We conclude that Vgll3, Akap11 and Six6 may influence Atlantic salmon maturation timing via affecting on adipogenesis and gametogenesis by regulating cell fate commitment and the HPG axis. These results may help to unravel general molecular mechanisms behind maturation.

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.

Salmon spawning in their local habitat have a clear reproductive advantage over dispersers from nearby populations., 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.

A genotyping assay for the Ion Torrent Ion PGM platform was developed for fast and cost-effective targeted genotyping of key single nucleotide polymorphisms (SNPs) earlier identified using a genome-wide SNP array in Atlantic salmon Salmo salar. The method comprised a simple primer design step for multiplex-polymerase chain reaction (PCR), followed by two rounds of Ion Torrent Ion PGM sequencing to empirically evaluate marker efficiency in large multiplexes and to optimise or exclude them when necessary. Of 282 primer pairs initially tested, 217 were successfully amplified, indicating good amplification success (>75%). These markers included the sdy partial gene product to determine genetic sex, as well as three additional modules comprising SNPs for assessing neutral genetic variation (NSNP = 150), examining functional genetic variation associated with sea age at maturity (NSNP = 5), and for performing genetic subpopulation assignment (NSNP = 61). The assay was primarily developed to monitor long-term genetic changes in S. salar from the Teno River, but modules are likely suitable for application in a wide range of S. salar populations. Furthermore, the fast and versatile assay development pipeline offers a strategy for developing targeted sequencing assays in any species.

Genetic correlations 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 thevgll3gene, and we used this opportunity demonstrate that the two traits are genetically correlated 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-maturingvgll3genotype (EE) compared to fish with the late-maturing genotype(LL). The association had a dominance architecture, although the dominant allele was reversed in the late-maturing group compared to younger groups that stayed only one year at sea before maturation.Post hocanalysis indicated that iteroparous fish with theEEgenotype had accelerated growth prior to first reproduction compared to first-time spawners, across all age groups, while this effect was not detected in fish with theLLgenotype. These results broaden the functional link around thevgll3genome 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.

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 dispersal disadvantage in reproductive success may act in natural populations to drive population divergence and local adaptation over microgeographic spatial scales without clear morphological differences or physical barriers to gene flow.

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.

Divergent selection at ecologically important traits is thought to be a major factor driving phenotypic differentiation between populations. To elucidate the role of different evolutionary processes shaping the variation in gill raker number of European whitefish (Coregonus lavaretus sensu lato) in the Baltic Sea basin, we assessed the relationships between genetic and phenotypic variation among and within three whitefish ecotypes (sea spawners, river spawners and lake spawners). To generate expected neutral distribution of FST and to evaluate whether highly variable microsatellite loci resulted in deflated FST estimates compared to less variable markers, we performed population genetic simulations under finite island and hierarchical island models. The genetic divergence observed among (FCT = 0.010) and within (FST = 0.014– 0.041) ecotypes was rather low. The divergence in gill raker number, however, was substantially higher between sea and river spawners compared to observed microsatellite data and simulated neutral baseline (PCT > FCT). This suggests that the differences in gill raker number between sea and river spawners are likely driven by divergent natural selection. We also found strong support for divergent selection on gill raker number among different populations of sea spawners (PST > FST), most likely caused by highly variable habitat use and diverse diet. The putative role of divergent selection within lake spawners initially inferred from empirical microsatellite data was not supported by simulated FST distributions. This work provides a first formal test of divergent selection on gill raker number in Baltic whitefish, and demonstrates the usefulness of population genetic simulations to generate informative neutral baselines for PST–FST analyses helping to disentangle the effects of stochastic evolutionary processes from natural selection.

An approach frequently used to demonstrate a genetic basis for population-level phenotypic differences is to employ common garden rearing designs, where observed differences are assumed to be attributable to primarily additive genetic effects. Here, in two common garden experiments, we employed factorial breeding designs between wild and domestic, and among wild populations of Chinook salmon (Oncorhynchus tshawytscha). We measured the contribution of additive (V(A)) and maternal (V(M)) effects to the observed population differences for 17 life history and fitness-related traits. Our results show that, in general, maternal effects contribute more to phenotypic differences among populations than additive genetic effects. These results suggest that maternal effects are important in population phenotypic differentiation and also signify that the inclusion of the maternal source of variation is critical when employing models to test population differences in salmon, such as in local adaptation studies.

Populations experiencing sudden environmental change must be capable of rapidly evolving to survive. Here we explore changes in gene transcription as a mechanism for rapid adaptation at four osmoregulatory genes (CFTR I, NaK ATPase1 alpha a, NaK ATPase1 alpha b and GHRII) in anadromous steelhead trout versus a derived land-locked population after 14 generations. Transcription was measured before and after a 24-h saltwater challenge in pure and reciprocal hybrid offspring of fish from both populations reared in a common environment for two generations. Significant differences between the landlocked and migratory populations were observed, particularly in fresh water at the NaK ATPase1 alpha a and GHRII genes, indicating rapid evolutionary change, possibly associated with reduced energy expenditure in the landlocked lake system. Phenotypic divergence analysis (Q (ST)) shows that the observed transcriptional differences deviate from neutral expectations. Some reciprocal crosses exhibited anomalous transcription consistent with sex-linked epistatic or genetic imprinting effects. Our results highlight unpredictable phenotypic outcomes of hybridization among locally adapted populations and the need to exercise caution when interbreeding populations for conservation purposes.

Temporal instability in population genetic structure has significant implications for management and conservation decisions. Here, we evaluate temporal stability in five populations of Chinook salmon ( Oncorhynchus tshawytscha ) from the Upper Fraser River, British Columbia, Canada, based on estimates of temporal allelic variance and effective population size (Ne) at 11 microsatellite loci. Significant temporal variation in allele frequencies was found within individual populations sampled at 5- to 12-year intervals. Removal of migrant fish or correcting for migrants resulted in higher allelic variance or reduced Ne. Populations with higher levels of temporally consistent gene flow show reduced temporal allelic variance (i.e., reduced genetic drift) and higher Ne. This study is an important empirical example of the effect of gene flow on genetic stability and Ne. In salmonids, low straying levels may have evolved to favor local adaptation; however, we show that even such low levels of gene flow can elevate effective population sizes and preserve genetic variability. This study highlights the importance of considering gene flow acting to temporally stabilize populations, particularly small ones, and should migration be interrupted, Nelevels may decline with no obvious change in census population sizes.

Summary A 991 bp DNA fragment, consisting of a 225 amino acid reading frame homologous to outer membrane protein coding ompA gene, was cloned from a purple sulfur bacterium Allochromatium vinosum. The homology analysis revealed up to 51% similarity to other bacterial species. The absence of branching within diazotrophs or other taxonomically related groups shows the structural importance of the protein regardless of the metabolism and evolution of the species.

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 genetic loci behind 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 57 salmon populations, 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 reducing intralocus sexual conflict and maintaining adaptive variation in wild populations. Using high density SNP data and whole genome re-sequencing, we found that vestigial-like family member 3 (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 39.4% of phenotypic variation, an unexpectedly high effect size 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 permitting greater optimisation 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 further 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

Declining trends in the abundance of many fish urgently call for more efficient and informative monitoring methods that would provide necessary demographic data for the evaluation of existing conservation, restoration, and management actions. We investigated how genetic sibship reconstruction from young-of-the-year brown trout (Salmo trutta L.) juveniles provides valuable, complementary demographic information that allowed us to disentangle the effects of habitat quality and number of breeders on juvenile density. We studied restored (n = 15) and control (n = 15) spawning and nursery habitats in 16 brown trout rivers and streams over 2 consecutive years to evaluate the effectiveness of habitat restoration activities. Similar juvenile densities both in restored and control spawning and nursery grounds were observed. Similarly, no differences in the effective number of breeders, Nb(SA), were detected between habitats, indicating that brown trout readily used recently restored spawning grounds. Only a weak relationship between the Nb(SA) and juvenile density was observed, suggesting that multiple factors affect juvenile abundance. In some areas, very low estimates of Nb(SA) were found at sites with high juvenile density, indicating that a small number of breeders can produce a high number of progeny in favorable conditions. In other sites, high Nb(SA) estimates were associated with low juvenile density, suggesting low habitat quality or lack of suitable spawning substrate in relation to available breeders. Based on these results, we recommend the incorporation of genetic sibship reconstruction to ongoing and future fish evaluation and monitoring programs to gain novel insights into local demographic and evolutionary processes relevant for fisheries management, habitat restoration, and conservation. El Uso de la Reconstruccion de Relaciones Fraternales para Complementar el Monitoreo Tradicional en el Manejo de Pesquerias y en la Conservacion de la Trucha Cafe Resumen Las tendencias de declinacion en la abundancia de muchos peces son un llamado urgente para metodos de monitoreo mas eficientes e informativos que proporcionarian los datos demograficos necesarios para la evaluacion de la conservacion actual, la restauracion y las acciones de manejo. Investigamos como la reconstruccion genetica del numero de crias producidas por una pareja de padres de juveniles de ese mismo ano de trucha cafe (Salmo trutta L.) proporciona informacion demografica valiosa y complementaria, la cual nos permitio revelar los efectos de la calidad de habitat y el numero de reproductores sobre la densidad juvenil. Estudiamos habitats de reproduccion y crianza restaurados (n = 15) y controlados (n = 15) en 16 rios y arroyos de trucha cafe a lo largo de dos anos consecutivos para evaluar la efectividad de las actividades de restauracion de habitat. Se observaron densidades juveniles similares en ambos tipos de habitat. De manera similar, no se detectaron diferencias entre los habitats en el numero efectivo de reproductores (Nb(SA)), lo que indica que la trucha cafe uso de manera inmediata y reciente los habitats de reproduccion restaurados. Solo se observo una relacion debil entre el Nb(SA) y la densidad juvenil, lo que sugiere que multiples factores afectan a la abundancia juvenil. En algunas areas, se encontraron estimados muy bajos de Nb(SA) en sitios con una alta densidad juvenil, lo que indica que un pequeno numero de reproductores puede producir un alto numero de descendencia en condiciones favorables. En otros sitios, los estimados altos de Nb(SA) estuvieron asociados con una baja densidad juvenil, lo que sugiere que una baja calidad de habitat o la falta de un sustrato adecuado para la reproduccion en relacion con los reproductores disponibles. Con base en estos resultados, recomendamos la incorporacion de esta reconstruccion genetica a la evaluacion actual y futura de peces y a los programas de monitoreo para obtener percepciones novedosas de los procesos demograficos y evolutivos relevantes para el manejo de pesqueras, restauracion de habitat y conservacion.

Understanding the factors that shape the evolution of gene expression is a central goal in biology, but the molecular mechanisms behind this remain controversial. A related major goal is ascertaining how such factors may affect the adaptive potential of a species or population. Here we demonstrate that temperature-driven gene expression changes in fish adapted to differing thermal environments are constrained by the level of gene pleiotropy estimated by either the number of protein interactions or gene biological processes. Genes with low pleiotropy levels were the main drivers of both plastic and evolutionary global expression profile changes, while highly pleiotropic genes had limited expression response to temperature treatment. Our study provides critical insights into the molecular mechanisms by which natural populations can adapt to changing environments. In addition to having important implications for climate change adaptation, these results suggest that gene pleiotropy should be considered more carefully when interpreting expression profiling data., The factors that shape the evolution of gene expression and their role in adaptation are poorly understood. Here, Papakostas et al. show that gene pleiotropy constrains protein expression evolution in freshwater salmonids adapted to different temperatures.

Background: Pedigree reconstruction using genetic analysis provides a useful means to estimate fundamental population biology parameters relating to population demography, trait heritability and individual fitness when combined with other sources of data. However, there remain limitations to pedigree reconstruction in wild populations, particularly in systems where parent-offspring relationships cannot be directly observed, there is incomplete sampling of individuals, or molecular parentage inference relies on low quality DNA from archived material. While much can still be inferred from incomplete or sparse pedigrees, it is crucial to evaluate the quality and power of available genetic information a priori to testing specific biological hypotheses. Here, we used microsatellite markers to reconstruct a multi-generation pedigree of wild Atlantic salmon (Salmo salar L.) using archived scale samples collected with a total trapping system within a river over a 10 year period. Using a simulation-based approach, we determined the optimal microsatellite marker number for accurate parentage assignment, and evaluated the power of the resulting partial pedigree to investigate important evolutionary and quantitative genetic characteristics of salmon in the system.Results: We show that at least 20 microsatellites (ave. 12 alleles/locus) are required to maximise parentage assignment and to improve the power to estimate reproductive success and heritability in this study system. We also show that 1.5 fold differences can be detected between groups simulated to have differing reproductive success, and that it is possible to detect moderate heritability values for continuous traits (h(2) similar to 0.40) with more than 80% power when using 28 moderately to highly polymorphic markers.Conclusion: The methodologies and work flow described provide a robust approach for evaluating archived samples for pedigree-based research, even where only a proportion of the total population is sampled. The results demonstrate the feasibility of pedigree-based studies to address challenging ecological and evolutionary questions in free-living populations, where genealogies can be traced only using molecular tools, and that significant increases in pedigree assignment power can be achieved by using higher numbers of markers.

Estimation of quantitative genetic parameters is important for improving salmonid broodstock management in commercial and government hatcheries. Using a replicated 2 x 2 factorial breeding design (48 families and 192 individuals), we partitioned early immune response transcription variation into additive genetic, non-additive genetic, and maternal components in juvenile Chinook salmon (Oncorhynchus tshawytscha). Transcription of four cytokine genes (IL1, TNF-alpha, IL-8, IL8-R) and two control genes (IgM and RPS-11) was measured relative to an endogenous control (EF1a) before and 24 h after immune stimulation with Vibrio vaccine. Additive genetic variation was not significant for cytokine transcription and heritability ranged from 0.44 (in pre-challenge IL1) to 0.04 (in post-challenge TNF-alpha). Non-additive genetic variance was significant in post-challenge IL1 (18 %) and TNF-alpha (12 %) while maternal effects contributed to pre-challenge cytokine transcription. Cytokine transcription co-expressed within but not between pre- and post-challenge states. The lack of additive genetic effects indicates that cytokine transcription is not a likely candidate for selection programs to improve immune function in Chinook salmon. Our results add to the growing evidence that non-additivity in salmon is common and contributes to our understanding of the genetic architecture of transcription. This indicates that transcription variation may act to maintain genetic variation and facilitate rapid adaptive response in salmonids.

Purple sulfur bacteria, which are known to be the most ancient among anoxygenic phototrophs, play an important role in the global sulfur cycle. Allochromatium vinosum oxidizes reduced sulfur compounds such as hydrogen sulfide, elemental sulfur and thiosulfide. At low oxygen concentrations, A. vinosum can grow chemotrophically using oxygen as the terminal electron acceptor. Being also a nitrogen fixer, A. vinosum is faced with the paradox of co-existence of aerobic metabolism and nitrogen fixation. Due to growth difficulties, only a few studies have dealt with the aerobic metabolism of the organism and, until now, there has been no information about the genes involved in the respiratory metabolism of purple sulfur bacteria. In this article we show the first terminal oxidase gene for A. vinosum. The presence of a Bd type of quinol oxidase is necessary to protect nitrogenases against the inhibitory effects of oxygen. In this case, a nitrogen fixation related gene is part of the cyd operon and this gene is co-transcribed with cydAB genes. Bd oxidase of A. vinosum may be the earliest form of oxidase where the function of the enzyme is to scavenge the contaminant oxygen during nitrogen fixation. This may be an important clue about the early evolution of oxygenic photosynthesis, perhaps as a protective mechanism for nitrogen fixation.

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.

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. Age at maturity in Atlantic salmon has been associated with a single locus with sex-specific effects. Here, the authors show rapid evolution towards early maturity in males of a large salmon population induced by sex-specific selection during sea migration.

Atlantic salmon (Salmo salar) is a species with diverse life‐history strategies, to which the timing of maturation contributes considerably. Recently, the genome region including the gene vgll3 has gained attention as a locus with a large effect on Atlantic salmon maturation timing, and recent studies on the vgll3 locus in salmon have indicated that its effect might be mediated through body condition and accumulation of adipose tissue. However, the cellular and physiological pathways leading from vgll3 genotype to phenotype are still unknown. Standard metabolic rate is a potentially important trait for resource acquisition and assimilation and we hypothesized that this trait, being a proxy for the maintenance energy expenditure of an individual, could be an important link in the pathway from vgll3 genotype to maturation timing phenotype. As a first step to studying links between vgll3 and the metabolic phenotype of Atlantic salmon, we measured the standard metabolic rate of 150 first‐year Atlantic salmon juveniles of both sexes, originating from 14 different families with either late‐maturing or early‐maturing vgll3 genotypes. No significant difference in mass‐adjusted standard metabolic rate was detected between individuals with different vgll3 genotypes, indicating that juvenile salmon of different vgll3 genotypes have similar maintenance energy requirements in the experimental conditions used and that the effects of vgll3 on body condition and maturation are not strongly related to maintenance energy expenditure in either sex at this life stage., We show that vgll3, a gene known to have significant effects on Atlantic salmon (Salmo salar) life‐history strategy, does not associate with standard metabolic rate in salmon juveniles. This indicates that the effects of vgll3 on age at maturity is not strongly related to maintenance energy expenditure or related physiological mechanisms at the life stage and conditions used in this study.