Thiamin dynamics during the adult life cycle of Atlantic salmon (Salmo salar).

Thiamin is an essential water-soluble B vitamin known for its wide range of metabolic functions and antioxidant properties. Over the past decades, reproductive failures induced by thiamin deficiency have been observed in several salmonid species worldwide, but it is unclear why this micronutrient deficiency arises. Few studies have compared thiamin concentrations in systems of salmonid populations with or without documented thiamin deficiency. Moreover, it is not well known whether and how thiamin concentration changes during the marine feeding phase and the spawning migration. Therefore, samples of Atlantic salmon (Salmo salar) were collected when actively feeding in the open Baltic Sea, after the sea migration to natal rivers, after river migration, and during the spawning period. To compare populations of Baltic salmon with systems without documented thiamin deficiency, a population of landlocked salmon located in Lake Vänern (Sweden) was sampled as well as salmon from Norwegian rivers draining into the North Atlantic Ocean. Results showed the highest mean thiamin concentrations in Lake Vänern salmon, followed by North Atlantic, and the lowest in Baltic populations. Therefore, salmon in the Baltic Sea seem to be consistently more constrained by thiamin than those in other systems. Condition factor and body length had little to no effect on thiamin concentrations in all systems, suggesting that there is no relation between the body condition of salmon and thiamin deficiency. In our large spatiotemporal comparison of salmon populations, thiamin concentrations declined toward spawning in all studied systems, suggesting that the reduction in thiamin concentration arises as a natural consequence of starvation rather than to be related to thiamin deficiency in the system. These results suggest that factors affecting accumulation during the marine feeding phase are key for understanding the thiamin deficiency in salmonids.

Large-effect loci mediate rapid adaptation of salmon body size after river regulation.

Understanding the potential of natural populations to adapt to altered environments is becoming increasingly relevant in evolutionary research. Currently, our understanding of adaptation to human alteration of the environment is hampered by lack of knowledge on the genetic basis of traits, lack of time series, and little or no information on changes in optimal trait values. Here, we used time series data spanning nearly a century to investigate how the body mass of Atlantic salmon (Salmo salar) adapts to river regulation. We found that the change in body mass followed the change in waterflow, both decreasing to ∼1/3 of their original values. Allele frequency changes at two loci in the regions of vgll3 and six6 predicted more than 80% of the observed body mass reduction. Modeling the adaptive dynamics revealed that the population mean lagged behind its optimum before catching up approximately six salmon generations after the initial waterflow reduction. Our results demonstrate rapid adaptation mediated by large-effect loci and provide insight into the temporal dynamics of evolutionary rescue following human disturbance.

Introgression from farmed escapees affects the full life cycle of wild Atlantic salmon.

After a half a century of salmon farming, we have yet to understand how the influx of genes from farmed escapees affects the full life history of Atlantic salmon (Salmo salar L.) in the wild. Using scale samples of over 6900 wild adult salmon from 105 rivers, we document that increased farmed genetic ancestry is associated with increased growth throughout life and a younger age at both seaward migration and sexual maturity. There was large among-population variation in the effects of introgression. Most saliently, the increased growth at sea following introgression declined with the population's average growth potential. Variation at two major-effect loci associated with age at maturity was little affected by farmed genetic ancestry and could not explain the observed phenotypic effects of introgression. Our study provides knowledge crucial for predicting the ecological and evolutionary consequences of increased aquaculture production worldwide.

Growth-enhanced salmon modify stream ecosystem functioning.

Use of fast-growing domesticated and/or genetically modified strains of fish is becoming increasingly common in aquaculture, increasing the likelihood of deliberate or accidental introductions into the wild. To date, their ecological impacts on ecosystems remain to be quantified. Here, using a controlled phenotype manipulation by implanting growth hormone in juvenile Atlantic salmon (Salmo salar), we found that growth-enhanced fish display changes in several phenotypic traits known to be important for ecosystem functioning, such as habitat use, morphology and excretion rate. Furthermore, these phenotypic changes were associated with significant impacts on the invertebrate community and key stream ecosystem functions such as primary production and leaf-litter decomposition. These findings provide novel evidence that introductions of growth-enhanced fish into the wild can affect the functioning of natural ecosystems and represent a form of intraspecific invasion. Consequently, environmental impact assessments of growth-enhanced organisms need to explicitly consider ecosystem-level effects.

Selection against individuals from genetic introgression of escaped farmed salmon in a natural population of Atlantic salmon.

The viability of wild Atlantic salmon populations is threatened by genetic introgression from escaped farmed salmon. Farmed Atlantic salmon are genetically improved for important commercial traits and a life in captivity but are poorly adapted to the natural environment. The rate of gene flow from escaped farmed to wild salmon depends on their spawning success and on offspring survival at various life stages. We here investigate relative survival of introgressed juvenile Atlantic salmon (parr) in a river in northern Norway. The studied population has experienced genetic introgression from farmed salmon for about four generations (20 years). We followed two cohorts of parr from the year of hatching (0+) to the age of 2 years (2+). Farmed genetic introgression was quantified at the individual level and on a continuous scale using diagnostic SNPs. Population-level genetic introgression decreased from 0+ to 2+ by 64% (2011 cohort) and 37% (2013 cohort). This change was driven by a 70% (2011 cohort) and 49% (2013 cohort) lower survival from age 0+ to 2+ in introgressed parr compared to parr of wild origin. Our observations show that there is natural selection against genetic introgression with a potential cost of lower productivity.

The structural variation landscape in 492 Atlantic salmon genomes.

Structural variants (SVs) are a major source of genetic and phenotypic variation, but remain challenging to accurately type and are hence poorly characterized in most species. We present an approach for reliable SV discovery in non-model species using whole genome sequencing and report 15,483 high-confidence SVs in 492 Atlantic salmon (Salmo salar L.) sampled from a broad phylogeographic distribution. These SVs recover population genetic structure with high resolution, include an active DNA transposon, widely affect functional features, and overlap more duplicated genes retained from an ancestral salmonid autotetraploidization event than expected. Changes in SV allele frequency between wild and farmed fish indicate polygenic selection on behavioural traits during domestication, targeting brain-expressed synaptic networks linked to neurological disorders in humans. This study offers novel insights into the role of SVs in genome evolution and the genetic architecture of domestication traits, along with resources supporting reliable SV discovery in non-model species.

Domestication leads to increased predation susceptibility.

Domestication involves adapting animals to the human-controlled environment. Genetic changes occurring during the domestication process may manifest themselves in phenotypes that render domesticated animals maladaptive for life in the wild. Domesticated Atlantic salmon frequently interbreed with wild conspecifics, and their offspring display reduced survival in the wild. However, the mechanism(s) contributing to their lower survival in the wild remains a subject of conjecture. Here, we document higher susceptibility to predation by brown trout in fast-growing domesticated salmon, as compared to their slow-growing wild conspecifics, demonstrating that directional selection for increased growth comes at a cost of decreased survival when under the risk of predation, as predicted by the growth/predation risk trade-off. Despite earlier documentation of altered risk-taking behavior, this study demonstrates for the first time that domestication of Atlantic salmon has lead to increased predation susceptibility, and that this consitutes a mechanism underpinning the observed survial differences in the wild.

Life-history genomic regions explain differences in Atlantic salmon marine diet specialization.

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. We aimed to test the hypothesis that heritable resource acquisition variation that covaries with efficiency along the ontogeny would influence maturation timing of individuals. 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. 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. 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.

Host specificity drives genetic structure in a freshwater mussel.

Parasites often depend on their hosts for long distance transport, and genetic population structure can be strongly affected by host specificity and dispersal. Freshwater pearl mussel (Margaritifera margaritifera) populations have previously been found to naturally infest either primarily Atlantic salmon ('salmon-mussel') or exclusively brown trout ('trout-mussel') across a wide geographic range. Here, we experimentally test whether this intraspecific variation in natural infestation can be explained by host specificity in freshwater pearl mussel. Our experiments show that when both host species were exposed to larvae from salmon- and trout-mussel respectively, salmon-mussel larvae almost never infested brown trout and vice versa. This suggests that host specificity can explain variation in natural infestation among the studied freshwater pearl mussel populations. Host specificity provides a link to the species' variable population genetic structure, as mussel populations limited to Atlantic salmon, the host with stronger dispersal, show higher genetic diversity and weaker differentiation than populations limited to brown trout as host.

Can variation in standard metabolic rate explain context-dependent performance of farmed Atlantic salmon offspring?

Escaped farmed Atlantic salmon interbreed with wild Atlantic salmon, leaving offspring that often have lower success in nature than pure wild salmon. On top of this, presence of farmed salmon descendants can impair production of wild-type recruits. We hypothesize that both these effects connect with farmed salmon having acquired higher standard metabolic rates (SMR, the energetic cost of self-maintenance) during domestication. Fitness-related advantages of phenotypic traits associated with both high SMR and farmed salmon (e.g., social dominance) depend on environmental conditions, such as food availability. We hypothesize that farmed offspring have an advantage at high food availability due to, for example, dominance behavior but suffer increased risks of starvation when food is scarce because this behavior is energy-demanding. To test these hypotheses, we first compare embryo SMR of pure farmed, farmed-wild hybrids and pure wild offspring. Next, we test early-life performance (in terms of survival and growth) of hybrids relative to that of their wild half-siblings, as well as their competitive abilities, in semi-natural conditions of high and low food availability. Finally, we test how SMR affects early-life performance at high and low food availability. We find inconclusive support for the hypothesis that domestication has induced increased SMR. Further, wild and hybrid juveniles had similar survival and growth in the semi-natural streams. Yet, the presence of hybrids led to decreased survival of their wild half-siblings. Contrary to our hypothesis about context-dependency, these effects were not modified by food availability. However, wild juveniles with high SMR had decreased survival when food was scarce, but there was no such effect at high food availability. This study provides further proof that farmed salmon introgression may compromise the viability of wild salmon populations. We cannot, however, conclude that this is connected to alterations in the metabolic phenotype of farmed salmon.

Supplementary stocking selects for domesticated genotypes.

Stocking of hatchery produced fish is common practise to mitigate declines in natural populations and may have unwanted genetic consequences. Here we describe a novel phenomenon arising where broodstock used for stocking may be introgressed with farmed individuals. We test how stocking affects introgression in a wild population of Atlantic salmon (Salmo salar) by quantifying how the number of adult offspring recaptured in a stocked river depend on parental introgression. We found that hatchery conditions favour farmed genotypes such that introgressed broodstock produce up to four times the number of adult offspring compared to non-introgressed broodstock, leading to increased introgression in the recipient spawning population. Our results provide the first empirical evidence that stocking can unintentionally favour introgressed individuals and through selection for domesticated genotypes compromise the fitness of stocked wild populations.

Gene flow from domesticated escapes alters the life history of wild Atlantic salmon.

Interbreeding between domesticated and wild animals occurs in several species. This gene flow has long been anticipated to induce genetic changes in life-history traits of wild populations, thereby influencing population dynamics and viability. Here, we show that individuals with high levels of introgression (domesticated ancestry) have altered age and size at maturation in 62 wild Atlantic salmon Salmo salar populations, including seven ancestral populations to breeding lines of the domesticated salmon. This study documents widespread changes to life-history traits in wild animal populations following gene flow from selectively bred, domesticated conspecifics. The continued high abundance of escaped, domesticated Atlantic salmon thus threatens wild Atlantic salmon populations by inducing genetic changes in fitness-related traits. Our results represent key evidence and a timely warning concerning the potential ecological impacts of the globally increasing use of domesticated animals.

Evaluating the Ryman-Laikre effect for marine stock enhancement and aquaculture.

The Ryman-Laikre (R-L) effect is an increase in inbreeding and a reduction in total effective population size (NeT ) in a combined captive-wild system, which arises when a few captive parents produce large numbers of offspring. To facilitate evaluation of the R-L effect for scenarios that are relevant to marine stock enhancement and aquaculture, we extended the original R-L formula to explicitly account for several key factors that determine NeT , including the numbers of captive and wild adults, the ratio of captive to wild Ne/N (ß), productivity of captive and wild breeders, and removal of individuals from the wild for captive breeding. We show how to provide quantitative answers to questions such as: What scenarios lead to no loss of effective size? What is the maximum effective size that can be achieved? and What scenarios insure that NeT will be no smaller than a specified value? Important results include the following: (1) For large marine populations, the value of ß becomes increasingly important as the captive contribution increases. Captive propagation will sharply reduce NeT unless the captive contribution is very small or ß is very large (∼103 or higher). (2) Very large values of ß are only possible if wild Ne/N is tiny. Therefore, large wild populations undergoing captive enhancement at even modest levels will suffer major reductions in effective size unless wild Ne is a tiny fraction of the census size (about 10-4 or lower).

Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon.

Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific loci underlying sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here we identify a large effect locus controlling age at maturity in Atlantic salmon (Salmo salar), an important fitness trait in which selection favours earlier maturation in males than females, and show it is a clear example of sex-dependent dominance that reduces intralocus sexual conflict and maintains adaptive variation in wild populations. Using high-density single nucleotide polymorphism data across 57 wild populations and whole genome re-sequencing, we find that the vestigial-like family member 3 gene (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39% of phenotypic variation, an unexpectedly large proportion for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal allowing greater optimization of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.

A standardized method for quantifying unidirectional genetic introgression.

Genetic introgression of domesticated to wild conspecifics is of great concern to the genetic integrity and viability of the wild populations. Therefore, we need tools that can be used for monitoring unidirectional gene flow from domesticated to wild populations. A challenge to quantitation of unidirectional gene flow is that both the donor and the recipient population may be genetically substructured and that the subpopulations are subjected to genetic drift and may exchange migrants between one another. We develop a standardized method for quantifying and monitoring domesticated to wild gene flow and demonstrate its usefulness to farm and wild Atlantic salmon as a model species. The challenge of having several wild and farm populations was circumvented by in silico generating one analytical center point for farm and wild salmon, respectively. Distributions for the probability that an individual is wild were generated from individual-based analyses of observed wild and farm genotypes using STRUCTURE. We show that estimates of proportions of the genome being of domesticated origin in a particular wild population can be obtained without having a historical reference sample for the same population. The main advantages of the method presented are the standardized way in which genetic processes within and between populations are taken into account, and the individual-based analyses giving estimates for each individual independent of other individuals. The method makes use of established software, and as long as genetic markers showing generic genetic differences between domesticated and wild populations are available, it can be applied to all species with unidirectional gene flow. Results from our method are easy to interpret and understand, and will serve as a powerful tool for management, especially because there is no need for a specific historical wild reference sample.

Spatial and temporal genetic structure of a river-resident Atlantic salmon (Salmo salar) after millennia of isolation.

The river-resident Salmo salar ("småblank") has been isolated from other Atlantic salmon populations for 9,500 years in upper River Namsen, Norway. This is the only European Atlantic salmon population accomplishing its entire life cycle in a river. Hydropower development during the last six decades has introduced movement barriers and changed more than 50% of the river habitat to lentic conditions. Based on microsatellites and SNPs, genetic variation within småblank was only about 50% of that in the anadromous Atlantic salmon within the same river. The genetic differentiation (F ST) between småblank and the anadromous population was 0.24. This is similar to the differentiation between anadromous Atlantic salmon in Europe and North America. Microsatellite analyses identified three genetic subpopulations within småblank, each with an effective population size Ne of a few hundred individuals. There was no evidence of reduced heterozygosity and allelic richness in contemporary samples (2005-2008) compared with historical samples (1955-56 and 1978-79). However, there was a reduction in genetic differentiation between sampling localities over time. SNP data supported the differentiation of småblank into subpopulations and revealed downstream asymmetric gene flow between subpopulations. In spite of this, genetic variation was not higher in the lower than in the upper areas. The meta-population structure of småblank probably maintains genetic variation better than one panmictic population would do, as long as gene flow among subpopulations is maintained. Småblank is a unique endemic island population of Atlantic salmon. It is in a precarious situation due to a variety of anthropogenic impacts on its restricted habitat area. Thus, maintaining population size and avoiding further habitat fragmentation are important.

SNP-array reveals genome-wide patterns of geographical and potential adaptive divergence across the natural range of Atlantic salmon (Salmo salar).

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

Generic genetic differences between farmed and wild Atlantic salmon identified from a 7K SNP-chip.

Genetic interactions between farmed and wild conspecifics are of special concern in fisheries where large numbers of domesticated individuals are released into the wild. In the Atlantic salmon (Salmo salar), selective breeding since the 1970's has resulted in rapid genetic changes in commercially important traits, such as a doubling of the growth rate. Each year, farmed salmon escape from net pens, enter rivers, and interbreed with wild salmon. Field experiments demonstrate that genetic introgression may weaken the viability of recipient populations. However, due to the lack of diagnostic genetic markers, little is known about actual rates of gene flow from farmed to wild populations. Here we present a panel of 60 single nucleotide polymorphisms (SNPs) that collectively are diagnostic in identifying individual salmon as being farmed or wild, regardless of their populations of origin. These were sourced from a pool of 7000 SNPs comparing historical wild and farmed salmon populations, and were distributed on all but two of the 29 chromosomes. We suggest that the generic differences between farmed and wild salmon at these SNPs have arisen due to domestication. The identified panel of SNPs will permit quantification of gene flow from farmed to wild salmon populations, elucidating one of the most controversial potential impacts of aquaculture. With increasing global interest in aquaculture and increasing pressure on wild populations, results from our study have implications for a wide range of species.

Atlantic salmon eggs favour sperm in competition that have similar major histocompatibility alleles.

Polyandry and post-copulatory sexual selection provide opportunities for the evolution of female differential sperm selection. Here, we examined the influence of variation in major histocompatibility (MH) class I allelic composition upon sperm competition dynamics in Atlantic salmon. We ran in vitro fertilization competitions that mimicked the gametic microenvironment, and replicated a paired-male experimental design that allowed us to compare differences in sperm competition success among males when their sperm compete for eggs from females that were genetically either similar or dissimilar at the MH class I locus. Concurrently, we measured variation in spermatozoal traits that are known to influence relative fertilization success under these conditions. Contrary to the findings demonstrating mechanisms that promote MH complex heterozygosity, our results showed that males won significantly greater relative fertilization success when competing for eggs from genetically similar females at the MH class I. This result also showed covariation with the known influences of sperm velocity on relative fertilization success. We discuss these unexpected findings in relation to sperm-egg recognition and hybridization avoidance mechanisms based upon immunogenetic variation.

Asymmetric competition drives lake use of coexisting salmonids.

To what degree are population differences in resource use caused by competition and the occupation of adjacent positions along environmental gradients evidence of competition? Habitat use may be the result of a competitive lottery, or restricted by competition. We tested to what extent population differences in habitat use of two salmonids, cutthroat trout (Oncorhynchus clarki) and Dolly Varden charr (Salvelinus malma) were influenced by interspecific competition. We hypothesized that the depth distribution of Dolly Varden charr would be affected by competition from the more littoral and surface-oriented cutthroat trout, and that the depth distribution of cutthroat trout would be little affected by competition from Dolly Varden charr. Sympatric populations of cutthroat trout and Dolly Varden charr were created by reciprocal transfers of previously allopatric populations in two experimental lakes. We found evidence of asymmetric competition, as Dolly Varden charr were displaced from littoral habitats when sympatric with cutthroat trout, whereas cutthroat trout remained unaffected by the presence of Dolly Varden charr. Evolved differences between the species, and differences between experimental lakes, also contributed to population differences in habitat use, but asymmetric competition remained as the main driver of different depth distributions in sympatry.