Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere.

Most Atlantic salmon (Salmo salar L.) populations follow an anadromous life cycle, spending early life in freshwater, migrating to the sea for feeding, and returning to rivers to spawn. At the end of the last ice age ~10,000 years ago, several populations of Atlantic salmon became landlocked. Comparing their genomes to their anadromous counterparts can help identify genetic variation related to either freshwater residency or anadromy. The objective of this study was to identify consistently divergent loci between anadromous and landlocked Atlantic salmon strains throughout their geographical distribution, with the long-term aim of identifying traits relevant for salmon aquaculture, including fresh and seawater growth, omega-3 metabolism, smoltification, and disease resistance. We used a Pool-seq approach (n = 10-40 individuals per population) to sequence the genomes of twelve anadromous and six landlocked Atlantic salmon populations covering a large part of the Northern Hemisphere and conducted a genomewide association study to identify genomic regions having been under different selection pressure in landlocked and anadromous strains. A total of 28 genomic regions were identified and included cadm1 on Chr 13 and ppargc1a on Chr 18. Seven of the regions additionally displayed consistently reduced heterozygosity in fish obtained from landlocked populations, including the genes gpr132, cdca4, and sertad2 on Chr 15. We also found 16 regions, including igf1 on Chr 17, which consistently display reduced heterozygosity in the anadromous populations compared to the freshwater populations, indicating relaxed selection on traits associated with anadromy in landlocked salmon. In conclusion, we have identified 37 regions which may harbor genetic variation relevant for improving fish welfare and quality in the salmon farming industry and for understanding life-history traits in fish.

Population genomics reveals repeated signals of adaptive divergence in the Atlantic salmon of north-eastern Europe.

Our ability to examine genetic variation across entire genomes has enabled many studies searching for the genetic basis of local adaptation. These studies have identified numerous loci as candidates for differential local selection; however, relatively few have examined the overlap among candidate loci identified from independent studies of the same species in different geographic areas or evolutionary lineages. We used an allelotyping approach with a 220K SNP array to characterize the population genetic structure of Atlantic salmon in north-eastern Europe and ask whether the same genomic segments emerged as outliers among populations in different geographic regions. Genome-wide data recapitulated the phylogeographic structure previously inferred from mtDNA and microsatellite markers. Independent analyses of three genetically and geographically distinct groups of populations repeatedly inferred the same 17 haploblocks to contain loci under differential local selection. The most strongly supported of these replicated haploblocks had known strong associations with life-history variation or immune response in Atlantic salmon. Our results are consistent with these genomic segments harbouring large-effect loci which have a major role in Atlantic salmon diversification and are ideal targets for validation studies.

Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar).

Understanding the genomic basis of host-parasite adaptation is important for predicting the long-term viability of species and developing successful management practices. However, in wild populations, identifying specific signatures of parasite-driven selection often presents a challenge, as it is difficult to unravel the molecular signatures of selection driven by different, but correlated, environmental factors. Furthermore, separating parasite-mediated selection from similar signatures due to genetic drift and population history can also be difficult. Populations of Atlantic salmon (Salmo salar L.) from northern Europe have pronounced differences in their reactions to the parasitic flatworm Gyrodactylus salaris Malmberg 1957 and are therefore a good model to search for specific genomic regions underlying inter-population differences in pathogen response. We used a dense Atlantic salmon SNP array, along with extensive sampling of 43 salmon populations representing the two G. salaris response extremes (extreme susceptibility vs resistant), to screen the salmon genome for signatures of directional selection while attempting to separate the parasite effect from other factors. After combining the results from two independent genome scan analyses, 57 candidate genes potentially under positive selection were identified, out of which 50 were functionally annotated. This candidate gene set was shown to be functionally enriched for lymph node development, focal adhesion genes and anti-viral response, which suggests that the regulation of both innate and acquired immunity might be an important mechanism for salmon response to G. salaris. Overall, our results offer insights into the apparently complex genetic basis of pathogen susceptibility in salmon and highlight methodological challenges for separating the effects of various environmental factors.

Protein degradation systems in the skeletal muscles of parr and smolt Atlantic salmon Salmo salar L. and brown trout Salmo trutta L.

Although protein degradation limits the rate of muscle growth in fish, the role of proteolytic systems responsible for degrading myofibrillar proteins in skeletal muscle is not well defined. The study herein aims to evaluate the role of calpains (calcium-activated proteases) and proteasomes (ATP-dependent proteases) in mediating muscle protein turnover at different life stages in wild salmonids. Protease activities were estimated in Atlantic salmon (Salmo salar L.) and brown trout (Salmo trutta L.) parr and smolts from the Indera River (Kola Peninsula, Russia). Calpain and proteasome activities in Atlantic salmon skeletal muscles were lower in smolts as compared with parr. Reduced muscle protein degradation accompanying Atlantic salmon parr-smolt transformation appeared to provide intense muscle growth essential for a minimum threshold size achievement that is required for smoltification. Calpain and proteasome activities in brown trout parr and smolts at age 3+ did not significantly differ. However, calpain activity was higher in smolts brown trout 4+ as compared with parr, while proteasome activity was lower. Results suggest that brown trout smoltification does not correspond with intense muscle growth and is more facultative and plastic in comparison with Atlantic salmon smoltification. Obtained data on muscle protein degradation capacity as well as length-weight parameters of fish reflect differences between salmon and trout in growth and smoltification strategies.

Age-Specific Lipid and Fatty Acid Profiles of Atlantic Salmon Juveniles in the Varzuga River.

The age-specific lipid and fatty acid profiles of juvenile Atlantic salmon at different ages (0+, 1+, and 2+ years) after hatching from nests located in the mainstream of a large Arctic River, the Varzuga River, and resettling to the favorable Sobachji shoal in autumn before overwinter are herein presented. The contemporary methods of the lipid analysis were used: thin layer chromatography and gas chromatography. The results show that the stability of the regulation of important functions in developing organisms is maintained through structural alterations in lipids. These alterations can be considered as a sequence of the modifications and changes in the ratios of certain lipid classes and fatty acids constituents. In general, changes in the lipids and fatty acids (FAs) maintained the physiological limits and controls through the adaptive systems of the organism. The mechanisms of juvenile fish biochemical adaptation to the environmental conditions in the studied biotope include the modification of the energy metabolism and anabolism, and here belongs to the energy characteristics of metabolic processes.

Features in the Lipid Status of Two Generations of Fingerlings (0+) of Atlantic Salmon (Salmo salar L.) Inhabiting the Arenga River (Kola Peninsula).

The present research focused on determining the lipid status of salmon fingerlings (0+) in early development after dispersal form groups of spawning nests in biotopes of different hydrological conditions. The revealed qualitative and quantitative differences in the levels of phospholipids and fatty acids among two generations of Atlantic salmon fingerlings (0+) living in different biotopes of the Arenga River (a tributary of the Varzuga River) may be associated with the peculiarities of their genetically determined processes of the biosynthesis and modification of individual lipid classes and trophoecological factors (food spectrum, quality and availability of food objects, and hydrological regime). The research was organized to observe the dynamics of these developmental changes from ages 0+ to 2+.

Footprints of directional selection in wild Atlantic salmon populations: evidence for parasite-driven evolution?

Mechanisms of host-parasite co-adaptation have long been of interest in evolutionary biology; however, determining the genetic basis of parasite resistance has been challenging. Current advances in genome technologies provide new opportunities for obtaining a genome-scale view of the action of parasite-driven natural selection in wild populations and thus facilitate the search for specific genomic regions underlying inter-population differences in pathogen response. European populations of Atlantic salmon (Salmo salar L.) exhibit natural variance in susceptibility levels to the ectoparasite Gyrodactylus salaris Malmberg 1957, ranging from resistance to extreme susceptibility, and are therefore a good model for studying the evolution of virulence and resistance. However, distinguishing the molecular signatures of genetic drift and environment-associated selection in small populations such as land-locked Atlantic salmon populations presents a challenge, specifically in the search for pathogen-driven selection. We used a novel genome-scan analysis approach that enabled us to i) identify signals of selection in salmon populations affected by varying levels of genetic drift and ii) separate potentially selected loci into the categories of pathogen (G. salaris)-driven selection and selection acting upon other environmental characteristics. A total of 4631 single nucleotide polymorphisms (SNPs) were screened in Atlantic salmon from 12 different northern European populations. We identified three genomic regions potentially affected by parasite-driven selection, as well as three regions presumably affected by salinity-driven directional selection. Functional annotation of candidate SNPs is consistent with the role of the detected genomic regions in immune defence and, implicitly, in osmoregulation. These results provide new insights into the genetic basis of pathogen susceptibility in Atlantic salmon and will enable future searches for the specific genes involved.

Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar).

Migrations between different habitats are key events in the lives of many organisms. Such movements involve annually recurring travel over long distances usually triggered by seasonal changes in the environment. Often, the migration is associated with travel to or from reproduction areas to regions of growth. Young anadromous Atlantic salmon (Salmo salar) emigrate from freshwater nursery areas during spring and early summer to feed and grow in the North Atlantic Ocean. The transition from the freshwater ('parr') stage to the migratory stage where they descend streams and enter salt water ('smolt') is characterized by morphological, physiological and behavioural changes where the timing of this parr-smolt transition is cued by photoperiod and water temperature. Environmental conditions in the freshwater habitat control the downstream migration and contribute to within- and among-river variation in migratory timing. Moreover, the timing of the freshwater emigration has likely evolved to meet environmental conditions in the ocean as these affect growth and survival of the post-smolts. Using generalized additive mixed-effects modelling, we analysed spatio-temporal variations in the dates of downstream smolt migration in 67 rivers throughout the North Atlantic during the last five decades and found that migrations were earlier in populations in the east than the west. After accounting for this spatial effect, the initiation of the downstream migration among rivers was positively associated with freshwater temperatures, up to about 10 °C and levelling off at higher values, and with sea-surface temperatures. Earlier migration occurred when river discharge levels were low but increasing. On average, the initiation of the smolt seaward migration has occurred 2.5 days earlier per decade throughout the basin of the North Atlantic. This shift in phenology matches changes in air, river, and ocean temperatures, suggesting that Atlantic salmon emigration is responding to the current global climate changes.

Temporal variation of genetic composition in Atlantic salmon populations from the Western White Sea Basin: influence of anthropogenic factors?

BACKGROUND: Studies of the temporal patterns of population genetic structure assist in evaluating the consequences of demographic and environmental changes on population stability and persistence. In this study, we evaluated the level of temporal genetic variation in 16 anadromous and 2 freshwater salmon populations from the Western White Sea Basin (Russia) using samples collected between 1995 and 2008. To assess whether the genetic stability was affected by human activity, we also evaluated the effect of fishing pressure on the temporal genetic variation in this region. RESULTS: We found that the genetic structure of salmon populations in this region was relatively stable over a period of 1.5 to 2.5 generations. However, the level of temporal variation varied among geographical regions: anadromous salmon of the Kola Peninsula exhibited a higher stability compared to that of the anadromous and freshwater salmon from the Karelian White Sea coast. This discrepancy was most likely attributed to the higher census, and therefore effective, population sizes of the populations inhabiting the rivers of the Kola Peninsula compared to salmon of the Karelian White Sea coast. Importantly, changes in the genetic diversity observed in a few anadromous populations were best explained by the increased level of fishing pressure in these populations rather than environmental variation or the negative effects of hatchery escapees. The observed population genetic patterns of isolation by distance remained consistent among earlier and more recent samples, which support the stability of the genetic structure over the period studied. CONCLUSIONS: Given the increasing level of fishing pressure in the Western White Sea Basin and the higher level of temporal variation in populations exhibiting small census and effective population sizes, further genetic monitoring in this region is recommended, particularly on populations from the Karelian rivers.