Biochemical genetics of the Atlantic salmon Salmo salar L.

In recent years, blood group and protein polymorphisms in Atlantic salmon have been investigated extensively with a view, primarily, to their use in identifying individuals of different spawning populations present in high seas fisheries. Erythrocyte antigens, haemoglobins, serum proteins and various tissue enzymes—mainly esterases and de-hydrogenases—have been studied by electrophoretic and immunological techniques. These studies are reviewed here for the first time.
Many of the protein systems exhibit multiple components and this fact, together with cytological evidence, indicates the occurrence of tetraploidy in the course of Salmonid evolution. The significance of a tetraploid origin in the evolution and ecological adaptation of Salmonids is discussed briefly.
Some protein systems studied exhibit phylogenetic variation, and analyses of phenotype ratios and allele frequencies indicate that the populations of different river systems are genetically distinct. Allele frequencies have not yet been shown to be stable from generation to generation however, and some of the factors likely to affect allele frequencies are discussed.
Different spawning populations can not be identified in high seas fisheries using these protein characters, although it may be possible to identify the continent of origin (N. America or Europe) of some individuals. Indeed, it has been proposed independently by two groups that North American and European populations of Atlantic salmon be assigned to different sub-species viz. S. s. americanus and S. s. europaeus respectively. The contradictory evidence on which these taxa are proposed is discussed, together with the evidence for other population groups proposed in the European part of the salmon's range. The possible role and future direction of studies on the biochemical genetics of salmon are outlined.     

Temporal change in genetic integrity suggests loss of local adaptation in a wild Atlantic salmon (Salmo salar) population following introgression by farmed escapees

In some wild Atlantic salmon populations, rapid declines in numbers of wild returning adults has been associated with an increase in the prevalence of farmed salmon. Studies of phenotypic variation have shown that interbreeding between farmed and wild salmon may lead to loss of local adaptation. Yet, few studies have attempted to assess the impact of interbreeding at the genome level, especially among North American populations. Here, we document temporal changes in the genetic makeup of the severely threatened Magaguadavic River salmon population (Bay of Fundy, Canada), a population that might have been impacted by interbreeding with farmed salmon for nearly 20 years. Wild and farmed individuals caught entering the river from 1980 to 2005 were genotyped at 112 single-nucleotide polymorphisms (SNPs), and/or eight microsatellite loci, to scan for potential shifts in adaptive genetic variation. No significant temporal change in microsatellite-based estimates of allele richness or gene diversity was detected in the wild population, despite its precipitous decline in numbers over the last two decades. This might reflect the effect of introgression from farmed salmon, which was corroborated by temporal change in linkage-disequilibrium. Moreover, SNP genome scans identified a temporal decrease in candidate loci potentially under directional selection. Of particular interest was a SNP previously shown to be strongly associated with an important quantitative trait locus for parr mark number, which retained its genetic distinctiveness between farmed and wild fish longer than other outliers. Overall, these results indicate that farmed escapees have introgressed with wild Magaguadavic salmon resulting in significant alteration of the genetic integrity of the native population, including possible loss of adaptation to wild conditions.     

Widespread hybridization between native Atlantic salmon, Salmo salar, and introduced brown trout, S. trutta, in eastern Newfoundland

Hybridization between native Atlantic salmon and introduced brown trout was found to occur at a mean frequency of 0.9% in Atlantic salmon populations in eastern Newfoundland. Hybrids were detected in five of the 10 watersheds studied, but consideration of sampling error suggests that they could have been present in the remaining five watersheds although they were not detected. The frequency found in the Newfoundland and other North American salmon populations is significantly greater than the 0.3% reported for salmon populations in the British Isles, and both are higher than frequencies observed in salmon populations in Sweden. The higher frequency in North America is in accord with the prediction that hybridization between species will be more frequent where one species is introduced than in areas where both are native.     

Climate and ecosystem linkages explain widespread declines in North American Atlantic salmon populations

North American Atlantic salmon (Salmo salar) populations experienced substantial declines in the early 1990s, and many populations have persisted at low abundances in recent years. Abundance and productivity declined in a coherent manner across major regions of North America, and this coherence points toward a potential shift in marine survivorship, rather than local, river‐specific factors. The major declines in Atlantic salmon populations occurred against a backdrop of physical and biological shifts in Northwest Atlantic ecosystems. Analyses of changes in climate, physical, and lower trophic level biological factors provide substantial evidence that climate conditions directly and indirectly influence the abundance and productivity of North American Atlantic salmon populations. A major decline in salmon abundance after 1990 was preceded by a series of changes across multiple levels of the ecosystem, and a subsequent population change in 1997, primarily related to salmon productivity, followed an unusually low NAO event. Pairwise correlations further demonstrate that climate and physical conditions are associated with changes in plankton communities and prey availability, which are ultimately linked to Atlantic salmon populations. Results suggest that poor trophic conditions, likely due to climate‐driven environmental factors, and warmer ocean temperatures throughout their marine habitat area are constraining the productivity and recovery of North American Atlantic salmon populations.     

Microsatellite Variation in Populations of Atlantic Salmon from North Europe

Our aim was to investigate the level of genetic differentiation in northern European populations of Atlantic salmon, to establish the genetic relationship among major salmon populations in Russia and North Norway, and to compare these to populations from the western Atlantic lineage. Samples were collected along an east—west axis, from Pechora River in Russia to Restigouche River in Quebec, Canada. A total of 439 individual salmon were collected from seven rivers (sample sizes from 50 to 84 individuals). The samples were analysed for variation at four microsatellite loci; Ssa13.37, Ssa14, Ssa171 and Ssa171. Significant differences were found between most of the European populations, and the populations from the Tana and Pechora Rivers were most distinct. The samples from the Rivers Mezenskaya Pizhma and Emtsa in Arkhangelsk oblast in Russia were not significantly different from each other in an exact test of population differences. All other river pairs were significantly different. These results confirmed the deep genetic divergence between American and European salmon populations demonstrated in earlier studies, with alleles specific to continent found in three of the microsatellites.     

Growth and survival of Atlantic salmon (Salmo salar) in Llyn Dwythwch, North Wales

SUMMARY. Atlantic salmon fry have been annually stocked into Llyn Dwythwch, North Wales, since 1969, in an attempt to increase the natural stocks of the area. The growth and survival of 1- and 2-year-old salmon were investigated, and compared with that of other lake-reared populations and also with salmon in the natural stream environment. Lake-reared salmon follow the same patterns of slow and rapid growth as found for river fish, but the growth rate was superior in the former. The variation in length – weight relationship with age and sex was investigated. Survival rates in general compared favourably with the survival in rivers, with high mortality rates of salmon in Llyn Dwythwch resulting from predation at spring stocking by the resident brown trout. This was later avoided by stocking larger fish in the autumn.     

Genomewide single nucleotide polymorphism discovery in Atlantic salmon (Salmo salar): validation in wild and farmed American and European populations

A considerable number of single nucleotide polymorphisms (SNPs) are required to elucidate genotype–phenotype associations and determine the molecular basis of important traits. In this work, we carried out de novo SNP discovery accounting for both genome duplication and genetic variation from American and European salmon populations. A total of 9 736 473 nonredundant SNPs were identified across a set of 20 fish by whole‐genome sequencing. After applying six bioinformatic filtering steps, 200 K SNPs were selected to develop an Affymetrix Axiom^® myDesign Custom Array. This array was used to genotype 480 fish representing wild and farmed salmon from Europe, North America and Chile. A total of 159 099 (79.6%) SNPs were validated as high quality based on clustering properties. A total of 151 509 validated SNPs showed a unique position in the genome. When comparing these SNPs against 238 572 markers currently available in two other Atlantic salmon arrays, only 4.6% of the SNP overlapped with the panel developed in this study. This novel high‐density SNP panel will be very useful for the dissection of economically and ecologically relevant traits, enhancing breeding programmes through genomic selection as well as supporting genetic studies in both wild and farmed populations of Atlantic salmon using high‐resolution genomewide information.     

Atlantic salmon (Salmo salar L.) genetics in the 21st century: taking leaps forward in aquaculture and biological understanding

Atlantic salmon (Salmo salar L.) is among the most iconic and economically important fish species and was the first member of Salmonidae to have a high‐quality reference genome assembly published. Advances in genomics have become increasingly central to the genetic improvement of farmed Atlantic salmon as well as conservation of wild salmon stocks. The salmon genome has also been pivotal in shaping our understanding of the evolutionary and functional consequences arising from an ancestral whole‐genome duplication event characterising all Salmonidae members. Here, we provide a review of the current status of Atlantic salmon genetics and genomics, focussed on progress made from genome‐wide research aimed at improving aquaculture production and enhancing understanding of salmonid ecology, physiology and evolution. We present our views on the future direction of salmon genomics, including the role of emerging technologies (e.g. genome editing) in elucidating genetic features that underpin functional variation in traits of commercial and evolutionary importance.     

Variation in the timing of river entry of Atlantic salmon (Salmo salar L.) in the Baltic

The timing of river entry in the Atlantic salmon is known to depend on genetic,demographic and environmental factors,but little is known about the relative magnitude of among population and among year variation and covariation in this respect in natural state Atlantic salmon rives.To investigate this,variability in the timing of river entry in three historical Finnish Atlantic salmon populations were analyzed using salmon trap data collected during 1870-1902.The analyses reveled that 1)the timing of river e...     

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.     

Continental and ecological variance components of European and North American Atlantic salmon (Salmo salar) phenotypes

Juvenile Atlantic salmon ( Salmo salar ) meristic and morphometric characteristics were examined from 47 European and North American river populations. The relative importance of continental origin, stream gradient, overall temperature regime, and seasonal temperatures in explaining the phenotypic variation of these populations was evaluated using multi-way ANOVA. Ecological factors explained a greater percentage of the variance than continental origin for both meristic and morphometric characters. Stream gradient was the most important factor explaining morphometric variation and April-May mean temperature was the most important factor explaining meristic variation.     

The application of molecular markers to the study and conservation of fish populations, with special reference to Salmo

The main molecular techniques which can be used to generate genetic markers, and the applications of these markers to studies of fish populations are outlined. Published and ongoing studies, in the authors' laboratories, on brown trout and Atlantic salmon are used to compare the resolution and applicability of allozyme, mitochondrial DNA and minisatellite (variable number of tandem repeats) markers for studies on population structuring, genetic variation within populations, and the impact of the accidental and deliberate introduction of non-native salmonids on the genetic make-up of natural populations.     

Atlantic salmon colonization of the Russian Arctic coast: pioneers from North America

Previous studies of the ESTD * isozyme locus in the Atlantic salmon show the * 80 allele to be absent across the species' European range, with the exception of northern Russia, whereas the allele is nearly fixed in North American populations. The allele was found in samples from 15 out of 18 rivers on the Kola Peninsula and White sea coast and had frequencies that ranged from 0·017 to 0·363. Typing of fish in nine of these rivers for mtDNA variation in the ND1 gene region found variation characteristic of North American salmon in three Kola Peninsula populations and is the only part of Europe where such variants have been detected. The study area was completely glaciated during the late Pleistocene period and the restriction of the European distribution of these ESTD * and mtDNA variants to this area suggests that salmon that colonized the Russian Arctic coast rivers included fish of North American origin after the Pleistocene glacier had retreated.     

Genetic interactions between marine finfish species in European aquaculture and wild conspecifics

The principal species of marine aquaculture in Europe are Atlantic salmon (Salmo salar), sea bass (Dicentrarchus labrax) and sea bream (Sparus auratus). For Atlantic salmon and sea bass, a substantial part of total genetic variation is partitioned at the geographical population level. In the case of sea bream, gene flow across the Azores/Mediterranean scale appears to be extensive and population structuring is not detected. For Atlantic salmon and sea bass, natural population structure is at risk from genetic interaction with escaped aquaculture conspecifics. The locally adaptive features of populations are at risk from interbreeding with non‐local aquaculture fish. Wild populations, generally, are at risk from interactions with aquaculture fish that have been subject to artificial selection or domestication. Atlantic salmon is the main European aquaculture species and its population genetics and ecology have been well‐studied. A general case regarding genetic interactions can be based on the information available for salmon and extended to cover other species, in the appropriate context. A generalized flow chart for interactions is presented. Salmon escape from aquaculture at all life stages, and some survive to breed among wild salmon. Reproductive fitness in the escaped fish is lower than in native, wild fish because of behavioural deficiencies at spawning. However, as the number of salmon in aquaculture greatly exceeds the number of wild fish, even small fractional rates of escape may result in the local presence of large numbers, and high frequencies, of escaped fish. At present, policy and legislation in relation to minimizing genetic interactions between wild and aquaculture fish is best developed for Atlantic salmon, through the recommendations of the Oslo Agreement developed by the North Atlantic Salmon Conservation Organization and subsequent agreements on their implementation. In future, the potential use of genetically modified fish in aquaculture will make additional policy development necessary. Improved containment is recommended as the key to minimizing the numbers and therefore the effects of escaped fish. Emergency recovery procedures are recommended as a back‐up measure in the case of containment failure. Reproductive sterility is recommended as a future key to eliminating the genetic potential of escaped fish. The maintenance of robust populations of wild fish is recommended as a key to minimizing the effects of escaped fish on wild populations.     

Adaptive strategies and life history characteristics in a warming climate: Salmon in the Arctic?

In the warming Arctic, aquatic habitats are in flux and salmon are exploring their options. Adult Pacific salmon, including sockeye (Oncorhynchus nerka), coho (O. kisutch), Chinook (O. tshawytscha), pink (O. gorbuscha) and chum (O. keta) have been captured throughout the Arctic. Pink and chum salmon are the most common species found in the Arctic today. These species are less dependent on freshwater habitats as juveniles and grow quickly in marine habitats. Putative spawning populations are rare in the North American Arctic and limited to pink salmon in drainages north of Point Hope, Alaska, chum salmon spawning rivers draining to the northwestern Beaufort Sea, and small populations of chum and pink salmon in Canada’s Mackenzie River. Pacific salmon have colonized several large river basins draining to the Kara, Laptev and East Siberian seas in the Russian Arctic. These populations probably developed from hatchery supplementation efforts in the 1960’s. Hundreds of populations of Arctic Atlantic salmon (Salmo salar) are found in Russia, Norway and Finland. Atlantic salmon have extended their range eastward as far as the Kara Sea in central Russian. A small native population of Atlantic salmon is found in Canada’s Ungava Bay. The northern tip of Quebec seems to be an Atlantic salmon migration barrier for other North American stocks. Compatibility between life history requirements and ecological conditions are prerequisite for salmon colonizing Arctic habitats. Broad-scale predictive models of climate change in the Arctic give little information about feedback processes contributing to local conditions, especially in freshwater systems. This paper reviews the recent history of salmon in the Arctic and explores various patterns of climate change that may influence range expansions and future sustainability of salmon in Arctic habitats. A summary of the research needs that will allow informed expectation of further Arctic colonization by salmon is given.     

Mitochondrial DNA Restriction site polymorphism in Drosophila montana and drosophila virilis

Mitochondrial DNA fragment patterns produced by ten restriction endonucleases have been studied for three geographically diverse Drosophila montana lines and two Drosophila virilis lines. The two species are estimated to differ at about 6% of mitochondrial DNA nucleotide sites. In both cases intraspecific genetic variation is relatively small (pairs of lines are estimated to differ at about 0.6% of mitochondrial DNA nucleotide sites). It appears that Japanese and North American D. montana populations have not been separated for an extended period. In D. virilis there is evidence for intraspecific variation in the size of the mitochondrial genome.     

Mitochondrial DNA and allozyme analysis of Atlantic salmon, Salmo salar L., in England and Wales

Allozyme variation was examined in 429 Atlantic salmon, from seven sampling sites in England and Wales. Contingency tests for genetic homogeneity using three diagnostic loci revealed no significant differences among populations from the north-east and north-west of the U.K., but detected significant aspartate aminotransferase (AAT) differences between these samples and those from the R. Itchen in Hampshire (southern England). Mitochondrial DNA variation was analysed in 40 salmon from five spawning sites in the R. Itchen. Eight restriction endonucleases were used, of which three (AVAII, HAE III and HINFI) revealed polymorphisms. Six matriarchal lineages were discriminated. Two of the six mtDNA types observed were site-specific. These results suggest a reasonable expectation of discriminating spawning aggregations of Atlantic salmon.     

Chromosome polymorphisms track trans‐Atlantic divergence and secondary contact in Atlantic salmon

Pleistocene glaciations drove repeated range contractions and expansions shaping contemporary intraspecific diversity. Atlantic salmon (Salmo salar) in the western and eastern Atlantic diverged >600,000 years before present, with the two lineages isolated in different southern refugia during glacial maxima, driving trans‐Atlantic genomic and karyotypic divergence. Here, we investigate the genomic consequences of glacial isolation and trans‐Atlantic secondary contact using 108,870 single nucleotide polymorphisms genotyped in 80 North American and European populations. Throughout North America, we identified extensive interindividual variation and discrete linkage blocks within and between chromosomes with known trans‐Atlantic differences in rearrangements: Ssa01/Ssa23 translocation and Ssa08/Ssa29 fusion. Spatial genetic analyses suggest independence of rearrangements, with Ssa01/Ssa23 showing high European introgression (>50%) in northern populations indicative of post‐glacial trans‐Atlantic secondary contact, contrasting with low European ancestry genome‐wide (3%). Ssa08/Ssa29 showed greater intrapopulation diversity, suggesting a derived chromosome fusion polymorphism that evolved within North America. Evidence of potential selection on both genomic regions suggests that the adaptive role of rearrangements warrants further investigation in Atlantic salmon. Our study highlights how Pleistocene glaciations can influence large‐scale intraspecific variation in genomic architecture of northern species.     

LANDSCAPE GENOMICS IN ATLANTIC SALMON (SALMO SALAR): SEARCHING FOR GENE–ENVIRONMENT INTERACTIONS DRIVING LOCAL ADAPTATION

A growing number of studies are examining the factors driving historical and contemporary evolution in wild populations. By combining surveys of genomic variation with a comprehensive assessment of environmental parameters, such studies can increase our understanding of the genomic and geographical extent of local adaptation in wild populations. We used a large‐scale landscape genomics approach to examine adaptive and neutral differentiation across 54 North American populations of Atlantic salmon representing seven previously defined genetically distinct regional groups. Over 5500 genome‐wide single nucleotide polymorphisms were genotyped in 641 individuals and 28 bulk assays of 25 pooled individuals each. Genome scans, linkage map, and 49 environmental variables were combined to conduct an innovative landscape genomic analysis. Our results provide valuable insight into the links between environmental variation and both neutral and potentially adaptive genetic divergence. In particular, we identified markers potentially under divergent selection, as well as associated selective environmental factors and biological functions with the observed adaptive divergence. Multivariate landscape genetic analysis revealed strong associations of both genetic and environmental structures. We found an enrichment of growth‐related functions among outlier markers. Climate (temperature–precipitation) and geological characteristics were significantly associated with both potentially adaptive and neutral genetic divergence and should be considered as candidate loci involved in adaptation at the regional scale in Atlantic salmon. Hence, this study significantly contributes to the improvement of tools used in modern conservation and management schemes of Atlantic salmon wild populations.