The effect of natural selection on estimates of genetic divergence among populations of the Atlantic salmon

The effect of natural selection on the _mMEP-2 * locus on measures of genetic divergence among Atlantic salmon populations was investigated by examining the pattern of change in the level of genetic differentiation (F_ST) averaged over loci when data on the _mMEP-2 * locus were either included or excluded. The level of F_ST among populations at various geographic scales was estimated from allele frequencies at up to four loci (_s AAT-4 *, IDDH-1 *, IDHP-3 *, and _mMEP-2 *). At smaller geographic scales (within river systems or limited geographic regions) levels of variance in _mMEP-2 * allele frequencies were reduced relative to mean levels. At larger geographic scales (across continents or the species range) variation in _mMEP-2 * allele frequencies was greater than mean levels. These results suggest an a priori hypothesis for the effect of selection on the _mMEP-2 * locus which may be applied in future studies on variation in protein coding or other (e.g. mini- and microsatellite) loci in the Atlantic salmon. It is recommended that estimates of gene flow among populations of the Atlantic salmon based on mean F _ST estimates which include data on the _mMEP-2 * locus should be viewed with caution.     

Population structure of lake‐type and river‐type sockeye salmon in transboundary rivers of northern British Columbia

The population structure of 'lake‐type' and 'river‐type' sockeye salmon Oncorhynchus nerka , primarily in transboundary rivers in northern British Columbia, was examined with a survey of microsatellite variation. Variation at 14 microsatellite loci was surveyed from c . 3000 lake‐type and 3200 river‐type sockeye salmon from 47 populations in six river drainages in British Columbia. The mean F _ST for the 14 microsatellite loci and 47 populations was 0·068, and 0·034 over all river‐type populations. River‐type sockeye salmon were more genetically diverse than lake‐type sockeye salmon, with expected heterozygosity of river‐type sockeye salmon 0·72 and with an average 12·7 alleles observed per locus, whereas expected heterozygosity of lake‐type sockeye salmon was 0·65 with and average 10·5 alleles observed per locus. River drainage of origin was a significant unit of population structure. There was clear evidence of genetic differentiation among river‐type populations of sockeye salmon from different drainages over a broad geographic range in British Columbia.     

Selective exploitation of early running fish may induce genetic and phenotypic changes in Atlantic salmon

Genetic evidence for the selective exploitation by anglers of early running fish was examined in four Iberian Atlantic salmon populations using protein and mtDNA markers. The populations studied had been exploited exclusively by anglers since 1949 during a fixed fishing season that ran approximately from March to July. Genetic variation at six protein loci was small and was accounted for by the MEP‐2 * and MDH‐3,4 * polymorphisms, which generally remained stable over time and were in Castle–Hardy–Weinberg equilibrium during the fishing season. Early running fish that had spent multiple winters at sea (MSW) generally had higher frequencies of the common MEP‐2 *(100) allele than did late running, one sea winter (1SW) grilse that were significantly smaller and tended to escape the fishery. Spawners differed from angler caught fish in their mtDNA frequencies and consistently had a lower sea‐age and a smaller body size. Spawners also smolted at an older age and displayed lower frequencies of the MEP‐2 *(100) allele in three of the four populations studied. These results suggest that in these rivers anglers selectively exploit a distinct component of the population and inadvertently cause a differential mortality of genetic types that is likely to be detrimental to population viability.     

Genetic studies on serum transferrins in Atlantic salmon

Published and unpublished data on genetic variation at the transferrin locus ( TF *) in Atlantic salmon from rivers in eastern North America sampled from 1968 to 1970 were reanalysed and compared with data for samples collected in 1998 from nine of the same rivers. Genetic differentiation among rivers was highly significant as was spatial differentiation among tributary samples within the Miramichi River system, the largest rivers studied. Comparison of allele frequencies in rivers also sampled in 1998 show no overall evidence of significant genetic change after 30 years, spanning 9 generations. The results strongly support the stability of the patterns of spatial genetic differentiation and support the occurrence in Atlantic salmon of reproductive isolation among rivers and among tributaries within large river systems.     

Evidence for co‐dominant allelic expression of a phosphoglucomutase regulatory locus polymorphism in the Atlantic salmon

Starch gel electrophoresis of the phosphoglucomutase isozyme, PGM‐1, in liver tissue in Atlantic salmon Salmo salar shows three phenotypes – full, partial and no expression. The genetic basis of the variation has not been established. Studies of the inheritance of the variation and of liver enzyme levels carried out indicate that the variation, as in rainbow trout Onchorynchus mykiss , reflects co‐dominant allelic variation at a cis ‐acting regulatory locus, designated PGM‐1r *, with one allele promoting and the other suppressing expression.     

The existence of two races of Atlantic salmon (Salmo salar L.) in the British Isles

Sera from approximately 10 000 Atlantic salmon collected from rivers in the British Isles have been analysed. Polymorphism at the transferrin locus was observed and the distribution of the transferrin alleles provides further evidence supporting the presence of two races of salmon first postulated by Payne et al. (1971 a ).     

Habitat selection by juvenile Atlantic salmon: the interaction between physical habitat and abundance

The effect of physical river habitat variables on the distribution of juvenile Atlantic salmon Salmo salar L. in the Rivière de la Trinité, Québec, Canada, was examined using generalized additive modelling. A survey of Atlantic salmon fry and parr densities and habitat variables (flow velocity, water column depth and substratum size) was conducted in the summer months from 1984 to 1992. Clear patterns of habitat use existed: specific ranges of habitat variables were selected, with parr preferring greater velocities, depths and substratum sizes than fry. There was a large variation, however, in juvenile densities for given velocities, depths or substratum sizes, with this variation being greatest in optimal habitats. On examination of an individual year, interaction between the variables was found to explain some of the variation. On a year‐to‐year basis the juvenile Atlantic salmon population was found to exhibit an 'Ideal Free Distribution', which resulted in greatest variation in optimal habitats with year‐to‐year changes in population abundance.     

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.     

Stocking‐related patterns of genetic variation at enzymatic loci in south European Atlantic salmon populations

Genetic variation at 24 enzymatic loci was investigated in eight south European Atlantic salmon populations from the rivers Nivelle, Cares, Sella, Narcea, Esva, Navia, Porcia and Eo. In these rivers, management based on supplementation of native populations with foreign stocks was carried out for more than one decade. Population genetic patterns expressed in terms of allele frequencies, mean heterozygosity and conformity to Hardy‐Weinberg equilibrium, were significantly different between populations. Relevant temporal changes of genetic variability were reported. Evidence that foreign stocking has disturbed the genetic patterns of some of the studied populations is presented.     

Genetic analysis of fish genomes and populations: allozyme variation within and among Atlantic salmon from Downeast rivers of Maine

Analysis of genetic variation within and among samples of naturally produced Atlantic salmon ( n  = 372) from 7 Maine (U.S.A.) and one Canadian river were conducted based on 54 allozyme loci. Eight of the 54 loci proved polymorphic, and estimated heterozygosities ( H _S) based on all loci ranged from 0·012 to 0·026 (mean = 0·021, s . e . = 0·002). Only one of 56 tests revealed genotypic proportions that deviated significantly from Hardy–Weinberg expectations. Genetic distances ( D ) between samples ranged from 0·002 to 0·022. No obvious association existed between genetic and geographic distances. Cluster analysis of genetic distances revealed the Dennys River sample as the most differentiated when all samples were included in the analysis, though bootstrap support of the cluster analysis was generally weak. G ‐tests revealed significant differences in allele frequencies among samples at five of the polymorphic loci, and the G ‐value summed over all loci also indicated significant differences among samples. F _ST values indicated that 3·4% of the total genetic diversity was due to variability among samples, while 96·6% was due to variability within samples. These results indicate that the Atlantic salmon analyzed in this study had levels of genetic variability and differentiation among samples comparable to native populations from other areas collected across a similar geographic range.     

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.     

Natural selection acts on Atlantic salmon major histocompatibility (MH) variability in the wild

Pathogen-driven balancing selection is thought to maintain polymorphism in major histocompatibility (MH) genes. However, there have been few empirical demonstrations of selection acting on MH loci in natural populations. To determine whether natural selection on MH genes has fitness consequences for wild Atlantic salmon in natural conditions, we compared observed genotype frequencies of Atlantic salmon (Salmo salar) surviving in a river six months after their introduction as eggs with frequencies expected from parental crosses. We found significant differences between expected and observed genotype frequencies at the MH class II alpha locus, but not at a MH class I-linked microsatellite or at seven non-MH-linked microsatellite loci. We therefore conclude that selection at the MH class II alpha locus was a result of disease-mediated natural selection, rather than any demographic event. We also show that survival was associated with additive allelic effects at the MH class II alpha locus. Our results have implications for both the conservation of wild salmon stocks and the management of disease in hatchery fish. We conclude that natural or hatchery populations have the best chance of dealing with episodic and variable disease challenges if MH genetic variation is preserved both within and among populations.     

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.     

Discriminating coho salmon (Oncorhynchus kisutch) populations within the Fraser River, British Columbia, using microsatellite DNA markers

Three microsatellite loci were used to examine genetic variation among 16 coho salmon ( Oncorhynchus kisutch ) populations within the Fraser River drainage system, in British Columbia, Canada. Each locus was highly polymorphic with 30 alleles at the Ots 101 locus, 15 alleles at the Ots 3 locus and 38 alleles at the Ots 103 locus. Average observed heterozygosities were 86.1%, 70%, and 56.1%, respectively. With the exception of the Dunn and Lemieux River populations, Chi-square tests and F _ST values indicated that all populations had significantly different allele frequencies. Two distinct population groups within the Fraser River drainage were observed. Lower Fraser River populations were strongly differentiated from populations spawning in the upper Fraser River, which includes the Thompson River (a tributary flowing into the upper Fraser) and the portion of the Fraser River beyond the precipitous Fraser River canyon. This regional population structure may have resulted from colonization of the upper and lower Fraser River regions by different founder populations following Pleistocene glaciation, and be maintained by adaptive differences between the two groups of coho salmon. Coho salmon populations in the upper Fraser and Thompson River drainages form an evolutionarily significant unit (ESU) of importance for conservation of biodiversity in coho salmon. Microsatellite DNA loci show promise as technically simple and highly informative genetic markers for coho salmon population management.     

Genetic evidence for lacustrine spawning of the non‐anadromous Atlantic salmon population of Little Gull Lake, Newfoundland

Allozyme markers were used to investigate the spatial boundaries of the non‐anadromous Atlantic salmon population of Little Gull Lake, Eastern Canada. Mixed year class samples of juvenile salmon were analysed from inlet streams, upstream lakes, the outlet river and sites downstream. No evidence was found that individuals from the Lake's non‐anadromous population were present in these samples, strongly suggesting that the non‐anadromous population is confined to the lake and has a lacustrine spawning habit.     

Genetic structure of freshwater Atlantic salmon (<Emphasis Type="Italic">Salmo salar</Emphasis> L.) populations from the lakes Onega and Ladoga of northwest Russia and implications for conservation

Freshwater Atlantic salmon (Salmo salar L.) populations are a living example of adaptation to the changing conditions caused by glacial cycles. The uniqueness of these populations is emphasized by almost complete resistance to the dangerous parasite Gyrodactylus salaris. In Europe, freshwater salmon populations occur primarily in north-western Russia in the republic of Karelia. These systems include Lakes Ladoga and Onega, the two largest lakes in Europe, each of which harbours a number of freshwater salmon spawning rivers. We used microsatellite markers to study the genetic structure and temporal stability of 11 freshwater salmon populations in Russian Karelia. Populations clustered according their region of origin. Although temporal variation in allele frequencies was observed in the majority of temporal comparisons, various lines of evidence demonstrated that this influence was relatively minor compared to spatial variation that explained eight times more of the variability than temporal variation. Temporal stability tended to occur in populations from rivers with a higher linear lake coefficient. The high level of genetic structuring observed in both lake systems and the apparent low level of migration between populations suggests that treating each river as a separate management unit is recommended. In addition, as the number of populations is large, the best strategy for such fine scale management would be to ensure that the level of natural reproduction in each river is sufficient to sustain the population. A prioritization strategy for population conservation based on estimating the relative roles of different evolutionary forces shaping the gene pools highlighted a number of populations where further monitoring is warranted and also identified populations which could be prioritized for conservation as living gene banks in the event that conservation resources are limited. This prioritization agreed well with the occurrence of temporal (in)stability.     

Genetic variation in Atlantic salmon, Salmo salar L., within the Tamar catchment in south-west England

Electrophoretic analysis of enzymes in 383 juvenile Atlantic salmon, Salmo salar L., within the Tamar catchment (south-west England) revealed significant genetic differences at the IDHP-3* locus between the three tributaries studied. Aspects of temporal and spatial variation, and management policy within catchments, are discussed.     

Return migration of one‐sea‐winter Atlantic salmon in the River Tana

Fifty‐three one‐sea‐winter Atlantic salmon Salmo salar (45–63 cm L _T) were radio‐tagged in the Tana fjord, Barents Sea, in 1995. Thirty‐seven fish (70%) entered the freshwater zone of the River Tana in an average of 3 days after release in the fjord. The migration speeds in the lowest river section below the first riffle area were significantly higher than in the subsequent river section below the second riffle area. Similarly, the observed time spent in the first riffle area was significantly lower than in the next riffle area. The majority of Atlantic salmon entered the river during the hours of high tide and the subsequent ebb tide. In addition, most river entries were recorded around midnight. No effects of river flow on the river entry or migration speed were detected, but the migration speed of Atlantic salmon in both river sections examined was greater at lower temperatures. Twenty‐eight fish (72%) were recaptured in the river, 71% of them with weirs and gillnets, and 29% by rod and line. Over half of the Atlantic salmon (54%) were recaptured within 3 weeks following river entry, and within the first 100 km of the river (56%). The results are discussed in relation to earlier studies on multi‐sea‐winter Atlantic salmon in the River Tana.     

Determination of body shape variation in Irish hatchery‐reared and wild Atlantic salmon

Discriminant function analysis was used to distinguish morphologically between samples of parr, smolts and adult Atlantic salmon Salmo salar from several hatchery and river systems in Ireland. The effect of habitat shift was investigated in Atlantic salmon parr. Parr grown from the eyed‐egg stage with a non‐sibling group in a hatchery environment, came to resemble the mean body shape of their host hatchery Atlantic salmon stock more closely than that of a full sibling group grown at their natal hatchery. Wild Atlantic salmon smolts differed in shape from hatchery‐reared smolts. This difference was less pronounced, but still statistically significant when wild adults were compared with hatchery‐reared adults captured in the coastal drift‐net fishery after a year spent at sea. Rearing conditions had a significant impact on the production and growth of fish body shape. This in turn may have affected adaptability and survivorship of ranched Atlantic salmon in the marine environment.     

Genetic comparison of salmon from the White Sea and north-western Atlantic Ocean

Samples of salmon Salmo salar from the River Kachkovka and the River Nilma in northern Russia were analysed by starch gel electrophoresis and compared to three Norwegian stocks, the Neiden river in northern Norway and Øyreselv and Hopselv rivers on the west coast. The comparison included the following polymorphic loci: AAT-4 *, IDDH-2 *, IDHP-3 *, MDH- 3,4 *, MEP-2 *, ESTD * as well as the newly discovered polymorphic loci FBALD-3 * and TPI-3 *. Samples were run side by side on gels, and the alleles found in the Russian stocks were the same as those found in the Norwegian stocks, although the electrophoretic methods used lead to differences in designations of alleles. A polymorphism in ESTD * which involves a slow allele was commonly observed in the three northern populations of the Nilma, Kachkovka and Neiden rivers. This allele was absent in the other Norwegian stocks and in a major brood stock of farmed salmon in Norway. The IDHP-3 * 116 allele was found in unusually high frequencies in the northern populations. Thus, the variability observed at these two loci indicates a barrier to gene flow between the northern salmon stocks and the more southern stocks in the East Atlantic area.