Microsatellite analysis in domesticated and wild Atlantic salmon (Salmo salar L.): allelic diversity and identification of individuals

Samples of wild and domesticated salmon in Norway were genotyped at 12 microsatellite loci to compare allelic variability and investigate the potential of microsatellite markers for identification of individuals. The following loci were amplified: Ssa20, Ssa62NVH, Ssa71NVH, Ssa90NVH, Ssa103NVH, Ssa105NVH, SsaF43; Ssa20.19; Ssa13.37; SsOSL85; Ssa197; Ssa28. All domesticated strain samples displayed reduced variability compared to wild salmon. On average 58% of the allelic richness observed within the four wild stocks were present in the samples taken from domesticated strains. No systematic differences in heterozygosity were observed between samples representing the two groups.

Pairwise genetic distances, as estimated by Fst values and Nei [1978] was 2–8 times higher among domesticated strains than among wild strains. Among the wild stocks, the highest genetic distances were observed between the river Neiden, located in northern Norway, and the other wild stocks located in the southwest of Norway.

Assignment tests indicated that the wild and domesticated salmon could be distinguished with high precision. Less than 4% of domesticated salmon were misassigned as wild salmon, and less than 3% of wild fish were misassigned as domesticated salmon. Fish from individual domesticated strains were identified with similarly high precision. Assignment to wild salmon stocks was less accurate, with the exception of the sample taken from the river Neiden, for which 93% of the individuals were correctly assigned.     

Maintenance of genetic variation in hatchery stocks of Atlantic salmon, Salmo salar L.: experiences from the River Bush, Northern Ireland

Abstract. An examination of biochemical-genetic variation at seven polymorphic loci was carried out among five year classes of wild Atlantic salmon, Salar L., in the R. Bush and in a hatchery strain derived from the wild population. Within some of the year classes, gene frequencies at several loci differed significantly between wild and artificially reared salmon. Highly significant temporal variation in gene frequencies was detected among successive year classes of the hatchery strain, while this was less significant among the wild salmon. Samples of wild salmon taken as 0+ and 1 + parr in the river showed no significant temporal variability in allelic frequencies. Heterozygosity levels among the wild and hatchery-reared salmon were comparable, averaging 0·185 and 0·176 respectively. The genetic variability of the artificially reared salmon is discussed in relation to numbers of broodstock and breeding regime used at the hatchery.     

Microsatellite variation reveals fine-scale genetic structure of masu salmon, Oncorhynchus masou, within the Atsuta River

Abstract –  To describe in detail the population genetic structure of masu salmon Oncorhynchus masou , seven anadromous populations in the Atsuta River were investigated by analysis of eight polymorphic microsatellite loci. Exact test and genetic differentiation ( F _ST) revealed that significant differentiation was observed at the within-river scale. Principal components analysis revealed that the spatial pattern of genetic composition was related to geographical location of each population. Furthermore, a significant correlation was observed between genetic differentiation and geographical distance, indicating that dispersal is less likely to occur between distant populations. The results of this study imply that masu salmon have potential to show clear genetic structure at the microgeographical scale (21 km) due to precise homing behaviour.     

Microsatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations

Genetic diversity between three farmed and four wild populations of Atlantic salmon from Ireland and Norway were analysed using 15 microsatellite markers. High levels of polymorphism were observed over all populations with the average number of alleles and average heterozygosity at 17.8 and 0.70, respectively. Farmed salmon showed less genetic variability than wild salmon in terms of allelic diversity but not necessarily in terms of overall heterozygosity. Between farmed populations significant differences were observed in expected heterozygosity suggesting that more intensive breeding practices may have resulted in a further erosion of genetic variability. Phylogenetic analysis using either populations or individuals as nodes show a clustering of populations into two groups, farmed and wild. This suggests that founder effects and subsequent selection have had more effect on the genetic differentiation between these strains than geographical separation. This technology has great potential for use in aquaculture situation where levels of genetic variation could be monitored and inbreeding controlled in a commercial breeding progra.     

Identification of differential broodstock contribution affecting genetic variability in hatchery stocks of Atlantic salmon (Salmo salar)

Supportive breeding of Atlantic salmon (Salmo salar) is commonly employed to maintain numbers of fish where the species has become locally endangered. Increasingly, one of the main aims of population management is the preservation of natural genetic diversity. If the stocks employed in supportive breeding exhibit reduced variation they can alter the natural pattern of genetic variation observed in wild populations. In northern Spain, wild adult salmon are caught every year from local rivers and artificially crossed in order to create supportive stocks. The offspring are hatchery reared until the juvenile stage, then released into the same river where their parents were caught. In the current study, our findings demonstrate that although adult broodstock exhibit a pattern of variation similar to the wild populations, variability at microsatellite loci was drastically reduced in the juveniles released into one of three rivers analyzed. The contribution of broodstock to this juvenile stock was examined by pedigree analysis. A restricted number of females contributing to the hatchery stock was identified as the main cause of loss in genetic variation, possibly due to overmaturity of some multi-sea-winter females. We suggest that better monitoring and control of parental contribution will help in solving the problem of loss of genetic diversity in hatchery populations.     

Incidence of hybridization between Atlantic salmon, Salmo salar L., and brown trout, Salmo trutta L., in Ireland

The substantial growth of the farmed salmon industry in Europe since the 1970s has highlighted concerns regarding the genetic impact of escaped farmed salmon on wild salmonid stocks. High incidences of salmon × trout hybrids have been recorded in rivers situated near intensive salmon farming in Norway and Scotland, which may be indicative of a breakdown in reproductive isolation between salmon, Salmo salar L., and brown trout, Salmo trutta L. In the present study, salmonid fry and 0+ parr were collected from rivers in western Ireland. Allozyme and minisatellite DNA analysis were carried out on fry to determine the frequency of F1 hybrids from 10 rivers located within 38 km of salmon farms and three rivers at least 80 km from salmon farms. A total of 49 hybrids were recorded from 4135 salmonid fry (frequency = 1.2%). Mitochondrial DNA analysis showed that all hybrids arose from Atlantic salmon female × brown trout male crosses. Hybrid parr were recorded from one of the low-risk rivers (1.0%), but were present in seven out of the 10 catchments located within 38 km of salmon farms, with frequencies ranging from 0.7% to 3.1%. The results of the present survey, which represents the first extensive record of the levels of salmon-trout hybridization in Ireland, are discussed in relation to the continued growth of salmon farming in this country.     

Population genetic structure of Atlantic salmon,Salmo salar L., in the River Tamar,southwest England

Abstract Population genetic studies can be useful for informing conservation and management. In Atlantic salmon, Salmo salar L., population structuring frequently occurs between river systems, but contrasting patterns occur within rivers, highlighting the need for catchment‐specific studies to inform management. Here, population structure of Atlantic salmon was examined in the River Tamar, United Kingdom, using 12 microsatellite loci. Gene diversity and allelic richness ranged from 0.80 to 0.84 and from 8.96 to 10.24, respectively. Some evidence of genetic structure was found, including significant genetic differentiation between samples in different subcatchments (pairwise θ and tests of genic differentiation), results from assignment tests and a pattern of isolation by distance. Conversely, structure revealed only one population cluster, and an analysis of molecular variance showed no significant variation between subcatchments. Evidence of population bottlenecks depended on the mutation model assumed and is discussed with reference to catchment‐specific studies of stock abundance. Implications for implementing management actions are considered.     

Reproductive strategies in small populations: using Atlantic salmon as a case study

Abstract –  Wild salmonid populations with only a few breeding adults may not exhibit a significant reduction in genetic variability compared with larger populations. Such an observation suggests that effective population sizes are larger than population size estimates based on direct adult counts and/or the mating strategy maximises outbreeding, contributing to increased heterozygosity. In the case of wild Atlantic salmon Salmo salar populations, stratification by age classes and sexes on the spawning grounds avoids inbreeding and increases genetic variability. We studied the breeding composition of four Spanish salmon populations. Over a 7-year period we concluded that the probability of within-cohort mating is very low: females generally reproduce after two sea-winters whereas males reproduce mostly as one sea-winter ( grilse ) and/or mature parr. Considering different levels of contribution of mature parr to spawning derived from field surveys, we developed a simple model for estimating effective population sizes and found that they doubled with 65% parr contribution expected for rivers at this latitude (43°N), and ranged from 100–800 individuals. The effect of between-cohort mating was modelled considering different ranges of differences in allele frequencies between cohorts and resulted in 28–50% increases in heterozygosity when considering a 65% parr contribution. The complex mating strategy of Atlantic salmon contributes to explain the high levels of genetic variability found for small populations of this species. This model can probably be extended to other animal species with mating strategies involving different cohorts.     

Long-term changes in the sea-age at maturity and seasonal time of return of salmon, Salmo salar L., to Scottish rivers

Abstract Using catch data, changes in salmon, Salmo salar L., sea-age and seasonal return time were compared between several Scottish east coast rivers over the last 150–200 years. Parallel long-term trends were found, suggesting common influences affecting salmon at sea. Long-term associations with marine environmental factors were investigated by literature review and comparisons with an index of Icelandic sea-ice abundance. Apparent associations were shown to exist since about 1900, although the cause was not demonstrated. However, over a longer timescale, the same associations were not apparent. Unique gradual marine changes since 1900 may have resulted in perceptible associations with salmon data which may otherwise be imperceptible when short-term marine environmental variability is greater than long-term variability. Marine factors must affect salmon, but the complexity of the marine environment and controls on age at maturity and time of return mean that a retrospective analysis cannot be expected to identify the causal factors.     

Distribution and population genetic structure of river- and sea-type sockeye salmon in western North America

Abstract– In contrast to the well-known "lake-type" sockeye salmon, two additional anadromous life-history types have been recognized within the species: 'river-type' sockeye salmon whose juveniles spend 1 or 2 years in off-channel river habitats prior to migrating to sea, and "sea-type" sockeye salmon that initially rear in similar river habitats yet migrate to sea as underyearlings. Persistent populations of river-/sea-type sockeye salmon occur in small numbers throughout the species'range in North America but are usually associated with glacier-fed rivers. We found published and unpublished records showing that riverine-spawning sockeye salmon occur in 11 rivers in western Washington, USA, that don't have access to juvenile lake-rearing habitat. Evidence of persistent spawning was strongest for the Nooksack and Skagit rivers in northern Puget Sound. We analyzed allozyme frequency differentiation in 26 laketype and 12 river-/sea-type populations of sockeye salmon in North America, ranging from northern Puget Sound, Washington (including 3 in the Nooksack and Skagit rivers) to northern Southeast Alaska. Across this 2000 km range, river-/sea-type sockeye salmon showed very little genetic differentiation between populations, much less than that displayed by the highly divergent lake-type sockeye salmon. Genetic similarity among river-/sea-type sockeye salmon in this study is likely a result of common ancestry and a high level of historical gene flow among river-/sea-type sockeye salmon populations.     

Genetic diversity in a Tasmanian hatchery population of Atlantic salmon (Salmo salar L.) compared with its Canadian progenitor population

The level of genetic diversity in a cultured Atlantic salmon (Salmo salar) population from Tasmania, Australia was examined at 11 microsatellite loci and compared with that in its progenitor population from the River Philip in Nova Scotia, Canada. The reference progenitor population consisted of archived scales collected from wild River Philip salmon in 1971 and 1972, not long after salmon from this river were imported into Australia in the mid‐1960s. The Tasmanian hatchery stock had a significant reduction in the mean number of alleles (31–43%) and mean allelic richness (28–39%) across all microsatellite loci compared with the wild Canadian population. Mean heterozygosity levels remained unchanged. Estimates of per‐generation effective population sizes for the Tasmanian population, based on allele frequency temporal variance with the wild progenitor population, ranged from 102–207 individuals and reflected hatchery records.     

Possible use of taxonomic characters to identify Newfoundland and Scottish stocks of Atlantic salmon, Salmo salar L.

Abstract. Based on a pooled sample of 367 specimens of juvenile Atlanlic salmon, Salmo salar L., from eight geographically distinct home rivers, stocks from Scotland and Newfoundland can be distinguished by meristic and morphometric character sets using discriminant analysis procedures. Reduced character sets require meristic counts of pectoral fin rays, dorsal fin rays, gill rakers and vertebrae, and morphometric measurements of standard length, pectoral and pelvic fin lengths, body depth and gape width. Regional differences based on these morphometric and meristic sets are substantiated by monomorphism at each MDH locus in Scottish fish in contrast to polymorphism at the MDH-1 and MDH-3 loci in Newfoundland fish. Only the morphometric discriminant function is highly accurate (>80%) in identifying home river origins of the fish examined with the discriminating power increasing with increased fish size. These findings for juvenile fish indicate that, while meristic, morphometric and electrophoretic criteria provide a likely means for distinguishing regional fish stocks, morphometric character sets would seem to offer the best possibility for identifying home river origins of adult Atlantic salmon in mixed fisheries.     

Occurrence of canthaxanthin in Atlantic salmon, Salmo salar L., fry in Irish rivers as an indicator of escaped farmed salmon

The rapid growth of Atlantic salmon, Salmo salar L., culture in north-western Europe has given rise to concerns regarding the biological consequences of fish farm escapes on wild salmonid populations. Canthaxanthin, a carotenoid pigment additive to farmed salmon feed which is passed from females to their progeny, may be used as an indicator of the numbers of escaped farmed salmon which spawn in the wild. In the present study, thin-layer chromatography and high-performance liquid chromatography (HPLC) were used to screen emergent Atlantic salmon fry sampled from seven river catchments in Ireland for canthaxanthin. The incidence of fry containing canthaxanthin at greater than trace levels (<5% of total carotenoid pigment) was 0–4%, with an average of 1.7%, among the seven rivers sampled, indicating that the progeny of farmed salmon were present at similarly low frequencies. Canthaxanthin was detected at trace levels in an unexpectedly high proportion (35%) of salmon fry. Canthaxanthin was present at levels exceeding trace amounts in 24% of 21 non-anadromous brown trout, Salmo trutta L., sampled from six Irish rivers and present at trace levels in a further 57% of the fish, indicating that dietary canthaxanthin is freely available to salmonids in Irish rivers. The widespread presence of trace levels in salmon fry may be attributable, at least in part, to the increased sensitivity of the HPLC methods and to rapid dietary uptake during early post-emergence feeding.     

Patterns of phenotypic and genetic variability show hidden diversity in Scottish Arctic charr

Abstract –  This study examined the degree and pattern of variability in trophic morphology in Arctic charr ( Salvelinus alpinus L. ) at three spatial scales: across 22 populations from Scotland and between and within two adjacent catchments (Laxford and Shin) in northern Scotland. In addition, the variability at six microsatellite loci between and within the Laxford and Shin systems was determined. Habitat use by charr differed significantly between populations. The pattern of variability in trophic morphology, known to influence foraging ability in charr, showed a very high degree of between-population variation with at least 52% of population pairs showing significant differences in head shape. Trophic morphology and genetic variation was also high over small geographical scales; variation being as high between charr from lakes within the same catchment, as between adjacent catchments. The pattern of both phenotypic and genotypic variation suggests a mosaic of variation across populations with geographically close populations often as distinct from each other as populations with much greater separation. Very low levels of effective migrants between populations, even within the same catchment, suggest that this variation is being maintained by very low straying rates between phenotypically and genetically distinct populations, even when there is no apparent barrier to movement. We conclude that the genetic and phenotypic integrity of charr populations across Scotland is high and that this adaptive radiation constitutes a 'hidden' element of diversity in northern freshwater systems. Two consequences of this are that the population (rather than the species) makes a more rational unit for the consideration of conservation strategies and that the habitat requirements and therefore management needs may differ significantly between populations.     

Variation in the population density of adult sea-trout, Salmo trutta, in 67 rivers in England and Wales

Abstract– Analysis of annual rod and commercial catches of adult seatrout demonstrated strong positive relationships between large-scale spatial variance (S²_s, variation in catches between rivers for each year) and spatial mean density (x?_s, mean catch per year), and also between temporal variance (S²_t, variation in catches between years for each river) and temporal mean density (x?_t, mean catch for each river). Both relationships were described by a power function, s²=ax^-b. For spatial variability, there were no significant differences between power functions for both rod and commercial catches from the North West, Welsh and South West regions. As the power b was not significantly different from two, relative spatial variability (measured by coefficients of variation (CV)) was fairly constant between years. Significantly higher values of b were obtained for the Wessex (GM b= 2.233) and North East (GM b=2.824) regions, and therefore the increase in CV with mean annual catch was significant but slight for Wessex rivers and marked for North East rivers. For temporal variability, there were no significant differences between power functions for both rod and commercial catches from all 5 regions and therefore a common power function was fitted to the data from all 67 rivers. As the power b was significantly less than two (GM b= 1.729), relative temporal variability (measured by CV) decreased significantly with increasing mean catch per river. Some limitations and implications of this analysis are discussed. Similar results from different regions for both rod and commercial catches suggest that such data do reflect adult population density, in spite of the different methods used to catch the sea-trout, variations in fishing effort and failures to report catches. The analysis of temporal variability provides a basis for classifying the major sea-trout rivers according to their mean annual catch and their relative variability in catches between years (using the CV).     

Inter-river, -annual and -seasonal variability in fecundity of Atlantic salmon, Salmo salar L., in rivers in Newfoundland and Labrador, Canada

Abstract  Fecundity is an integral component of the calculation of Atlantic salmon, Salmo salar L., egg depositions in rivers. Fecundity determinations can be time consuming and prohibitively expensive in terms of application on a broad scale. Consequently, where river specific and annual data are not available, default means are used in calculations in Newfoundland and Labrador. It is important therefore to know the extent of variability among rivers, years and seasons and the potential error involved in using default values. Annual fecundity data were available for one river in Labrador and nine rivers in Newfoundland. Fecundity was determined from ovaries collected in the recreational fishery in the summer for all 10 rivers. For three of these rivers, fecundity determined from summer sampling was compared with that obtained from sampling at time of spawning in autumn. There was significant variability in fecundity with length as a covariate among rivers, years and seasons. Mean number of eggs per female decreased between 8.3% and 29.0% from summer to autumn while mean number of eggs per cm decreased from 5.0% to 28.5%. Depending on the measure of relative fecundity used (no. of eggs kg⁻¹ or no. of eggs cm⁻¹), results of simulations showed that estimates of egg deposition incorporating defaults can deviate from those obtained by applying year-specific and river-specific values by 50–75%, without adjusting for the seasonal reduction in fecundity, and by 30–50% with an adjustment. A sensitivity analysis revealed that of three parameters used in the calculation of egg deposition (size, percent female and fecundity), fecundity was the most influential.     

Population structure and stock identification of chum salmon Oncorhynchus keta from Japan determined by microsatellite DNA variation

Variation at 14 microsatellite loci was surveyed in 26 chum salmon Oncorhynchus keta populations from Japan, one population from West Kamchatka and three populations from North America to determine population structure. Microsatellites were then applied to estimate stock composition of chum salmon in mixed-stock fisheries. The genetic differentiation index (F _st) over all populations and loci was 0.031, with individual locus values ranging from 0.010 to 0.081. Seven regional populations were observed in Japanese chum salmon, with late-run populations from the Pacific Coast of Honshu the most distinct. Japanese populations displayed greater genetic diversity than did those in North America. Transplantation history in some Japanese river populations influenced their present genetic characteristics. Analysis of simulated mixtures from fishery sampling suggested that accurate and precise regional estimates of stock composition should be produced when the microsatellites were used to estimate stock compositions. Stock compositions for a 2005 sample of maturing, migrating chum salmon off the north-west coast of Hokkaido near the border of the Sea of Japan and the Sea of Okhotsk indicated that this region may be a migration corridor for Hokkaido populations from the Sea of Japan coast. Microsatellites have the ability to provide fine-scale resolution of stock composition in Japanese coastal fisheries.     

Regional variability in Atlantic salmon (Salmo salar) riverscapes: a simple landscape ecology model explaining the large variability in size of salmon runs across Gaspé watersheds,Canada

Kim M, Lapointe M. Regional variability in Atlantic salmon (Salmo salar) riverscapes: a simple landscape ecology model explaining the large variability in size of salmon runs across Gaspé watersheds, Canada.
Ecology of Freshwater Fish 2011: 20: 144–156. © 2010 John Wiley & Sons A/S Abstract – Atlantic salmon (Salmo salar) rivers in the Gaspé Peninsula, Quebec, present a 20 to 1 variability in the average numbers of returning adult salmon per km² of watershed area (the ‘specific run size’). These variations are very poorly explained by interbasin differences in total stream length (R² = 0.033, P = 0.533) or in estimates of total area of salmon habitat that fail to take into account complementarity and interconnections across life stage habitats (R² = 0.065, P = 0.448). The relative spatial distribution of three complementary habitat types (adult holding pools, spawning beds, parr habitats) is hypothesised to be an important factor controlling the production of salmon at any given watershed area or given total stream length, and by extension the numbers of adults returning each year to spawn. We developed a simple riverine landscape ecology (or riverscape) model that uses easily accessible topographic map sources to identify optimally productive river segments. These segments were identified based on large‐scale river and valley features and the associated spatial organisation of complementary salmon habitats. We tested the ability of this model to predict salmon run sizes for 14 watersheds in the Gaspé Peninsula. The aggregate length of optimally productive segments, as defined in our model, is a strong predictor of the average size of the annual salmon runs for these watersheds (R² = 0.913, P < 0.0005). Furthermore, specific salmon run sizes were accurately predicted (R² = 0.771, P < 0.0005) after removal of the obvious scale effects of watershed size.     

A genetic comparison of sympatric anadromous and resident Atlantic salmon

Many studies have identified the importance of local adaptation in Atlantic salmon (Salmo salar) and the strong genetic differences that exist between allopatric or parapatric resident and anadromous populations. However, as truly sympatric migratory phenotypes of Atlantic salmon have not been studied, it remains unclear whether distinct genotypes previously associated with life history differences are maintained through reproductive isolation and subsequent genetic drift or through natural selection induced by different life history requirements. In this study, sympatric anadromous and resident Atlantic salmon were sampled from three Newfoundland (Canada) watersheds to evaluate the genetic divergence of these life history forms. Eight microsatellite loci were used to quantify genetic variation within and among populations. Metrics of genetic differentiation (exact tests for population differentiation, pairwise θ values) provide no evidence of genetic differentiation between some sympatric anadromous and resident phenotypes within a system with no history of segregation. In the remaining two watersheds, the observed differentiation appears to be a consequence of historical segregation rather than life history form. Nonetheless, these differences have been maintained in contemporary times for several generations. At broader spatial scales, resident salmon were more genetically divergent from one another than anadromous life history forms and were more closely related to anadromous salmon from within their watershed than to resident salmon from other watersheds. The study indicates that both life history forms can be maintained within a single population, but that sympatric populations of different life histories can maintain genetic differences for at least several generations after being reconnected.     

Evolution of introduced Chinook salmon (Oncorhynchus tshawytscha) in Lake Huron: emergence of population genetic structure in less than 10 generations

Abstract – Population genetic structure was detected in Chinook salmon Oncorhynchus tshawytscha in their non‐native range of Lake Huron using microsatellite DNA. All Chinook salmon in this system descend from Green River, Washington cohorts, originally transplanted to Michigan hatcheries in the late 1960s. We tested for population genetic differentiation of age 0 fish collected from 13 rivers and two hatcheries in 2007. The amount of genetic differentiation among collection sites was low but statistically significant, with F_ST values ranging from 0.036 to 0.133 and R_ST values ranging from 0.008 to 0.157 for specific loci. Based on pairwise F_ST and R_ST values and Bayesian cluster analysis, the Maitland River population in the Main Basin of Lake Huron was genetically distinct from the remaining collection sites. Based on analysis of bycatch data from commercial gill net fisheries, Chinook salmon likely colonised the Main Basin by 1975 (10 generations ago) and the North Channel and southern Georgian Bay regions by 1980 (eight generations ago). Thus, population genetic structure has emerged in Lake Huron Chinook salmon in <10 generations.