Philip McGinnity

Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon.

The high level of escapes from Atlantic salmon farms, up to two million fishes per year in the North Atlantic, has raised concern about the potential impact on wild populations. We report on a two-generation experiment examining the estimated lifetime successes, relative to wild natives, of farm, F1 and F2 hybrids and BC1 backcrosses to wild and farm salmon. Offspring of farm and ‘hybrids’ (i.e. all F1, F2 and BC1 groups) showed reduced survival compared with wild salmon but grew faster as juveniles and displaced wild parr, which as a group were significantly smaller. Where suitable habitat for these emigrant parr is absent, this competition would result in reduced wild smolt production. In the experimental conditions, where emigrants survived downstream, the relative estimated lifetime success ranged from 2% (farm) to 89% (BC1 wild) of that of wild salmon, indicating additive genetic variation for survival. Wild salmon primarily returned to fresh water after one sea winter (1SW) but farm and ‘hybrids’ produced proportionately more 2SW salmon. However, lower overall survival means that this would result in reduced recruitment despite increased 2SW fecundity. We thus demonstrate that interaction of farm with wild salmon results in lowered fitness, with repeated escapes causing cumulative fitness depression and potentially an extinction vortex in vulnerable populations.

Genetic impact of escaped farmed Atlantic salmon (Salmo salar L.) on native populations: use of DNA profiling to assess freshwater performance of wild, farmed, and hybrid progeny in a natural river environment

McGinnity, P., Stone, C., Taggart, J. B., Cooke, D., Cotter, D., Hynes, R., McCamley, C., Cross, T., and Ferguson, A. 1997. Genetic impact of escaped farmed Atlantic salmon (Sulmo salar L.) on native populations: use of DNA profiling to assess freshwater performance of wild, farmed, and hybrid progeny in a natural river environment. - ICES Journal of Marine Science, 54: 998-1008. Since Atlantic salmon (Salmo salur L.) used for farming are usually genetically different from local wild populations, breeding of escaped farmed salmon potentially results in genetic changes in wild populations. To determine the likelihood and impact of such genetic change, an experiment was undertaken, in a natural spawning tributary of the Burrishoole system in western Ireland, to compare the performance of wild, farmed, and hybrid Atlantic salmon progeny. Juveniles were assigned to family and group parentage by DNA profiling based on composite genotypes at seven minisatellite loci. Survival of the progeny of farmed salmon to the smolt stage was significantly lower than that of wild salmon, with increased mortality being greatest in the period from the eyed egg to the first summer. However, progeny of farmed salmon grew fastest and competitively displaced the smaller native fish downstream. The offspring of farmed salmon showed a reduced incidence of male parr maturity compared with native fish. The latter also showed a greater tendency to migrate as autumn pre-smolts. Growth and performance of hybrids were generally either intermediate or not significantly different from the wild fish. The demonstration that farmed and hybrid progeny can survive in the wild to the smolt stage, taken together with unpublished data that show that these smolts can survive at sea and home to their river of origin, indicates that escaped farmed salmon can produce long-term genetic changes in natural populations. These changes affect both single-locus and high-heritability quantitative traits, e.g. growth, sea age of maturity. While some of these changes may be advantageous from an angling management perspective, they are likely, in specific circumstances, to reduce population fitness and productivity. Full assessment of these changes will require details of marine survival, homing and reproductive performance of the adults together with information on the F, generation. 0 1997 International Council for the Exploration of the Sea

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

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

Restocking of salmonids—opportunities and limitations

Stocking can be a cost effective method of enhancing salmonid populations, in particular where the aim is to restore populations or mitigate against developments. There are risks associated with any intervention and it is suggested that all stockings undergo risk screening in order to identify the high risk areas. The main concern regarding stocking relates to the impact on the genetic fitness of the wild population, and proposals to minimise the impact while still maintaining a fishery are made. To ensure that the greatest benefit from a stocking programme is realised, stocking rates should be optimal for the type of habitat being stocked. How this can be determined is presented together with guidelines for stocking different types of habitat. Benefit, in terms of cost of adult return or per adult fish caught, enables comparisons to be made with other management options. Information on survival rates of wild and hatchery-reared fish, unit cost of production and the economic value of fish and fishing is summarised enabling simple estimates of cost: benefit to be determined.

Impact of naturally spawning captive-bred Atlantic salmon on wild populations: depressed recruitment and increased risk of climate-mediated extinction

The assessment report of the 4th International Panel on Climate Change confirms that global warming is strongly affecting biological systems and that 20–30% of species risk extinction from projected future increases in temperature. It is essential that any measures taken to conserve individual species and their constituent populations against climate-mediated declines are appropriate. The release of captive bred animals to augment wild populations is a widespread management strategy for many species but has proven controversial. Using a regression model based on a 37-year study of wild and sea ranched Atlantic salmon (Salmo salar) spawning together in the wild, we show that the escape of captive bred animals into the wild can substantially depress recruitment and more specifically disrupt the capacity of natural populations to adapt to higher winter water temperatures associated with climate variability. We speculate the mechanisms underlying this seasonal response and suggest that an explanation based on bio-energetic processes with physiological responses synchronized by photoperiod is plausible. Furthermore, we predict, by running the model forward using projected future climate scenarios, that these cultured fish substantially increase the risk of extinction for the studied population within 20 generations. In contrast, we show that positive outcomes to climate change are possible if captive bred animals are prevented from breeding in the wild. Rather than imposing an additional genetic load on wild populations by releasing maladapted captive bred animals, we propose that conservation efforts should focus on optimizing conditions for adaptation to occur by reducing exploitation and protecting critical habitats. Our findings are likely to hold true for most poikilothermic species where captive breeding programmes are used in population management.

Management of salmonid fisheries in the British Isles: towards a practical approach based on population genetics

The evidence for structuring of Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) into distinct reproductive populations and for genetic differentiation and local adaptation is compelling. The effect of genetic variation among populations is demonstrably a factor determining the economic value of salmonid fisheries in the British Isles. Genetic considerations are, therefore, a matter of self-interest for fisheries managers and a shared interest with those advocating more general approaches to the conservation of diversity and variation. The local population is the basic unit of production and, therefore, the preferred unit of management. However, salmonid populations are numerous and many are small. These factors limit practical possibilities for management at the population level. We suggest that this difficulty can be addressed by combining populations in fisheries-biased management units that comprise interchangeable, nested groupings of populations that are both genetically and biologically meaningful. This population-based approach addresses the necessity of managing the fisheries in ways that are consistent with the conservation of adaptive potential in relation to the dynamic aspects of populations, their capacity to respond to changing environmental conditions, and the likelihood that salmonids will remain a worthwhile resource for the future.

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.

The biogeography of the atlantic salmon (Salmo salar) gut microbiome.

Although understood in many vertebrate systems, the natural diversity of host-associated microbiota has been little studied in teleosts. For migratory fishes, successful exploitation of multiple habitats may affect and be affected by the composition of the intestinal microbiome. We collected 96 Salmo salar from across the Atlantic encompassing both freshwater and marine phases. Dramatic differences between environmental and gut bacterial communities were observed. Furthermore, community composition was not significantly impacted by geography. Instead life-cycle stage strongly defined both the diversity and identity of microbial assemblages in the gut, with evidence for community destabilisation in migratory phases. Mycoplasmataceae phylotypes were abundantly recovered in all life-cycle stages. Patterns of Mycoplasmataceae phylotype recruitment to the intestinal microbial community among sites and life-cycle stages support a dual role for deterministic and stochastic processes in defining the composition of the S. salar gut microbiome.

Demographics and landscape features determine intrariver population structure in Atlantic salmon (Salmo salar L.): the case of the River Moy in Ireland

Contemporary genetic structure of Atlantic salmon (Salmo salar L.) in the River Moy in Ireland is shown here to be strongly related to landscape features and population demographics, with populations being defined largely by their degree of physical isolation and their size. Samples of juvenile salmon were collected from the 17 major spawning areas on the river Moy and from one spawning area in each of five smaller nearby rivers. No temporal allele frequency differences were observed within locations for 12 microsatellite loci, whereas nearly all spatial samples differed significantly, suggesting that each was a separate population. Bayesian clustering and landscape genetic analyses suggest that these populations can be combined hierarchically into five genetically informative larger groupings. Lakes were found to be the single most important determinant of the observed population structure. Spawning area size was also an important factor. The salmon population of the closest nearby river resembled genetically the largest Moy population grouping. In addition, we showed that anthropogenic influences on spawning habitats, in this case arterial drainage, can affect relationships between populations. Our results show that Atlantic salmon biodiversity can be largely defined by geography, and thus, knowledge of landscape features (for example, as characterized within Geographical Information Systems) has the potential to predict population structure in other rivers without an intensive genetic survey, or at least to help direct sampling. This approach of combining genetics and geography, for sampling and in subsequent statistical analyses, has wider application to the investigation of population structure in other freshwater/anadromous fish species and possibly in marine fish and other organisms.

Screen for Footprints of Selection during Domestication/Captive Breeding of Atlantic Salmon.

Domesticated animals provide a unique opportunity to identify genomic targets of artificial selection to the captive environment. Here, we screened three independent domesticated/captive Atlantic salmon (Salmo salar) strains and their wild progenitor populations in an effort to detect potential signals of domestication selection by typing of 261 SNPs and 70 microsatellite loci. By combining information from four different neutrality tests, in total ten genomic regions showed signs of directional selection based on multiple sources of evidence. Most of the identified candidate regions were rather small ranging from zero to a few centimorgans (cM) in the female Atlantic salmon linkage map. We also evaluated how adaptation from standing variation affects adjacent SNP and microsatellite variation along the chromosomes and, by using forward simulations with strong selection, we were able to generate genetic differentiation patterns comparable to the observed data. This study highlights the significance of standing genetic variation during the early stages of adaptation and represents a useful step towards identifying functional variants involved in domestication of Atlantic salmon.