A General Model of Distant Hybridization Reveals the Conditions for Extinction in Atlantic Salmon and Brown Trout (original) (raw)

Consequences of farmed–wild hybridization across divergent wild populations and multiple traits in salmon

Ecological Applications, 2010

Theory predicts that hybrid fitness should decrease as population divergence increases. This suggests that the effects of human-induced hybridization might be adequately predicted from the known divergence among parental populations. We tested this prediction by quantifying trait differentiation between multigenerational crosses of farmed Atlantic salmon (Salmo salar) and divergent wild populations from the Northwest Atlantic; the former escape repeatedly into the wild, while the latter are severely depleted. Under common environmental conditions and at the spatiotemporal scale considered (340 km, 12 000 years of divergence), substantial cross differentiation had a largely additive genetic basis at behavioral, life history, and morphological traits. Wild backcrossing did not completely restore hybrid trait distributions to presumably more optimal wild states. Consistent with theory, the degree to which hybrids deviated in absolute terms from their parental populations increased with increasing parental divergence (i.e., the collective environmental and life history differentiation, genetic divergence, and geographic distance between parents). Nevertheless, while these differences were predictable, their implications for risk assessment were not: wild populations that were equally divergent from farmed salmon in the total amount of divergence differed in the specific traits at which this divergence occurred. Combined with ecological data on the rate of farmed escapes and wild population trends, we thus suggest that the greatest utility of hybridization data for risk assessment may be through their incorporation into demographic modeling of the short-and long-term consequences to wild population persistence. In this regard, our work demonstrates that detailed hybridization data are essential to account for life-stage-specific changes in phenotype or fitness within divergent but interrelated groups of wild populations. The approach employed here will be relevant to risk assessments in a range of wild species where hybridization with domesticated relatives is a concern, especially where the conservation status of the wild species may preclude direct fitness comparisons in the wild.

Interspecific Hybridization, a Matter of Pioneering? Insights from Atlantic Salmon and Brown Trout

Journal of Heredity, 2011

Interspecific hybridization may occur in situations of recent contact between a colonizer and a resident species, being more intense in the colonization front. Atlantic salmon Salmo salar and brown trout S. trutta have been sympatric species since their origin and they share spatial and temporal spawning niches, exhibiting low levels of bidirectional interspecific hybridization and introgression throughout their distribution range. Different causes have been identified for increased hybridization, from escapes or deliberate releases of domesticated fish to sneaking male behavior. We have examined hybridization rates and direction in different situations of advance of one of these species into a territory formerly inhabited by the other (247 samples were analyzed in northern Spain and 487 in Kerguelen Islands). In all cases, hybrids found in the colonization front were offspring of colonizer females and resident males. We hypothesize that these findings are the result of adaptive relaxed mate choice of colonizing females, regardless of the relative abundance of each species.

Beyond hybridization: the genetic impacts of nonreproductive ecological interactions of salmon aquaculture on wild populations

Aquaculture Environment Interactions, 2020

Cultured Atlantic salmon Salmo salar are of international socioeconomic value, and the process of domestication has resulted in significant behavioural, morphological, and allelic differences from wild populations. Substantial evidence indicates that direct genetic interactions or interbreeding between wild and escaped farmed Atlantic salmon occurs, genetically altering wild salmon and reducing population viability. However, genetic interactions may also occur through ecological mechanisms (e.g. disease, parasites, predation, competition), both in conjunction with and in the absence of interbreeding. Here we examine existing evidence for ecological and non-reproductive genetic interactions between domestic Atlantic salmon and wild populations and the potential use of genetic and genomic tools to resolve these impacts. Our review identified examples of genetic changes resulting from ecological processes, predominately through pathogen or parasite transmission. In addition, many examp...

Interspecific hybridization and introgression are associated with stock transfers in salmonids

Aquaculture, 2008

Domestic stocks may endanger wild populations by escapes or deliberate releases, not only through competition for resources but also through gene pool contamination if they reproduce in the wild. One of the risks is increased interspecific hybridization by interspecific matings. Stocking of domesticated genomes into wild ecosystems leads to a heightened frequency of interspecific hybridization in sympatric south European Atlantic salmon Salmo salar and brown trout Salmo trutta. Introgressive hybridization involving brown trout males of domestic origin was demonstrated. Following cessation of domestic stock releases in eight south European rivers, hybridization decreased significantly. These results emphasize the risks associated with stock transfers and escapes of domestic individuals in wild ecosystems and illustrate the potential role of domestic stocks when they contribute to secondary contact between species.

Ecological segregation moderates a climactic conclusion to trout hybridization

Global change biology, 2017

For decades, it has been assumed that introgressive hybridization between introduced rainbow trout and native cutthroat trout in western North America will lead to genomic extinction of the latter. A broad-scale re-examination of their interaction indicates that ecological differences between these species and demographic processes are dictating the location and extent of their hybrid zones, and that runaway introgression between these taxa is unlikely.

The Relative Risks of Inbreeding and Outbreeding Endangered Populations of Atlantic Salmon, Salmo salar

The negative consequences associated with inbreeding depression and the loss of within-population genetic diversity may be similar in scope to those associated with outbreeding depression. Here, inbred and outbred crosses were generated using three neighbouring endangered Atlantic salmon (Salmo salar) populations. In the laboratory common-garden environment, there were no significant differences in fitness-related traits between the crosses. In the wild environment reciprocal transplant, there was consistent evidence for extrinsic outbreeding depression and inbreeding depression for one river population and there was among-site variability in the responses of the other two river populations examined. There was also evidence of intrinsic outbreeding depression for one second-generation hybrid cross in the wild environment. The findings reported here demonstrate that salmon populations may be locally adapted at small spatial scales and that the fitness consequences resulting from genetic interactions between population pairs can not readily be predicted.

Maintenance of asymmetric hybridization between Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) via postzygotic barriers and paternal effects

At the southern European edge of Atlantic salmon (Salmo salar) distribution, all the hybrids found in nature are the product of crosses between female salmon and male brown trout (Salmo trutta). By artificially producing reciprocal crosses between salmon and trout, we demonstrate that unidirectional hybridization observed in nature is the result of postzygotic barriers that produce very high mortality rates (95%) in female trout × male salmon hybrids and not the consequence of prezygotic isolation or behavioural differences between the two species. Mortality of female trout × male salmon hybrids mainly occurs during the last phases of development, and a high percentage of these surviving hybrids showed external deformities that could compromise survival in the wild. Another important finding is the existence of paternal factor in embryo development. Using time to midhatch as an indicator of developmental rate, female salmon × male trout hybrids hatched faster than female trout × male salmon hybrids, with both developing at a rate intermediate to the pure crosses. The early emergence of female salmon × male trout hybrids, which have similar survival to pure salmons, could have fitness repercussions, since early emerging fry have a competitive advantage over later emerging fry.

Interbreeding of genetically distinct native brown trout (Salmo trutta) populations designates offspring fitness

Aquaculture, 2012

Supportive breeding with subsequent stocking is an important long-term conservation tool for sustaining harvestable populations and genetic diversity in wild fish populations. In salmonids, this strategy often implies, inadvertently or for logistic reasons, breeding of a mixture of local populations, which may lead to loss of local adaptation and pose risks to receiving populations. In an alpine lake system in Norway (Pålsbu-Tunhovd), we assessed long-term effects of interbreeding three brown trout (Salmo trutta) populations from separate and environmentally contrasting spawning and recruitment habitats. Using a Bayesian genetic assignment algorithm we compared numeric contributions and genetic and demographic characteristics of wild-born and lake-stocked fish within and across populations. Population contribution by the broodstock was disproportional to the number of surviving and reproductively ready stocked brown trout, indicating higher lifetime survival for brown trout descending from a large river dominated by large fish. Life history selection was further indicated by a discrepancy between observed and expected numbers of adult hybrids, i.e., fewer hybrids suggest negative fitness effects of hybridization. Hence, supportive breeding changed gene frequencies, although reduced genetic variation was not documented in mature stocked brown trout. Post stocking, these fish retained the initial length advantage relative to the fastest-growing wild-born population until the age of ten. Stocked brown trout had similar growth rates regardless of genetic origin, whereas wild-born brown trout growth rates differed among recruitment habitats. Our study in this system indicates that genetic origin determined longevity. Genetics may be a less important determinant for growth rates in lake-stocked than in wild-born brown trout.

Outbreeding depression in hybrids between spatially separated pink salmon, Oncorhynchus gorbuscha, populations: marine survival, homing ability, and variability in …

… biology of fishes, 2004

Hybridization between distinct populations and introgression of nonnative genes can erode fitness of native populations through outbreeding depression, either by producing a phenotype intermediate to that of both contributing genomes (and maladapted in either population's environment) or by disrupting distinct coadapted complexes of epistatic genes. In salmon, fitness-related traits such as homing ability or family-size distribution may be eroded. We investigated geographically separated pink salmon populations in repeated trials in independent broodyears (odd and even). Hybrids were made between female Auke Creek (Southeast Alaska) pink salmon and Pillar Creek (Kodiak Island, ∼1 000 km away) males; hybrids and their offspring were compared to offspring of control crosses of the same females with Auke Creek males. Parentage assignment from microsatellite analysis was used to improve estimates of survival and straying and to examine variation of family size. Hybridization reduced return rates of adults (a proxy for survival at sea) in the F 1 generation in the odd-year broodline (p < 0.0001) but not in the evenyear broodline (p = 0.678). Hybridization reduced survival in both the odd-and even-broodyear F 2 (p < 0.005 and p < 0.0001). Hybridization did not appear to impair homing ability; weekly surveys revealed similar straying rates (∼2%) by both hybrid and control fish into nearby (∼1 km) Waydelich Creek in both generations in both trials. Hybridization did not increase the index of variability (σ 2 /µ) in family size. Decreased survival in the hybrid F 2 generation supports an epistatic model of outbreeding depression; nonepistatic effects may have contributed to reduced survival in the odd-broodyear F 1 hybrid fish. Outbreeding depression in hybrids of geographically separated populations demonstrates that introgression of nonnative fish can erode fitness, and should be recognized as a potential detriment of both aquaculture and management practices.