Testing the effects of genetic crossing distance on embryo survival within a metapopulation of brown trout (Salmo trutta)

Abstract

Predicting progeny performance from parental genetic divergence can potentially enhance the efficiency of supportive breeding programmes and facilitate risk assessment. Yet, experimental testing of the effects of breeding distance on offspring performance remains rare, especially in wild populations of vertebrates. Recent studies have demonstrated that embryos of salmonid fish are sensitive indicators of additive genetic variance for viability traits. We therefore used gametes of wild brown trout (Salmo trutta) from five genetically distinct populations of a river catchment in Switzerland, and used a full factorial design to produce over 2,000 embryos in 100 different crosses with varying genetic distances (F ST range: 0.005-0.035). Customized egg capsules allowed recording the survival of individual embryos until hatching under natural field conditions. Our breeding design enabled us to evaluate the role of the environment, of genetic and non-genetic parental contributions, and of interactions between these factors, on embryo viability. We found that embryo survival was strongly affected by maternal environmental (i.e. non-genetic) effects and by the microenvironment, i.e. by the location within the gravel. However, embryo survival was not predicted by population divergence, parental allelic dissimilarity, or heterozygosity, neither in the field nor under laboratory conditions. Our findings suggest that the genetic effects of inter-population hybridization within a genetically differentiated meta-population can be minor in comparison to environmental effects.

Effects of intraspecific hybridisation between two hatchery‐reared strains of Atlantic salmon, Salmo salar, on juvenile survival and fitness‐related traits

“…As noted by Stelkens et al . (), no significant sire effects were found in this study, and with a lack of additive genetic effects, it is still possible that environmental factors (maternal or otherwise) masked part of the genetic effects and therefore hybridisation effects.…”

“…When evaluating outbreeding in brown trout ( Salmo trutta ) using a full‐factorial cross, Stelkens et al . () did not find any significant effect of genetic distance over embryo survival, but maternal environmental effects were significant and possibly masked the effects of genetic distance. As noted by Stelkens et al .…”

Effects of altered river network connectivity on the distribution of Salmo trutta: Insights from a metapopulation model

“…Brown trout ( Salmo trutta Linnaeus, 1758) is a salmonid species that has been shown to present a metapopulation structure in previous studies (Massa‐Gallucci, Coscia, O'Grady, Kelly‐Quinn, & Mariani, ; Stelkens, Pompini, & Wedekind, ). Brown trout is one of the most widespread salmonid fish species in European inland waters and its natural distribution is fundamentally restricted to this area (Elliott, ), although it has been introduced to many countries worldwide (Elliott, ).…”

Genetic benefits of extreme sequential polyandry in a terrestrial‐breeding frog

“…Nevertheless, to exclude the possibility that microenvironmental variations among subclutches might influence estimates of genetic variance, future studies should aim to separate embryos immediately after fertilization and rear offspring independently. This approach has been effectively employed by studies testing for additive and nonadditive genetic effects on offspring survivorship and performance in various externally fertilizing fish species (Jacob et al 2007;Wedekind et al 2008;Jacob et al 2010;Clark, Stelkens et al 2013;Clark, Wilkins et al 2013;Pompini et al 2013;Brazzola et al 2014;Stelkens et al 2014;da Cunha et al 2018;da Cunha et al 2019).…”

“…), both additive and nonadditive genetic variance have been shown to contribute significantly to variance in offspring survivorship (Wedekind et al 2001;Neff 2006, 2007;Wedekind et al 2008;Brazzola et al 2014;Clark et al 2014). By contrast, in a slow growing small type Alpine whitefish (Coregonus albellus) and brown trout (Salmo trutta), offspring survival appears to be predominantly influenced by additive genetic effects, with no or negligible nonadditive genetic effects reported (Jacob et al 2007;Jacob et al 2010;Brazzola et al 2014;Stelkens et al 2014;da Cunha et al 2019). This differs from Atlantic cod (Gadus Morhua L.), where, similar to our study, only nonadditive effects appear to be important (Rudolfsen et al 2005).…”