Pre-fertilization gamete thermal environment influences reproductive success, unmasking opposing sex-specific responses in Atlantic salmon (Salmo salar).

The environment gametes perform in just before fertilization is increasingly recognized to affect offspring fitness, yet the contributions of male and female gametes and their adaptive significance remain largely unexplored. Here, we investigated gametic thermal plasticity and its effects on hatching success and embryo performance in Atlantic salmon (Salmo salar). Eggs and sperm were incubated overnight at 2°C or 8°C, temperatures within the optimal thermal range of this species. Crosses between warm- and cold-incubated gametes were compared using a full-factorial design, with half of each clutch reared in cold temperatures and the other in warm temperatures. This allowed disentangling single-sex interaction effects when pre-fertilization temperature of gametes mismatched embryonic conditions. Pre-fertilization temperature influenced hatch timing and synchrony, and matching sperm and embryo temperatures resulted in earlier hatching. Warm incubation benefited eggs but harmed sperm, reducing the hatching success and, overall, gametic thermal plasticity did not enhance offspring fitness, indicating vulnerability to thermal changes. We highlight the sensitivity of male gametes to higher temperatures, and that gamete acclimation may not effectively buffer against deleterious effects of thermal fluctuations. From an applied angle, we propose the differential storage of male and female gametes as a tool to enhance sustainability within the hatcheries.

In sea trout, the physiological response to salmon louse is stronger in female than in males.

The aims of this study were to compare male and female sea trout (Salmo trutta) with respect to their hypo-osmoregulatory ability over a simulated migration to seawater and their clinical and physiological response to salmon louse (Lepeophtheirus salmonis) infection in seawater and over a simulated pre-mature return to freshwater. For this purpose, 2-year-old hatchery-reared male and female brown trout (F1 offspring of wild caught anadromous fish) were infected with salmon lice and measured for changes in plasma ions, glucose, lactate and osmolality and relative heart, liver and gonad sizes during a simulated seawater migration and thereafter a premature return to freshwater after 4 weeks in seawater (pre-adult louse). Un-infected trout served as control. Male trout used longer time to develop full hypo-osmoregulatory ability in seawater and showed a stronger response in plasma glucose and lactate following simulated premature return to freshwater, compared to female trout. Response to salmon louse was stronger in female trout, shown by stronger osmotic stress by chalimus (plasma Cl-) and pre-adult louse (plasma osmolality) and elevated relative liver size (hepatosomatic index) by pre-adult louse in female compared to male trout. Moreover, high plasma cortisol in infected female and low plasma cortisol in infected male trout produced a significant treatment-sex interaction on plasma cortisol. Lice infection intensity was initially higher in male (0.18 lice g-1) compared to female trout (0.11 lice g-1) at the chalimus stage, but equal between sexes at the pre-adult stage (male 0.15 and female 0.17 lice g-1). This study showed that female trout were better adapted for changes in water salinity, while male trout were more robust against salmon louse infection. These results suggests that the elevated salmon louse infection pressure generated by salmon farming have strong and unexplored negative effects on wild sea trout populations. Further research on this topic is vital for the conservation of wild sea trout populations.

Genetic variation for upper thermal tolerance diminishes within and between populations with increasing acclimation temperature in Atlantic salmon.

Populations may counteract lasting temperature changes or recurrent extremes through plasticity or adaptation. However, it remains underexplored how outbreeding, either naturally, unintentionally, or facilitated, may modify a local response potential and whether genotype-by-environment interactions or between-trait correlations can restrict this potential. We quantified population differences and outbreeding effects, within-population genetic variation, and plasticity of these, for thermal performance proxy traits using 32 pedigreed wild, domesticated, and wild-domesticated Atlantic salmon families reared under common-garden conditions. Following exposure to ambient cold (11.6 °C) or ~4° and ~8° warmer summer temperatures, populations differed notably for body length and critical thermal maximum (CTmax) and for thermal plasticity of length, condition, and CTmax, but not for haematocrit. Line-cross analysis suggested mostly additive and some dominant outbreeding effects on means and solely additive outbreeding effects on plasticity. Heritability was detected for all traits. However, with increasing acclimation temperature, differences in CTmax between populations and CTmax heritability diminished, and CTmax breeding values re-ranked. Furthermore, CTmax and body size were negatively correlated at the genetic and phenotypic levels, and there was indirect evidence for a positive correlation between growth potential and thermal performance breadth for growth. Thus, population differences (including those between wild and domesticated populations) in thermal performance and plasticity may present a genetic resource in addition to the within-population genetic variance to facilitate, or impede, thermal adaptation. However, unfavourable genotype-by-environment interactions and negative between-trait correlations may generally hamper joint evolution in response to an increase in average temperature and temporary extremes.

Evolutionary drivers of kype size in Atlantic salmon (Salmo salar): domestication, age and genetics.

The diversity of reproduction and associated mating patterns in Atlantic salmon (Salmo salar) has long captivated evolutionary biologists. Salmo salar exhibit strategies involving migration, bold mating behaviours and radical morphological and physiological change. One such radical change is the elongation and curvature of the lower jaw in sexually mature males into a hook-like appendage called the kype. The kype is a secondary sexual characteristic used in mating hierarchies and a prime candidate for sexual selection. As one of the core global aquaculture fish species, however, mate choice, and thus sexual selection, has been replaced by industrial artificial fertilization seeking to develop more commercially viable strains. Removal of mate choice provides a unique opportunity to examine the kype over successive generations in the absence of sexual selection. Here we use a large-scale common-garden experiment, incorporating six experimental strains (wild, farmed and wild × farmed hybrids), experiencing one to three sea winters, to assess the impact of age and genetic background. After controlling for allometry, fork length-adjusted kype height (AKH) was significantly reduced in the domesticated strain in comparison to two wild strains. Furthermore, genetic variation at a locus on linkage group SSA1 was associated with kype height, and a locus on linkage group SSA23 was associated with fork length-adjusted kype length (AKL). The reduction in fork length-AKH in domesticated salmon suggests that the kype is of importance in mate choice and that it has decreased due to relaxation of sexual selection. Fork length-AKL showed an increase in domesticated individuals, highlighting that it may not be an important cue in mate choice. These results give us insight into the evolutionary significance of the kype, as well as implications of genetic induced phenotypic change caused by domesticated individuals escaping into the natural environment.

Plasticity in growth of farmed and wild Atlantic salmon: is the increased growth rate of farmed salmon caused by evolutionary adaptations to the commercial diet?

BACKGROUND: Domestication of Atlantic salmon for commercial aquaculture has resulted in farmed salmon displaying substantially higher growth rates than wild salmon under farming conditions. In contrast, growth differences between farmed and wild salmon are much smaller when compared in the wild. The mechanisms underlying this contrast between environments remain largely unknown. It is possible that farmed salmon have adapted to the high-energy pellets developed specifically for aquaculture, contributing to inflated growth differences when fed on this diet. We studied growth and survival of 15 families of farmed, wild and F1 hybrid salmon fed three contrasting diets under hatchery conditions; a commercial salmon pellet diet, a commercial carp pellet diet, and a mixed natural diet consisting of preserved invertebrates commonly found in Norwegian rivers. RESULTS: For all groups, despite equal numbers of calories presented by all diets, overall growth reductions as high 68 and 83%, relative to the salmon diet was observed in the carp and natural diet treatments, respectively. Farmed salmon outgrew hybrid (intermediate) and wild salmon in all treatments. The relative growth difference between wild and farmed fish was highest in the carp diet (1: 2.1), intermediate in the salmon diet (1:1.9) and lowest in the natural diet (1:1.6). However, this trend was non-significant, and all groups displayed similar growth reaction norms and plasticity towards differing diets across the treatments. CONCLUSIONS: No indication of genetic-based adaptation to the form or nutritional content of commercial salmon diets was detected in the farmed salmon. Therefore, we conclude that diet alone, at least in the absence of other environmental stressors, is not the primary cause for the large contrast in growth differences between farmed and wild salmon in the hatchery and wild. Additionally, we conclude that genetically-increased appetite is likely to be the primary reason why farmed salmon display higher growth rates than wild salmon when fed ad lib rations under hatchery conditions. Our results contribute towards an understanding of the potential genetic changes that have occurred in farmed salmon in response to domestication, and the potential mechanisms underpinning genetic and ecological interactions between farmed escapees and wild salmonids.

Does density influence relative growth performance of farm, wild and F1 hybrid Atlantic salmon in semi-natural and hatchery common garden conditions?

The conditions encountered by Atlantic salmon, Salmo salar L., in aquaculture are markedly different from the natural environment. Typically, farmed salmon experience much higher densities than wild individuals, and may therefore have adapted to living in high densities. Previous studies have demonstrated that farmed salmon typically outgrow wild salmon by large ratios in the hatchery, but these differences are much less pronounced in the wild. Such divergence in growth may be explained partly by the offspring of wild salmon experiencing higher stress and thus lower growth when compared under high-density farming conditions. Here, growth of farmed, wild and F1 hybrid salmon was studied at contrasting densities within a hatchery and semi-natural environment. Farmed salmon significantly outgrew hybrid and wild salmon in all treatments. Importantly, however, the reaction norms were similar across treatments for all groups. Thus, this study was unable to find evidence that the offspring of farmed salmon have adapted more readily to higher fish densities than wild salmon as a result of domestication. It is suggested that the substantially higher growth rate of farmed salmon observed in the hatchery compared with wild individuals may not solely be caused by differences in their ability to grow in high-density hatchery scenarios.

Thermal plasticity in farmed, wild and hybrid Atlantic salmon during early development: has domestication caused divergence in low temperature tolerance?

BACKGROUND: In the past three decades, millions of domesticated Atlantic salmon Salmo salar L. have escaped from farms into the wild. Their offspring display reduced survival in the natural environment, which demonstrates that gene-flow is likely to have a negative effect on wild populations. However, inter-population differences in introgression of farmed salmon have been observed, and the underlying ecological mechanisms remain enigmatic. We hypothesised that domestication-driven divergence in tolerance to low temperatures during early development may contribute to lower survival of farmed salmon offspring in the wild, which in turn, may influence patterns of introgression among populations exposed to different temperature regimes. We reared the offspring of 35 families of wild, farmed and hybrid origin at three temperatures (3.9, 5.6 and 12°C) from the onset of exogenous feeding and throughout their first summer. Thermal reaction norms for growth and survival were investigated along the gradient. RESULTS: The main results of this study, which is based upon the analysis of juvenile salmon from five wild strains, two farmed strains and two hybrid strains, can be summarised as; (i) salmon of all origins were able to successfully initiate feeding at all temperatures and similar survival reaction norms were detected in all strains across the temperature gradient; (ii) deviating growth reaction norms were detected between strains, although this result was most likely due to an overall lack of growth in the lower temperature treatments. CONCLUSIONS: This study revealed no evidence of domesticated-driven divergence in low temperature tolerance in Atlantic salmon during early development. Although the potential interaction between low temperature and other river-specific factors cannot be excluded, our results indicate that the reduced survival of farmed offspring in the wild is not explained by farmed salmon displaying impaired abilities to initiate feeding at low temperatures. We therefore suggest that the observed inter-population patterns of introgression are not low-temperature driven and that other ecological or biological factors may explain why detection of farmed salmon in wild rivers is not synonymous with introgression. In general, our results support the literature indicating that phenotypic plasticity instead of thermal adaption has been selected for in Atlantic salmon.