Introgression of domesticated salmon changes life history and phenology of a wild salmon population.

The release of domesticated conspecifics into the natural environment, whether deliberate or accidental, has the potential to alter the genetic integrity and evolutionary trajectory of wild populations. This widespread challenge is of particular concern for wild Atlantic salmon. By investigating phenotypic differences between the offspring of domesticated, hybrid, and wild Atlantic salmon released into the natural environment, earlier studies have documented the short-term consequences of introgression from domesticated fish into wild salmon populations. However, few studies have investigated the joined product of introgression and natural selection after several generations. Here, we investigated the phenotypic response of an Atlantic salmon population that has been subjected to an average of 24% genetic admixture by domesticated conspecifics escaping from fish farms over three decades (approximately 6-7 generations). Individual levels of admixture were positively correlated with increased size at the smolt and adult stages for both sexes, a decrease in the age of male smolts, and a decrease in the age at maturity for males. These life history changes are presumably the consequence of the well-documented directional selection for increased growth in domesticated salmon and are likely maladaptive. However, the most novel result of this study is that admixture was positively linked with delayed date of return to the river, with highly admixed fish arriving up to 26 days later than nonadmixed fish. Potentially, this phenological change provides admixed individuals with a survival advantage in the later phase of the life cycle as it reduces their period of exposure to selection through rod and line angling. We, therefore, conclude that while gene flow from domesticated conspecifics changes life history and phenological traits of wild Atlantic salmon populations, most of which are likely to be maladaptive, when pressured by additional anthropogenic challenges, some changes may confer a fitness advantage for a short part of the life cycle.

Domestication-induced reduction in eye size revealed in multiple common garden experiments: The case of Atlantic salmon (Salmo salar L.).

Domestication leads to changes in traits that are under directional selection in breeding programmes, though unintentional changes in nonproduction traits can also arise. In offspring of escaping fish and any hybrid progeny, such unintentionally altered traits may reduce fitness in the wild. Atlantic salmon breeding programmes were established in the early 1970s, resulting in genetic changes in multiple traits. However, the impact of domestication on eye size has not been studied. We measured body size corrected eye size in 4000 salmon from six common garden experiments conducted under artificial and natural conditions, in freshwater and saltwater environments, in two countries. Within these common gardens, offspring of domesticated and wild parents were crossed to produce 11 strains, with varying genetic backgrounds (wild, domesticated, F1 hybrids, F2 hybrids and backcrosses). Size-adjusted eye size was influenced by both genetic and environmental factors. Domesticated fish reared under artificial conditions had smaller adjusted eye size when compared to wild fish reared under identical conditions, in both the freshwater and marine environments, and in both Irish and Norwegian experiments. However, in parr that had been introduced into a river environment shortly after hatching and sampled at the end of their first summer, differences in adjusted eye size observed among genetic groups were of a reduced magnitude and were nonsignificant in 2-year-old sea migrating smolts sampled in the river immediately prior to sea entry. Collectively, our findings could suggest that where natural selection is present, individuals with reduced eye size are maladapted and consequently have reduced fitness, building on our understanding of the mechanisms that underlie a well-documented reduction in the fitness of the progeny of domesticated salmon, including hybrid progeny, in the wild.

Autosomal sdY Pseudogenes Explain Discordances Between Phenotypic Sex and DNA Marker for Sex Identification in Atlantic Salmon.

Despite the key role that sex-determination plays in evolutionary processes, it is still poorly understood in many species. In salmonids, which are among the best studied fishes, the master sex-determining gene sexually dimorphic on the Y-chromosome (sdY) has been identified. However, sdY displays unexplained discordance to the phenotypic sex, with a variable frequency of phenotypic females being reported as genetic males. Multiple sex determining loci in Atlantic salmon have also been reported, possibly as a result of recent transposition events in this species. We hypothesized the existence of an autosomal copy of sdY, causing apparent discordance between phenotypic and genetic sex, that is transmitted in accordance with autosomal inheritance. To test this, we developed a qPCR methodology to detect the total number of sdY copies present in the genome. Based on the observed phenotype/genotype frequencies and linkage analysis among 2,025 offspring from 64 pedigree-controlled families of accurately phenotyped Atlantic salmon, we identified both males and females carrying one or two autosomal copies of sdY in addition to the Y-specific copy present in males. Patterns across families were highly consistent with autosomal inheritance. These autosomal sdY copies appear to have lost the ability to function as a sex determining gene and were only occasionally assigned to the actual sex chromosome in any of the affected families.

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.

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.

Hatching time and alevin growth prior to the onset of exogenous feeding in farmed, wild and hybrid Norwegian Atlantic salmon.

The onset of exogenous feeding, when juveniles emerge from the gravel, is a critical event for salmonids where early emergence and large size provide a competitive advantage in the wild. Studying 131 farmed, hybrid and wild Norwegian Atlantic salmon families, originating from four wild populations and two commercial strains, we investigated whether approximately 10 generations of selection for faster growth has also resulted in increased somatic growth prior to the onset of exogenous feeding. In addition, we tested whether relaxed selection in farms has allowed for alterations in hatching time between farmed and wild salmon. Across three cohorts, wild salmon families hatched earlier than farmed salmon families, while hybrid families displayed intermediate hatching times. While the observed differences were small, i.e., 1-15 degree-days (0-3 days, as water temperatures were c. 5-6°C), these data suggest additive genetic variation for hatching time. Alevin length prior to exogenous feeding was positively related to egg size. After removal of egg size effects, no systematic differences in alevin length were observed between the wild and farmed salmon families. While these results indicate additive genetic variation for egg development timing, and wild salmon families consistently hatched earlier than farmed salmon families, these differences were so small they are unlikely to significantly influence early life history competition of farmed and wild salmon in the natural environment. This is especially the case given that the timing of spawning among females can vary by several weeks in some rivers. The general lack of difference in size between farmed and wild alevins, strongly suggest that the documented differences in somatic growth rate between wild and farmed Norwegian Atlantic salmon under hatchery conditions are first detectable after the onset of exogenous feeding.

Growth reaction norms of domesticated, wild and hybrid Atlantic salmon families in response to differing social and physical environments.

BACKGROUND: Directional selection for growth has resulted in the 9-10th generation of domesticated Atlantic salmon Salmo salar L. outgrowing wild salmon by a ratio of approximately 3:1 when reared under standard hatchery conditions. In the wild however, growth of domesticated and wild salmon is more similar, and seems to differ at the most by a ratio of 1.25:1. Comparative studies of quantitative traits in farmed and wild salmon are often performed by the use of common-garden experiments where salmon of all origins are reared together to avoid origin-specific environmental differences. As social interaction may influence growth, the large observed difference in growth between wild and domesticated salmon in the hatchery may not be entirely genetically based, but inflated by inter-strain competition. This study had two primary aims: (i) investigate the effect of social interaction and inter-strain competition in common-garden experiments, by comparing the relative growth of farmed, hybrid and wild salmon when reared together and separately; (ii) investigate the competitive balance between wild and farmed salmon by comparing their norm of reaction for survival and growth along an environmental gradient ranging from standard hatchery conditions to a semi-natural environment with restricted feed. RESULTS: The main results of this study, which are based upon the analysis of more than 6000 juvenile salmon, can be summarised as; (i) there was no difference in relative growth between wild and farmed salmon when reared together and separately; (ii) the relative difference in body weight at termination between wild and farmed salmon decreased as mortality increased along the environmental gradient approaching natural conditions. CONCLUSIONS: This study demonstrates that potential social interactions between wild and farmed salmon when reared communally are not likely to cause an overestimation of the genetic growth differences between them. Therefore, common-garden experiments represent a valid methodological approach to investigate genetic differences between wild and farmed salmon. As growth of surviving salmon of all origins became more similar as mortality increased along the environmental gradient approaching natural conditions, a hypothesis is presented suggesting that size-selective mortality is a possible factor reducing growth differences between these groups in the wild.

Does domestication cause changes in growth reaction norms? A study of farmed, wild and hybrid Atlantic salmon families exposed to environmental stress.

One of the most important traits linked with the successful domestication of animals is reducing their sensitivity to environmental stressors in the human controlled environment. In order to examine whether domestication selection in Atlantic salmon Salmo salar L., over approximately ten generations, has inadvertently selected for reduced responsiveness to stress, we compared the growth reaction norms of 29 wild, hybrid and domesticated families reared together under standard hatchery conditions (control) and in the presence of a stressor (reduced water level twice daily). The experiment was conducted for a 14 week period. Farmed salmon outgrew wild salmon 1:2.93 in the control tanks, and no overlap in mean weight was displayed between families representing the three groups. Thus, the elevation of the reaction norms differed among the groups. Overall, growth was approximately 25% lower in the stressed tanksl; however, farmed salmon outgrew wild salmon 1:3.42 under these conditions. That farmed salmon maintained a relatively higher growth rate than the wild salmon in the stressed tanks demonstrates a lower responsiveness to stress in the farmed salmon. Thus, flatter reaction norm slopes were displayed in the farmed salmon, demonstrating reduced plasticity for this trait under these specific experimental conditions. For all growth measurements, hybrid salmon displayed intermediate values. Wild salmon displayed higher heritability estimates for body weight than the hybrid and farmed salmon in both environments. This suggests reduced genetic variation for body weight in the farmed contra wild salmon studied here. While these results may be linked to the specific families and stocks investigated, and verification in other stocks and traits is needed, these data are consistent with the theoretical predictions of domestication.