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Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface.

ABSTRACT: BACKGROUND:Quantitative traits are typically considered to be under additive genetic control. Although there are indications that non-additive factors have the potential to contribute to trait variation, experimental demonstration remains scarce. Here, we investigated the genetic basis of growth in Atlantic salmon by exploiting the high level of genetic diversity and trait expression among domesticated, hybrid and wild populations. RESULTS:After rearing fish in common-garden experiments under aquaculture conditions, we performed a variance component analysis in four mapping populations totaling ~?7000 individuals from six wild, two domesticated and three F1 wild/domesticated hybrid strains. Across the four independent datasets, genome-wide significant quantitative trait loci (QTLs) associated with weight and length were detected on a total of 18 chromosomes, reflecting the polygenic nature of growth. Significant QTLs correlated with both length and weight were detected on chromosomes 2, 6 and 9 in multiple datasets. Significantly, epistatic QTLs were detected in all datasets. DISCUSSION:The observed interactions demonstrated that the phenotypic effect of inheriting an allele deviated between half-sib families. Gene-by-gene interactions were also suggested, where the combined effect of two loci resulted in a genetic effect upon phenotypic variance, while no genetic effect was detected when the two loci were considered separately. To our knowledge, this is the first documentation of epistasis in a quantitative trait in Atlantic salmon. These novel results are of relevance for breeding programs, and for predicting the evolutionary consequences of domestication-introgression in wild populations.

SUBMITTER: Besnier F

PROVIDER: S-EPMC7006396 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface.

Besnier Francois F Solberg Monica F MF Harvey Alison C AC Carvalho Gary R GR Bekkevold Dorte D Taylor Martin I MI Creer Simon S Nielsen Einar E EE Skaala Øystein Ø Ayllon Fernando F Dahle Geir G Glover Kevin A KA

BMC genetics 20200207 1

<h4>Background</h4>Quantitative traits are typically considered to be under additive genetic control. Although there are indications that non-additive factors have the potential to contribute to trait variation, experimental demonstration remains scarce. Here, we investigated the genetic basis of growth in Atlantic salmon by exploiting the high level of genetic diversity and trait expression among domesticated, hybrid and wild populations.<h4>Results</h4>After rearing fish in common-garden exper ...[more]

PMID: 32033538

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Project description:BackgroundDomestication is the process by which organisms become adapted to the human-controlled environment. Since the selection pressures that act upon cultured and natural populations differ, adaptations that favour life in the domesticated environment are unlikely to be advantageous in the wild. Elucidation of the differences between wild and domesticated Atlantic salmon may provide insights into some of the genomic changes occurring during domestication, and, help to predict the evolutionary consequences of farmed salmon escapees interbreeding with wild conspecifics. In this study the transcriptome of the offspring of wild and domesticated Atlantic salmon were compared using a common-garden experiment under standard hatchery conditions and in response to an applied crowding stressor.ResultsTranscriptomic differences between wild and domesticated crosses were largely consistent between the control and stress conditions, and included down-regulation of environmental information processing, immune and nervous system pathways and up-regulation of genetic information processing, carbohydrate metabolism, lipid metabolism and digestive and endocrine system pathways in the domesticated fish relative to their wild counterparts, likely reflective of different selection pressures acting in wild and cultured populations. Many stress responsive functions were also shared between crosses and included down-regulation of cellular processes and genetic information processing and up-regulation of some metabolic pathways, lipid and energy in particular. The latter may be indicative of mobilization and reallocation of energy resources in response to stress. However, functional analysis indicated that a number of pathways behave differently between domesticated and wild salmon in response to stress. Reciprocal F1 hybrids permitted investigation of inheritance patterns that govern transcriptomic differences between these genetically divergent crosses. Additivity and maternal dominance accounted for approximately 42 and 25% of all differences under control conditions for both hybrids respectively. However, the inheritance of genes differentially expressed between crosses under stress was less consistent between reciprocal hybrids, potentially reflecting maternal environmental effects.ConclusionWe conclude that there are transcriptomic differences between the domesticated and wild salmon strains studied here, reflecting the different selection pressures operating on them. Our results indicate that stress may affect certain biological functions differently in wild, domesticated and hybrid crosses and these should be further investigated.

Project description: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.

Project description:Interactions between domesticated escapees and wild conspecifics represent a threat to the genetic integrity and fitness of native populations. For Atlantic salmon, the recurrent presence of large numbers of domesticated escapees in the wild makes it necessary to better understand their impacts on native populations. We planted 254,400 eggs from 75 families of domesticated, F1-hybrid, and wild salmon in a river containing up- and downstream traps. Additionally, 41,630 hatchery smolts of the same pedigrees were released into the river. Over 8 years, 6,669 out-migrating smolts and 356 returning adults were recaptured and identified to their families of origin with DNA. In comparison with wild salmon, domesticated fish had substantially lower egg to smolt survival (1.8% vs. 3.8% across cohorts), they migrated earlier in the year (11.8 days earlier across years), but they only displayed marginally larger smolt sizes and marginally lower smolt ages. Upon return to freshwater, domesticated salmon were substantially larger at age than wild salmon (2.4 vs. 2.0, 4.8 vs. 3.2, and 8.5 vs. 5.6 kg across sexes for 1, 2, and 3 sea-winter fish) and displayed substantially lower released smolt to adult survival (0.41% vs. 0.94% across releases). Overall, egg-to-returning adult survival ratios were 1:0.76:0.30 and 1:0.44:0.21 for wild:F1-hybrid:domesticated salmon, respectively, using two different types of data. This study represents the most updated and extensive analysis of domesticated, hybrid, and wild salmon in the wild and provides the first documentation of a clear genetic difference in the timing of smolt migration-an adaptive trait presumed to be linked with optimal timing of entry to seawater. We conclude that spawning and hybridization of domesticated escapees can lead to (i) reduced wild smolt output and therefore wild adult abundance, through resource competition in freshwater, (ii) reduced total adult abundance due to freshwater competition and reduced marine survival of domesticated salmon, and (iii) maladaptive changes in phenotypic traits.

Project description: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.

Project description:BackgroundAtlantic salmon have been subject to domestication for approximately ten generations, beginning in the early 1970s. This process of artificial selection will have created various genetic differences between wild and farmed stocks. Each year, hundreds of thousands of farmed fish escape into the wild. These escapees may interbreed with wild conspecifics raising concerns for both the fish-farming industry and fisheries managers. Thus, a better understanding of the interactions between domesticated and wild salmon is essential to the continued sustainability of the aquaculture industry and to the maintenance of healthy wild stocks.ResultsWe compared the transcriptomes of a wild Norwegian Atlantic salmon population (Figgjo) and a Norwegian farmed strain (Mowi) at two life stages: yolk sac fry and post first-feeding fry. The analysis employed 44 k oligo-microarrays to analyse gene expression of 36 farmed, wild and hybrid (farmed dam x wild sire) individuals reared under identical hatchery conditions. Although some of the transcriptional differences detected overlapped between sampling points, our results highlighted the importance of studying various life stages. Compared to the wild population, the Mowi strain displayed up-regulation in mRNA translation-related and down regulation in nervous and immune system -related pathways in the sac fry, whereas up-regulation of digestive and endocrine activities, carbohydrate, energy, amino acid and lipid metabolism and down-regulation of environmental information processing and immune system pathways were evident in the feeding fry. Differentially regulated pathways that were common among life stages generally belonged to environmental information processing and immune system functional groups. In addition, we found indications of strong maternal effects, reinforcing the importance of including reciprocal hybrids in the analysis.ConclusionsIn agreement with previous studies we showed that domestication has caused changes in the transcriptome of wild Atlantic salmon and that many of the affected pathways are life-stage specific We highlighted the importance of reciprocal hybrids to the deconvolution of maternal/paternal effects and our data support the view that the genetic architecture of the strains studied highly influences the genes differentially expressed between wild and domesticated fish.

Project description:Increased knowledge of heritable traits in Atlantic Salmon (Salmo salar) is important to overcome bottlenecks in salmonid aquaculture. Atlantic salmonid populations, both landlocked and anadromous, represent an interesting model to gain insight into anadromy related traits, most notably, the probability to smoltify. While a previous study has identified several genomic regions diverging between anadromous and landlocked populations across the species range, the present study explores these data further with the aim to uncover if some of these genomic regions are linked to beneficial genetic traits associated with smoltification. In this study 17 of these loci were monitored in 669 anadromous salmon originating from 36 full-sibling families that had been reared under common garden conditions. The Smolt Index was calculated, using multiple visual markers, and provided a means of assessing smoltification stage. One SNP, located in Ssa04, showed a significant association with probability to smoltify, where individuals homozygous for the landlocked variant (LL) displayed a decrease in probability of smoltifying after one winter when compared with the homozygous for the anadromous variant (AA). This effect was independent of individual fish size. A separate common garden study comprising 200 individuals from either anadromous or landlocked strains showed that expression levels of ncor1, a thyroid mediator hormone located on the same chromosomal region (Ssa04), were significantly reduced in landlocked individuals post smoltification but remained constant in their anadromous counterparts. This study therefore suggests that while size is still the most important trigger for the induction of smoltification, there may also be an additional genetic component or trigger that has been 'lost' during the years deprived of SW transfer. In conclusion, the LL genotype identified here could potentially be used by the industry to delay smoltification and may also represent one of the first clues to the genetic regulation of smoltification in Atlantic salmon.

Dataset Information

Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface.

Publications

Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface.

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