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

Francois Besnier,Alison C Harvey,Monica F Solberg,Fernando Ayllon,Geir Dahle,Martin I Taylor,Øystein Skaala,Einar E Nielsen,Simon Creer,Dorte Bekkevold,Gary R Carvalho,Kevin A Glover

doi:10.1186/s12863-020-0816-y

Abstract

BackgroundQuantitative 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.ResultsAfter 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.DiscussionThe 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.

Highlights

Quantitative traits are typically considered to be under additive genetic control
Polygenic traits are often simultaneously influenced by non-additive genetic mechanisms [10], and while heritability is the main target of focus to improve the performance of a given breed, non-additive genetic effects may play a key role in explaining phenotypic diversity
Significant Quantitative trait loci (QTL) on chromosome 2 affecting growth have been documented in domesticated and wild European Atlantic salmon studied in the wild [31]. These results strongly suggest the presence of QTLs on chromosome 2 linked to both juvenile and adult growth in Atlantic salmon, it is worth mentioning that a QTL on chromosome 2 is not reported in all studies [30], nor at all sampling points over time, when the same mapping material is sampled repeatedly [26]

Summary

Introduction

Quantitative traits are typically considered to be under additive genetic control. there are indications that non-additive factors have the potential to contribute to trait variation, experimental demonstration remains scarce. Polygenic traits are often simultaneously influenced by non-additive genetic mechanisms (dominance/epistasis) [10], and while heritability is the main target of focus to improve the performance of a given breed, non-additive genetic effects may play a key role in explaining phenotypic diversity. This is especially important when looking at fitness related traits (e.g., growth, shyness, foraging, predator awareness) in populations that are subjected to domestication, but still occasionally interbreed with their wild conspecifics (e.g., Atlantic salmon, Salmo salar L.). In order to understand the genetic architecture shaping the fitness of wild and domesticated fish as well as their hybrids, it is important to consider all possible types of genetic mechanisms, including dominance and epistasis

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Conclusion