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.

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

“…Within Atlantic salmon, sdY has been mapped to chromosomes Ssa02, Ssa03 and Ssa06 in domesticated and wild strain of salmon from North America and Norway ( Eisbrenner et al, 2014 ; Kijas et al, 2018 ; Besnier et al, 2020 ). It has also been mapped to chromosomes Ssa02 and Ssa21 in six wild Spanish populations ( Gabian et al, 2019 ).…”

“…Over the past decade, we have conducted a number of pedigree-controlled studies on a multiple-generation experimental population of domesticated and wild Atlantic salmon and their crosses at the aquaculture facility owned by the Institute of Marine Research located in Matre, western Norway ( Solberg et al, 2013 , 2014 ; Ayllon et al, 2015 ; Harvey et al, 2016 , 2018 ; Glover et al, 2018 , 2020 ; Perry et al, 2019 ; Besnier et al, 2020 ). The reader is directed to these publications for full details regarding the standard rearing conditions experienced in this fish farm.…”

“…The final dataset for mapping included 109 genome-wide distributed SNPs once those displaying poor coverage and clustering were removed. The list of SNPs are available elsewhere ( Besnier et al, 2015 , 2020 ) and their genomic location can be retrieved from the article describing the Atlantic salmon linkage map ( Lien et al, 2011 ).…”

Sex determining gene transposition as an evolutionary platform for chromosome turnover

“…Within Atlantic salmon, sdY has been mapped to chromosomes Ssa02, Ssa03 and Ssa06 in a domesticated strain of salmon originating from North America, and, in both wild and domesticated Norwegian strains (Eisbrenner et al 2014;Kijas et al 2018;Besnier et al 2020).…”

Big fish, little fish: a multi-omics investigation of growth traits in silver trevally (Pseudocaranx georgianus – araara)

“…For this reason the location and effects of detected QTLs can vary between mapping populations. For example, in the Atlantic salmon, QTLs involved in growth have been found on different linkage groups according to different studies (Baranski et al, 2010;Besnier et al, 2020;Tsai et al, 2015).…”