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 g...

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Main Authors: Francois Besnier, Monica F. Solberg, Alison C. Harvey, Gary R. Carvalho, Dorte Bekkevold, Martin I. Taylor, Simon Creer, Einar E. Nielsen, Øystein Skaala, Fernando Ayllon, Geir Dahle, Kevin A. Glover
Format: Article
Language:English
Published: BMC 2020-02-01
Series:BMC Genetics
Subjects:
Online Access:https://doi.org/10.1186/s12863-020-0816-y
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spelling doaj-3865bdbf60754326a534dd0a71ee73b72021-02-07T12:47:46ZengBMCBMC Genetics1471-21562020-02-0121111710.1186/s12863-020-0816-yEpistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interfaceFrancois Besnier0Monica F. Solberg1Alison C. Harvey2Gary R. Carvalho3Dorte Bekkevold4Martin I. Taylor5Simon Creer6Einar E. Nielsen7Øystein Skaala8Fernando Ayllon9Geir Dahle10Kevin A. Glover11Population Genetics Research group, Institute of Marine ResearchPopulation Genetics Research group, Institute of Marine ResearchPopulation Genetics Research group, Institute of Marine ResearchMolecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor UniversitySection for Marine Living Resources, National Institute of Aquatic Resources, Technical University of DenmarkSchool of Biological Sciences, University of East AngliaMolecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, Bangor UniversitySection for Marine Living Resources, National Institute of Aquatic Resources, Technical University of DenmarkPopulation Genetics Research group, Institute of Marine ResearchPopulation Genetics Research group, Institute of Marine ResearchPopulation Genetics Research group, Institute of Marine ResearchPopulation Genetics Research group, Institute of Marine ResearchAbstract 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.https://doi.org/10.1186/s12863-020-0816-yLinkage mappingGrowthHybridIntrogressionInheritanceNon-additive
collection DOAJ
language English
format Article
sources DOAJ
author Francois Besnier
Monica F. Solberg
Alison C. Harvey
Gary R. Carvalho
Dorte Bekkevold
Martin I. Taylor
Simon Creer
Einar E. Nielsen
Øystein Skaala
Fernando Ayllon
Geir Dahle
Kevin A. Glover
spellingShingle Francois Besnier
Monica F. Solberg
Alison C. Harvey
Gary R. Carvalho
Dorte Bekkevold
Martin I. Taylor
Simon Creer
Einar E. Nielsen
Øystein Skaala
Fernando Ayllon
Geir Dahle
Kevin A. Glover
Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface
BMC Genetics
Linkage mapping
Growth
Hybrid
Introgression
Inheritance
Non-additive
author_facet Francois Besnier
Monica F. Solberg
Alison C. Harvey
Gary R. Carvalho
Dorte Bekkevold
Martin I. Taylor
Simon Creer
Einar E. Nielsen
Øystein Skaala
Fernando Ayllon
Geir Dahle
Kevin A. Glover
author_sort Francois Besnier
title Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface
title_short Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface
title_full Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface
title_fullStr Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface
title_full_unstemmed Epistatic regulation of growth in Atlantic salmon revealed: a QTL study performed on the domesticated-wild interface
title_sort epistatic regulation of growth in atlantic salmon revealed: a qtl study performed on the domesticated-wild interface
publisher BMC
series BMC Genetics
issn 1471-2156
publishDate 2020-02-01
description 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.
topic Linkage mapping
Growth
Hybrid
Introgression
Inheritance
Non-additive
url https://doi.org/10.1186/s12863-020-0816-y
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