Training the salmon's genes: influence of aerobic exercise, swimming performance and selection on gene expression in Atlantic salmon

Abstract

Background: Farmed and wild Atlantic salmon are exposed to many infectious and non-infectious challenges that can cause mortality when they enter the sea. Exercise before transfer promotes growth, health and survival in the sea. Swimming performance in juveniles at the freshwater parr stage is positively associated with resistance to some diseases. Genetic variation is likely to affect response to exercise. In this study we map genetic differences associated with aerobic exercise, swimming performance and genetic origin. Eggs from the selectively bred Bolaks salmon and wild Lærdal River salmon strains were reared until parr in a common environment. Swimming performance was assessed by subjecting the fish to either continuous hard exercise or control conditions for 18 days. Heart was sampled for examination of gene expression using RNA-seq (~60 fish/treatment).

Results: Lower expression of genes affecting immune function was found in domesticated than wild parr. Among wild parr under control exercise the expression of a large number of genes involved in general metabolism, stress and immune response was lower in superior swimmers suggesting that minimisation of energy expenditure during periods of low activity makes parr better able to sustain bursts of swimming for predator avoidance. A similar set of genes were down-regulated with training among wild parr with inferior swimming performance. These parr react to training in a way that their cardiac expression patterns become like the superior performing wild parr under control exercise conditions. Diversifying selection caused by breeding of domesticated stock, and adaptive pressures in wild stock, has affected the expression and frequency of single nucleotide polymorphisms (SNPs) for multiple functional groups of genes affecting diverse processes. SNPs associated with swimming performance in wild parr map to genes involved in energetic processes, coding for contractile filaments in the muscle and controlling cell proliferation.

Conclusions: Domesticated parr have less phenotypic plasticity in response to training and lower expression of genes with functions affecting immune response. The genetic response to training is complex and depends on the background of parr and their swimming ability. Exercise should be tailored to the genetics and swimming performance of fish.

Keywords: Exercise; Gene expression; Immune function; Natural selection; SNP polymorphisms; Salmo salar; Selective breeding; Swimming performance.

Fig. 1

Source of wild parents for parr used in the study showing the main tributary of the Lærdal River (red) in Norway (inset). The figure was made using altitude raster data (30s resolution) obtained from the WorldClim dataset [78] and the open-source program QGIS v1.8

Fig. 2

Principle component analysis (PCA) of DESeq2 normalised and transformed (regularised-logarithm) read abundance data. Variables: swimming performance (best/superior or poor/inferior); exercise (rested/control or trained) and; source (Bolaks or Lærdal)

Fig. 3

Volcano plots of adjusted P-values (P _adj) and log fold change in expression (log₂FC) of genes in the superior compared to the inferior swimming parr. Separate plots are for wild Lærdal parr under control (a) and trained (b) exercise conditions, and for domesticated Bolaks parr under control (c) and trained (d) exercise conditions. Red points show genes with P _adj < 0.05 while green points show genes with P _adj < 0.05 and log₂FC > 1

Fig. 4

Spiders web plots showing the average differential expression (P _adj < 0.05) of genes in parr subjected to training versus control exercise regimes. Functional categories are grouped according to immune function (a), metabolism (b), cell (c) and tissue (heart, d). Points and joining lines are for wild Lærdal superior performing (green) and wild Lærdal inferior performing (red), domesticated Bolaks superior performing (purple) and domesticated Bolaks inferior performing (yellow) parr. TNF, tumour necrosis factors. IFN, interferon. GTP, guanosine triphosphate

Fig. 5

Heat map of differentially expressed (P _adj < 0.05) functional categories of genes in parr subjected to training versus control exercise regimes. Average log-fold difference in gene expression within each functional category is represented on a colour scale from red (down-expression in the trained parr) to green (up-expression in the trained parr). The heat map is split into domesticated Bolaks and wild Lærdal superior and inferior swimming parr. Numbers of significantly differentially expressed genes in each category are shown

Fig. 6

Volcano plots of adjusted P-values (P _adj) and log fold change in expression (log₂FC) of genes in parr subjected to trained compared to control exercise regimes. Separate plots are for wild Lærdal parr with inferior (a) and superior (b) swimming performance, and for domesticated Bolaks parr with inferior (c) and superior (d) swimming performance. Red points show genes with P _adj < 0.05 while green points show genes with P _adj < 0.05 and log₂FC > 1

Fig. 7

Heat map of differentially expressed (P _adj < 0.05) functional categories of genes in the superior versus the inferior swimming parr. Average log-fold difference in gene expression within each functional category is represented on a colour scale from red (down-expression in the superior swimming performers) to green (up-expression in the superior swimming performers). The heat map is split into domesticated Bolaks and wild Lærdal trained and rested (control) parr. Numbers of significantly differentially expressed genes in each category are shown

Fig. 8

Spiders web plots showing the average differential expression (P _adj < 0.05) of genes in the superior versus the inferior swimming parr. Functional categories are grouped according to immune function (a), metabolism (b), cell (c) and tissue (heart, d). Points and joining lines are for wild Lærdal control (green), wild Lærdal trained (red), domesticated Bolaks control (purple) and domesticated Bolaks trained (yellow) parr. TNF, tumour necrosis factors. IFN, interferon. GTP, guanosine triphosphate