Captive rearing effects on the methylome of Atlantic salmon after oceanic migration: Sex-specificity and intergenerational stability

Abstract

Captive rearing in salmon hatcheries can have considerable impacts on both fish phenotype and fitness within a single generation, even in the absence of genetic change. Evidence for hatchery-induced changes in DNA methylation is becoming abundant, though questions remain on the sex-specificity of these effects, their persistence until spawning and potential for transmission to future generations. Here we performed whole genome methylation sequencing of fin tissue for 16 hatchery and 16 wild Atlantic salmon (Salmo salar) returning to spawn in the Rimouski River, Québec, Canada. We identified two cohorts of hatchery-reared salmon through methylation analysis, one of which was epigenetically similar to wild fish, suggesting that supplementation efforts may be able to minimize the epigenetic effects of hatchery rearing. We found considerable sex-specific effects of hatchery rearing, with few genomic regions being affected in both males and females. We also analysed the methylome of 32 F₁ offspring from four groups (pure wild, pure hatchery origin and reciprocal hybrids). We found that few epigenetic changes due to parental hatchery rearing persisted in the F₁ offspring though the patterns of inheritance appear to be complex, involving nonadditive effects. Our results suggest that the epigenetic effects of hatchery rearing can be minimal in F₀. There may also be minimal epigenetic inheritance and rapid loss of epigenetic changes associated with hatchery rearing. However, due to sex-specificity and nonadditive patterns of inheritance, methylation changes due to captive rearing are rather complex and the field would benefit from further research on minimizing the epigenetic effects of captive rearing in conservation efforts.

Keywords: conservation; epigenetics; hatchery rearing; salmonid.

FIGURE 1

PCA plots for methylation data showing (a) differentiation between F₀ hatchery cohorts and wild fish, and (b) lack of whole genome F₁ differentiation based on parental rearing environment.

FIGURE 2

F₀ differential methylation results between hatchery cohorts (“normal” = orange, “wildtype” = brown) and wild salmon (green). We detected (a) 2007 DMRs between wild and “normal” hatchery salmon, (b) 1285 DMRs between “normal” and “wildtype” hatchery cohorts, and (c) only 156 DMRs between the “wildtype” hatchery cohort and wild salmon. Hierarchical clustering was performed based on Euclidean distances. Percentage methylation is denoted by the yellow to indigo scale for each DMR (0%–100%).

FIGURE 3

F₀ sex‐specific DMRs due to rearing environment. We identified (a) 5717 DMRs between male hatchery‐reared and wild salmon, and (b) 2439 DMRs between female salmon.

FIGURE 4

F₁ DMR analysis identified (a) 284 DMRs due to maternal source, (b) 254 DMRs due to paternal source and (c) 271 DMRs due to their interaction.