Inbreeding effects on gene‐specific DNA methylation among tissues of Chinook salmon

Abstract

Inbreeding depression is the loss of fitness resulting from the mating of genetically related individuals. Traditionally, the study of inbreeding depression focused on genetic effects, although recent research has identified DNA methylation as also having a role in inbreeding effects. Since inbreeding depression and DNA methylation change with age and environmental stress, DNA methylation is a likely candidate for the regulation of genes associated with inbreeding depression. Here, we use a targeted, multigene approach to assess methylation at 22 growth-, metabolic-, immune- and stress-related genes. We developed PCR-based DNA methylation assays to test the effects of intense inbreeding on intragenic gene-specific methylation in inbred and outbred Chinook salmon. Inbred fish had altered methylation at three genes, CK-1, GTIIBS and hsp70, suggesting that methylation changes associated with inbreeding depression are targeted to specific genes and are not whole-genome effects. While we did not find a significant inbreeding by age interaction, we found that DNA methylation generally increases with age, although methylation decreased with age in five genes, CK-1, IFN-ɣ, HNRNPL, hsc71 and FSHb, potentially due to environmental context and sexual maturation. As expected, we found methylation patterns differed among tissue types, highlighting the need for careful selection of target tissue for methylation studies. This study provides insight into the role of epigenetic effects on ageing, environmental response and tissue function in Chinook salmon and shows that methylation is a targeted and regulated cellular process. We provide the first evidence of epigenetically based inbreeding depression in vertebrates.

Higher-order organisation of extremely amplified, potentially functional and massively methylated 5S rDNA in European pikes (Esox sp.)

“…Indeed, 5S genes in both E. lucius and E. cisalpinus were heavily methylated at CG motifs suggesting that a powerful epigenetic system has evolved in this genus. There were no apparent differences in methylation levels between different tissues reported in other systems [55] suggesting that most genes are evenly methylated. However, our restriction enzyme-based methylation assay reveals global level of 5S rDNA methylation while its resolution is unable to detect changes at the single gene level.…”

DNA methylation in adults and during development of the self‐fertilizing mangrove rivulus, Kryptolebias marmoratus

“…If this mechanism happens in K. marmoratus together with a deep, late, and long reprogramming event, thus, elucidation of the epigenetic mark transmission, and of the potential impact of embryonic demethylation on inbreeding depression limitation (Vergeer, Wagemaker, & Ouborg, ), might provide clues about the evolutionary pathways leading to this mix‐mating system and differences in selfing rates reported among natural populations. Stability of this mixed mating system is indeed possibly linked to the magnitude of inbreeding depression that is affected by environmental conditions (Cheptou & Donohue, ), and self‐fertilization increases homozygosity with, in consequences, the fitness reduction of individuals (Venney, Johansson, & Heath, ). However, in K .…”

“…Stability of this mixed mating system is indeed possibly linked to the magnitude of inbreeding depression that is affected by environmental conditions (Cheptou & Donohue, 2013), and self-fertilization increases homozygosity with, in consequences, the fitness reduction of individuals (Venney, Johansson, & Heath, 2016). However, in K. marmoratus, selfing maintain locally well-adapted genotype and the study of this unique reprogramming pattern might be a key to explore.…”

Local parasite pressures and host genotype modulate epigenetic diversity in a mixed‐mating fish

“…Higher variation in DNA methylation has been reported for clonal and inbred individuals (Liebl et al, ; Massicotte & Angers, ; Nakamura & Hosaka, ; Richards et al, ; Veerger et al, ) and has been interpreted as an adaptive mechanism to compensate for low genetic variation (Schrey et al, ), or as a potential consequence of inbreeding (as in Vergeer, Wagemaker, & Ouborg, ) responsible, at least in part, for inbreeding depression (Nakamura & Hosaka, ; Vergeer et al, ). Yet, our results suggest that, at least in this species, either inbreeding does not affect genome‐wide DNA methylation variation or it does in a gene‐specific manner (Venney, Johansson, & Heath, ), although further research would be needed to address this question.…”