Contrasting DNA methylation responses of inbred fish lines to different rearing environments

Abstract

Epigenetic mechanisms generate plastic phenotypes that can become locally adapted across environments. Disentangling genomic from epigenomic variation is challenging in sexual species due to genetic variation among individuals, but it is easier in self-fertilizing species. We analysed DNA methylation patterns of two highly inbred strains of a naturally self-fertilizing fish reared in two contrasting environments to investigate the obligatory (genotype-dependent), facilitated (partially depend on the genotype) or pure (genotype-independent) nature of the epigenetic variation. We found higher methylation differentiation between genotypes than between environments. Most methylation differences between environments common to both strains followed a pattern where the two genotypes (inbred lines) responded to the same environmental context with contrasting DNA methylation levels (facilitated epialleles). Our findings suggest that, at least in part, DNA methylation could depend on the dynamic interaction between the genotype and the environment, which could explain the plasticity of epigenetically mediated phenotypes.

Prospects for incorporation of epigenetic biomarkers in human health and environmental risk assessment of chemicals

“…Despite this topic being almost unexplored, Berbel‐Filho et al . () recently analysed the DNAm patterns of two highly inbred strains of a naturally self‐fertilising fish reared in two contrasting environments, in order to understand the obligatory (genotype dependent), facilitated (partially genotype dependent) or pure (genotype independent) nature of epigenetic variation. Their results showed higher methylation differences between genotypes than between environments, suggesting that in some cases genotypes have an overriding influence on DNAm patterns.…”

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

“…Using data from all sampling sites, we found that genome‐wide DNA methylation was strongly influenced by selfing lineage, and only at a smaller scale by inbreeding through its interaction with selfing lineage (Bell et al, ; Bjornsson et al, ; Dubin et al, ; Gertz et al, ). Strong epigenetic differences between selfing lines had been identified previously in K. marmoratus (Berbel‐Filho et al, ; Ellison et al, ), indicating an important role of the genetic background in the epigenetic variation of mangrove killifishes. In addition, we also found a significant correlation between DNA methylation and genetic variation (at both AFLP and microsatellites data), suggesting that autonomous variation in DNA methylation may be limited (Dubin et al, ).…”

“…DNA methylation is the best characterized epigenetic modification (Lea, Vilgalys, Durst, & Tung, ) and has important roles on pretranscriptional control in several biological processes, such as cell differentiation and genomic imprinting (Koch et al, ). Variation in DNA methylation is not completely independent from the genome, and epialleles can have different degrees of autonomy from the genotype (Berbel‐Filho, Rodríguez‐Barreto, Berry, Garcia de Leaniz & Consuegra, ; Richards ; Dubin et al, ; Leung, Breton, & Angers, ). In addition, in some plants and animals, individuals with low levels of heterozygosity display high levels of genome‐wide DNA methylation variation (Liebl, Schrey, Richards, & Martin, ; Richards, Schrey, & Pigliucci, ; Schrey et al, ), suggesting that DNA methylation could contribute to the adaptation of organisms with limited genetic diversity to environmental change (Castonguay & Angers, ; Douhovnikoff & Dodd, ; Liebl et al, ; Schrey et al, ; Verhoeven & Preite, ).…”

Genome-wide DNA methylation of the liver reveals delayed effects of early-life exposure to 17-α-ethinylestradiol in the self-fertilizing mangrove rivulus

“…The percentage of CpG covered in the RR genome reached 6.1% of the total number of genomic CpGs, which was similar to mouse and zebrafish (7.0% and 5.3%, respectively, (Chatterjee et al, 2013)), but higher than what other studies reported for diverse fish species such as stickleback [1% (Metzger & Schulte, 2017)], Atlantic salmon [2.75% (Uren Webster et al, 2018)], rainbow trout [<1% (Baerwald et al, 2016)] and guppies [1.5-2% (Hu et al, 2018)]. In mangrove rivulus brain, Berbel-Filho et al (Berbel-Filho et al, 2019b) also reported a lower CpG coverage at 1.2%. This is surprising considering that different tissues of the same species usually show the same methylation profile (Zhang, Hoshida, & Sadler, 2016), and methodological aspects can not be rejected to explain this discrepancy.…”