Genome‐wide methylation in the panmictic European eel (Anguilla anguilla)

Abstract

The role of methylation in adaptive, developmental and speciation processes has attracted considerable interest, but interpretation of results is complicated by diffuse boundaries between genetic and non‐genetic variation. We studied whole genome genetic and methylation variation in the European eel, distributed from subarctic to subtropical environments, but with panmixia precluding genetically based local adaptation beyond single‐generation responses. Overall methylation was 70.9%, with hypomethylation predominantly found in promoters and first exons. Redundancy analyses involving juvenile glass eels showed 0.06% and 0.03% of the variance at SNPs to be explained by localities and environmental variables, respectively, with GO terms of genes associated with outliers primarily involving neural system functioning. For CpGs 2.98% and 1.36% of variance was explained by localities and environmental variables. Differentially methylated regions particularly included genes involved in developmental processes, with Hox clusters featuring prominently. Life stage (adult versus glass eels) was the most important source of inter‐individual variation in methylation, probably reflecting both ageing and developmental processes. Demethylation of transposable elements relative to pure European eel was observed in European X American eel hybrids, possibly representing postzygotic barriers in this system characterized by prolonged speciation and ongoing gene flow. Whereas the genetic data are consistent with a role of single‐generation selective responses, the methylation results underpin the importance of epigenetics in the life cycle of eels and suggest interactions between local environments, development and phenotypic variation mediated by methylation variation. Eels are remarkable by having retained eight Hox clusters, and the results suggest important roles of methylation at Hox genes for adaptive processes.

Epigenetic patterns in Atlantic herring (Clupea harengus): Temperature and photoperiod as environmental stressors during larval development

“…We documented the global methylation level of fall spawning Atlantic herring at early stages of development (average 74.07% for 2019 and 72.03% for 2020) which is comparable to reported global methylation levels in fishes across different life stages [e.g. 1-monthold stickleback: 70.3% (Metzger & Schulte, 2018); adult zebrafish: 80.3% (Feng et al, 2010); juvenile and adult European eel: 70.9% (Liu et al, 2022)]. We then assessed the impact on the methylome of environmental stressors in the form of changes in temperature and photoperiod during incubation and early developmental stages.…”

The role of salinity on genome‐wide DNA methylation dynamics in European sea bass gills

“…In mammals, Brenet et al (2011) have established a negative correlation between DNA methylation and gene expression in the first exon, and this correlation was stronger than between promoter DNA methylation and gene expression. Similar investigations have later been done in fish (Anastasiadi et al, 2018; Liu et al, 2022). The functional role of DNA methylation in different genomic contexts is worth considering and requires further investigations in different species, tissues and environmental conditions.…”

“…An inverse correlation between gene expression and DNA methylation levels was found in promoters, first introns and first exons at both salinities, with very similar correlation coefficients when considering both salinity treatments separately. This inverse correlation has previously been highlighted by Anastasiadi et al (2018), who compared DNA methylation levels in muscles and testes of D. labrax , and later by Liu et al (2022) in Anguilla anguilla muscles for first exons. The presence of unmethylated CpG islands in the proximity of the TSS is consistent with the role of first introns and first exons in the regulation of gene expression.…”

“…by Anastasiadi et al (2018), who compared DNA methylation levels in muscles and testes of D. labrax, and later by Liu et al (2022) in Anguilla anguilla muscles for first exons. The presence of unmethylated CpG islands in the proximity of the TSS is consistent with the role of first introns and first exons in the regulation of gene expression.…”

Panmixia in the American eel extends to its tropical range of distribution: Biological implications and policymaking challenges

“…Phenotype, life history, and behavior of American eel changes with both latitude and habitat (Cairns et al., 2008; Jessop, 2010; Laflamme et al., 2012). Confirmation of panmixia across the entire species' range suggests that within‐generation habituation to local conditions is driven by spatially varying selection (polygenic selection within each generation; Babin et al., 2017; Gagnaire et al., 2012; Laporte et al., 2016; Pavey et al., 2015; reviewed in Pujolar et al., 2022), epigenetic adaptation (Liu et al., 2022), and/or habitat choice (Mensinger et al., 2021), alone or in synergy. In the absence of a genetic basis for these local differences, it can be expected that for genotypically determined traits, American eel individuals will react similarly to environmental cues range‐wide.…”