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

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, likely 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 suggests 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.