The hundreds of cichlid species forming part of the radiation of East African Lakes show a remarkable diversity of phenotypic and ecological adaptation. Despite this, recent studies highlighted that genetic diversity within the radiation is among the lowest ever observed in vertebrates.

Such a high phenotype/genotype diversity ratio makes cichlids a promising system to investigate the role of genetics and, for the first time at a species level, epigenetics in the context of adaptation and convergent evolution. Yet, the molecular mechanisms and, in particular, any epigenetic aspects underlying such phenotypic diversity and speciation success remain largely unknown.

Here, I focus on whole-genome DNA methylation (methylome), a heritable and dynamic epigenetic mark that has been reported to be responsible for rapid and transmissible changes in phenotype in plants and mammals. In light with phenotypic plasticity related to diet adaptation, I hypothesise that the liver methylome may affect liver function and thus be related to diet. I thus performed sequencing of liver tissues of different cichlid species presenting distinct eco-morphological and trophic adaptation from both Lake Malawi and crater lake Massoko, Tanzania.

The main results reveal striking differences in methylome at conserved underlying DNA sequences – some variation shared in cichlids of both lakes. Furthermore, I observe an enrichment for methylome variation in transposable elements (TE) and promoter regions. Remarkably, most of the variation (ca 80%) common to fishes from both lakes are located in TEs and is, in part, correlated with differential expression levels at some key metabolic and developmental genes in liver. This suggests a possible conserved role of TE-related methylome in the adaptation of liver function.

Furthermore, I generated inter-species hybrids to investigate the inheritance of DNAme variation in cichlids. The liver methylome of F1 hybrids, although mostly resembling parental methylomes, exhibited some level of divergence, suggesting unique DNAme patterns in hybrid offspring and possible transgressive segregation.

I conclude there might be a conserved crosstalk between the local environment and methylome in different natural populations of cichlids. The results presented in this thesis postulate an important role of natural DNA methylation variation in promoting adaptive phenotypic diversification in divergent habitats during the early stages of speciation.