Abstract
Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.
Highlights
Epigenetic variation modulates gene expression and can be heritable
The molecular mechanisms underlying adaptive phenotypic diversification are subject of intense interest[34,36,38,58,59] and the extent of the role of epigenetic processes is hotly debated[2,4,60]
In-depth molecular epigenetic studies remain rare in evolutionary genomics and its key model systems[2,4,29,60]
Summary
Epigenetic variation modulates gene expression and can be heritable. knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. DNA methylation, or the covalent addition of a methyl group onto the 5th carbon of cytosine (mC) in DNA, is a reversible epigenetic mark present across multiple kingdoms[8,9,10], can be heritable, and has been linked to transmission of acquired phenotypes in plants and animals[2,5,6,11,12,13] The importance of this mechanism is underlined by the fact that proteins involved in the deposition of mC (‘writers’, DNA methyltransferases [DNMTs]), in mC maintenance during cell division, and in the removal of mC (‘erasers’, ten-eleven translocation methylcytosine dioxygenases [TETs]), are mostly essential and show high degrees of conservation across vertebrates species[14,15,16,17]. Recent large-scale genetic studies have revealed that the Lake Malawi cichlid flock is characterised by an overall very low genetic divergence among species (0.1−0.25%), combined with a low mutation rate, a high rate of hybridisation and extensive incomplete lineage sorting (shared retention of ancestral genetic variation across species)[34,36,38,39]
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