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In invertebrates that harbor functional DNA methylation enzymatic machinery, gene-bodies are the primary targets for CpG methylation. However, virtually all other aspects of invertebrate DNA methylation have remained a mystery until now. Here, using a comparative methylomics approach, we demonstrate that  Nematostella vectensis ,  Ciona intestinalis ,  Apis mellifera , and  Bombyx mori  show two distinct populations of genes differentiated by gene-body CpG density. Genome-scale DNA methylation profiles for  A. mellifera  spermatozoa reveal CpG-poor genes are methylated in the germline, as predicted by the depletion of CpGs. We find an evolutionarily conserved distinction between CpG-poor and GpC-rich genes: The former are associated with basic biological processes, the latter with more specialized functions. This distinction is strikingly similar to that recently observed between euchromatin-associated genes in  Drosophila  that contain intragenic histone 3 lysine 36 trimethylation (H3K36me3) and those that do not, even though  Drosophila  does not display CpG density bimodality or methylation. We confirm that a significant number of CpG-poor genes in  N. vectensis ,  C. intestinalis ,  A. mellifera , and  B. mori  are orthologs of H3K36me3-rich genes in  Drosophila . We propose that over evolutionary time, gene-body H3K36me3 has influenced gene-body DNA methylation levels and, consequently, the gene-body CpG density bimodality characteristic of invertebrates that harbor CpG methylation.

Comparative methylomics reveals gene-body H3K36me3 in Drosophila predicts DNA methylation and CpG landscapes in other invertebrates