Evolutionary consequences of DNA methylation in a basal metazoan

Gene body methylation (gbM) is an ancestral and widespread feature in Eukarya, yet its adaptive value and evolutionary implications remain unresolved. The occurrence of gbM within protein coding sequences is particularly puzzling, because methylation causes cytosine hypermutability and hence is likely to produce deleterious amino acid substitutions. We investigate this enigma using an evolutionarily basal group of Metazoa, the stony corals (order Scleractinia, class Anthozoa, phylum Cnidaria). We show that gbM correlates with breadth and abundance of transcription and with slow sequence evolution. We also show a strong correlation between gbM and codon bias due to systematic replacement of CpG bearing codons. We suggest that the ancestral function of gene body methylation is tied to selective pressure for accurate and stable gene expression, and that mutation caused by gbM may be a previously unrecognized driver of adaptive codon evolution.