Pervasive relaxed selection in termite genomes

Abstract

The genetic changes that enabled the evolution of eusociality have long captivated biologists. In recent years, attention has focussed on the consequences of eusociality on genome evolution. Studies have reported higher molecular evolutionary rates in eusocial hymenopteran insects compared with their solitary relatives. To investigate the genomic consequences of eusociality in termites, we sequenced genomes from three of their non-eusocial cockroach relatives. Using a phylogenomic approach, we found that termite genomes experienced lower rates of synonymous mutations than those of cockroaches, possibly as a result of longer generation times. We identified higher rates of nonsynonymous mutations in termite genomes than in cockroach genomes, and identified pervasive relaxed selection in the former (24-31% of the genes analysed) compared with the latter (2-4%). We infer that this is due to a reduction in effective population size, rather than gene-specific effects (e.g., indirect selection of caste-biased genes). We found no obvious signature of increased genetic load in termites, and postulate efficient purging at the colony level. Additionally, we identified genomic adaptations that may underpin caste formation, such as genes involved in post-translational modifications. Our results provide insights into the evolution of termites and the genomic consequences of eusociality more broadly.