Pervasive relaxed selection in termite genomes

Abstract

Genetic changes that enabled the evolution of eusociality have long captivated biologists. More recently, 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 analysed nine genomes, including newly sequenced genomes from three non-eusocial cockroaches. Using a phylogenomic approach, we found that termite genomes have experienced lower rates of synonymous substitutions than those of cockroaches, possibly as a result of longer generation times. We identified higher rates of non-synonymous substitutions 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 reductions 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 of deleterious alleles at the colony level. Additionally, we identified genomic adaptations that may underpin caste differentiation, 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.

Keywords: Blattodea; effective population size; eusociality; indirect selection; phylogenomics; relaxed selection.

Figure 1.

(a) Density plot for the three-ratio d_N/d_S model for the cockroaches and termites. (b) Proportion of genes under significant relaxed selection for each of the focal branches based on the RELAX analyses (after Holm–Bonferroni correction). (c) Phylogenetic tree of analysed termite and cockroach genomes (genomes generated in this study in bold), with branches coloured by their median relaxed selection parameter (k) determined using RELAX, whereby k < 1 indicates relaxed selection and k > 1 indicates intensified selection (the outgroup has been pruned from the tree). (d) Venn diagram displaying overlapping orthologues under relaxed selection on the termite terminal branches.

Figure 2.

(a) Proportion of orthologues (n = 1491) on various branches undergoing positive selection, determined using aBSREL analyses (see electronic supplementary material, table S6, for names of genes undergoing positive selection in termite taxa). (b) Number of gene expansions (green) and contractions (red) on each branch of the cockroach/termite tree (see electronic supplementary material, table S7, for names of genes that had significant expansions/contractions in termite taxa). The number of gene expansions/contractions combined results from the small and large orthogroups analysed.