Caste-biased genes in a subterranean termite are taxonomically restricted: implications for novel gene recruitment during termite caste evolution

Abstract

The caste system of social insects presents a classic polyphenism in which widely divergent reproductive and non-reproductive phenotypes are expressed from the same genome. In termites, the sterile soldier caste is particularly divergent in phenotype and presumably evolved under selection for defensiveness. In this study, we use genomic phylostratigraphy to show that genes with soldier- and other caste-biased expression from the Eastern subterranean termite Reticulitermes flavipes are more taxonomically restricted on the tree of life than genes with no caste-biased expression. This pattern suggests that caste-biased genes are relatively young and implies past selection for novel gene recruitment during termite caste evolution. Moreover, a soldier-biased set of 74 genes contains a higher proportion of orphan genes with no known homology than does a nymph-biased set or any null gene sets. This again suggests that the termite caste—and soldiers in particular—makes disproportionate use of evolutionarily novel genes that are potentially recruited from non-coding regions of the genome. Given that Reticulitermes and most termite soldiers are sterile, any past selection for genetic novelty of this caste must have been indirect and mediated through reproducing relatives.