Soldier-biased gene expression in a subterranean termite implies functional specialization of the defensive caste.

Abstract

In a termite colony, reproduction is typically monopolized by a small number of sexuals that are supported by reproductively altruistic soldiers and workers. We expect caste differentiation to be associated with clear-cut differences in gene expression, and for these differences to reflect caste function and development. Here, we use RNA-Sequencing to compare the gene expression profiles of sexual nymphs and two non-reproductive helper castes (i.e., workers and soldiers) of the Eastern subterranean termite Reticulitermes flavipes. We found that of n = 93 genes that are strictly expressed as a function of caste, a majority (78%) show a soldier-specific pattern. This conspicuous soldier-bias in genome-wide expression suggests that this defensively specialized caste is functionally well-differentiated from both the reproductive and the other non-reproductive caste of this species, despite a shared developmental program with workers. Gene ontology analysis supports the notion of functional specialization by soldiers, as soldier-biased gene sets are enriched for novel biological processes. Whether this pattern reflects ancient or more recent bouts of selection for caste novelty at the gene-regulatory level is not known, but because soldiers are sterile and thus have no direct fitness, any selection for novelty must have been mediated indirectly, through reproducing relatives.