Differential Selection on Caste-Associated Genes in a Subterranean Termite

SIMPLE SUMMARY: Social insects can sometimes boldly invade new habitats, including areas of human habitation where they can become unwanted domestic or agricultural pests. In this study, we use molecular sequence analysis to study genetic patterns associated with the invasion and division of labour in the Eastern subterranean termite Reticulitermes flavipes. By studying how genes vary by caste and by population, we show that even termites invasive to a metropolitan city can still harbour plenty of genetic variation, as much or more as native termite populations. We suggest therefore that invasive termites do not necessarily suffer long term loss-of-variation upon invasion. Second, we show that genes associated in their expression with the soldier caste evolve approximately twice as fast as genes expressed by other castes of this species, regardless of from what population the castes were sampled. Why termite soldier genes evolve quickly is not known, but it seems unrelated to invasion or the invaded habitat. Given that soldiers are sterile and thus have no direct fitness, the evidence for gene-level selection in the soldier caste is an intriguing example of kin selection. ABSTRACT: Analyzing the information-rich content of RNA can help uncover genetic events associated with social insect castes or other social polymorphisms. Here, we exploit a series of cDNA libraries previously derived from whole-body tissue of different castes as well as from three behaviourally distinct populations of the Eastern subterranean termite Reticulitermes flavipes. We found that the number (~0.5 M) of single nucleotide variants (SNVs) was roughly equal between nymph, worker and soldier caste libraries, but d(N)/d(S) (ratio of nonsynonymous to synonymous substitutions) analysis suggested that some of these variants confer a caste-specific advantage. Specifically, the d(N)/d(S) ratio was high (~4.3) for genes expressed in the defensively specialized soldier caste, relative to genes expressed by other castes (~1.7–1.8) and regardless of the North American population (Toronto, Raleigh, Boston) from which the castes were sampled. The populations, meanwhile, did show a large difference in SNV count but not in the manner expected from known demographic and behavioural differences; the highly invasive unicolonial population from Toronto was not the least diverse and did not show any other unique substitution patterns, suggesting any past bottleneck associated with invasion or with current unicoloniality has become obscured at the RNA level. Our study raises two important hypotheses relevant to termite sociobiology. First, the positive selection (d(N)/d(S) > 1) inferred for soldier-biased genes is presumably indirect and of the type mediated through kin selection, and second, the behavioural changes that accompany some social insect urban invasions (i.e., ‘unicoloniality’) may be detached from the loss-of-diversity expected from invasion bottlenecks.