Zugzwang: Elevated histone acetylation in termite queens enhances queen phenotype while accelerating senescence signals

Social insects are prime examples of polyphenism as individuals with the same genetic background develop into different castes. Compared to the workers, the queens of termites are characterized by long lifespan, increased juvenile hormone (JH) signaling and queen-specific cuticular hydrocarbons (CHCs). We hypothesized that such queen-specific traits are under epigenetic control via histone acetylation and tested this in the drywood termite Cryptotermes secundus. Using RNA interference (RNAi), we silenced the histone deacetylase 3 (HDAC3) gene in young, fertile C. secundus queens and analyzed transcriptomes of their fat bodies. We revealed upregulation of transposable elements (TEs) and TE-defence genes, typical of old termite queens, as well as genes associated with JH signaling and CHC biosynthesis pathways. To test for a phenotypic effect, we re-did the experiment and analyzed the CHC profiles using GC-MS. We observed an increase in the proportion of CHCs typical of queens and a decrease of worker-CHCs after HDAC3 silencing. Our results suggest a role for HDAC3 in the regulation of JH signaling, CHC biosynthesis and longevity.