Social insects form complex societies with division of labor between different female castes. In most species, a single queen heads the colony; in others, several queens share the task of reproduction. These different social organizations are often associated with distinct queen morphologies and life history strategies and occur in different environments. In the ant Temnothorax rugatulus, two queen morphs - macrogynes and microgynes - exist associated with mono- and polygynous colonies, respectively, which occur at lower and higher elevations. We analyzed plastic changes in brain transcriptomes in response to the social environment in these queen morphs and their workers. We manipulated the number of queens over several weeks to investigate whether transcriptional activity is influenced by queen morph, social environment, or their interaction. Changes in gene expression in the queens’ brains in response to our manipulations were subtle and largely influenced by the interaction between social environment and queen morph, rather than independently by these factors. Macrogynes and microgynes thus adjust differently to their social environment. Similarly, worker transcriptomes were influenced by an interaction between behavioral type, i.e., nurses or foragers, and queen morph. Nurses differentially regulated genes related to nutrition depending on queen morph, suggesting a link between social environment and metabolic dynamics in ant colonies. Overall, our study shed light on how the social environment influences the molecular physiology of social insects. Furthermore, we demonstrate that in this ant with two queen morphs, worker physiology depends on queen morph and their role in the colony.

In insect societies, the queen monopolizes reproduction while workers perform tasks such as brood care or foraging. Queen loss leads to ovary development and lifespan extension in workers from many ants. However, the underlying molecular mechanisms of this phenotypic plasticity remain unclear. Recent studies highlight the importance of epigenetics in regulating plastic traits in social insects. We investigated the role of histone acetylation in the regulation of worker reproduction in the ant Temnothorax rugatulus. We removed queens from their colonies to induce worker fecundity, and either fed workers with chemical inhibitors of histone acetylation (C646), deacetylation (Trichostatin A), or the solvent (DMSO) as control. We monitored worker number for six weeks after which we assessed ovary development and sequenced fat body mRNA. Workers survived better in queenless colonies and developed their ovaries after queen removal in control colonies as expected, but not in colonies treated with chemical inhibitors. Both inhibitors affected gene expression, although the inhibition of histone acetylation using C646 influenced the expression of more genes with immunity, fecundity, and longevity functionalities. Interestingly, these C646-treated workers shared many upregulated genes with infertile workers from queenright colonies. We also identified one gene with antioxidant properties commonly downregulated in infertile workers from queenright colonies and both C646 and TSA-treated workers from queenless colonies. Our results indicate that histone acetylation is involved in the molecular regulation of worker reproduction and lifespan, and thus point to an important role of histone modifications in modulating phenotypic plasticity of life history traits in social insects.