Histone acetylation regulates the expression of genes involved in worker reproduction and lifespan in the ant Temnothorax rugatulus

Abstract

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.

Ant phylogenomics reveals a natural selection hotspot preceding the origin of complex eusociality

“…Functional enrichment analyses for the formicoid branch revealed that histone acetylation was the most significantly over-represented function among the 110 positively selected genes. Histone acetylation is well-known for controlling transcriptional activity 23 , reprograming foraging behaviour of the major worker caste into the minor worker caste 24 , colony activity rhythms 25 , and the longevity/fecundity trade-off in workers 26 . Histone acetylation is also involved in caste determination of honeybees through the effect of royal jelly 27 and has been identified as a key caste-specific enhancer of transcription regulating the differential larval development of queens and workers 28 .…”

Queen loss fails to elicit physiological and transcriptional responses in workers of the invasive garden antLasius neglectus

“…Queenless workers in other ants were also typically longer lived or more stress resistant than workers with queen (Majoe et al, 2021;Choppin, 2022;, possibly because molecular pathways for egg production also affect body maintenance. For instance, the egg yolk precursor vitellogenin protects honeybee workers from oxidative stress (Münch & Amdam, 2010).…”