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

Marina Choppin,Barbara Feldmeyer,Susanne Foitzik

doi:10.1186/s12864-021-08196-8

Marina Choppin, Barbara Feldmeyer + Show 1 more

Open Access

https://doi.org/10.1186/s12864-021-08196-8

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Abstract

BackgroundIn insect societies, queens monopolize reproduction while workers perform tasks such as brood care or foraging. Queen loss leads to ovary development and lifespan extension in workers of many ant species. 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. Thus, we investigated the role of histone acetylation in regulating 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 (TSA), or the solvent (DMSO) as control. We monitored worker number for six weeks after which we assessed ovary development and sequenced fat body mRNA.ResultsWorkers survived better in queenless colonies. They also developed their ovaries after queen removal in control colonies as expected, but not in colonies treated with the chemical inhibitors. Both inhibitors affected gene expression, although the inhibition of histone acetylation using C646 altered 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.ConclusionOur results suggest that histone acetylation is involved in the molecular regulation of worker reproduction, and thus point to an important role of histone modifications in modulating phenotypic plasticity of life history traits in social insects.

Highlights

In insect societies, queens monopolize reproduction while workers perform tasks such as brood care or foraging
Gene expression and functional enrichment We found 346 differentially expressed genes (DEGs) between workers from the “queenless” and “queenright” groups (Additional file 2), among which 206 were upregulated and 140 downregulated in the queenright group
Effects of chemical inhibitors Worker number, egg production, and fecundity Here we focus on queenless colonies that were either fed with Dimethyl Sulfoxide (DMSO) only as control or treated with C646, Trichostatin A (TSA), or both inhibitors

Summary

Introduction

Queens monopolize reproduction while workers perform tasks such as brood care or foraging. Eusocial insect societies exhibit a reproductive division of labor where one or a few females (often called queens) reproduce, whereas workers perform all other tasks including brood care, nest defense, and foraging [1]. Workers sacrifice their own reproduction and Choppin et al BMC Genomics (2021) 22:871 queenright colonies, social insect workers can circumvent those restraints and successfully gain direct fitness benefits by laying haploid, male-destined eggs [9,10,11,12,13]. The transcriptomic changes linked to worker reproduction have been well characterized, while the underlying gene regulatory mechanisms remain largely unexplored

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