Social insects are models for the evolution of phenotypic plasticity. Social insect workers specialise on specific tasks. This division of labour is an adaptive trait that largely contributes to the ecological success of their societies. Task specialisation is neither genetically determined nor rigid, but changes with age and in response to colony needs. Typically, young workers take over brood care and older workers focus on risky outside tasks such as foraging. We could show that gene expression is often more linked to task than to age (Kohlmeier et al. 2018) and histone acetylation can regulate worker behaviour in ants (Libbrecht et al. 2020, see also Simola et al. 2016). Further regulatory mechanisms, such as other histone modifications, microRNAs or DNA Methylation could also be involved and may interact in regulating division of labour. We aim to understand how these regulatory processes respond to external cues, the expression of what kind of genes they alter and how fast these can change their expression. We have focussed on ant Temnothorax longispinosus with its small colonies and long-lived workers to investigate division of labour, the expression and functions of task-specific genes, and the importance of histonemodifications for their expression. Theory posits that task switching requires shifts in responsiveness to task-related cues. We identified a candidate gene, vg-like A, that regulates task allocation and social cue responsiveness (Kohlmeier et al. 2018): Once knocked down via RNAi, young workers reduce brood- but increase nestmate care, a behaviour typical for older workers. This was accompanied by a shift in worker responsiveness from brood to adult worker odorant cues. Our newest results reveal that gene expression in the antennae - the organ of odorant perception – differs more than eight times as strongly between brood carers and foragers than brain transcriptomes, indicating the importance of the peripheral nervous system for the regulation of division of labour. The administration of histone acetyltransferase (HAT) inhibitors impeded the switch of foragers back to brood care, but promoted the reverse change from brood care to foraging. HAT inhibition did not affect workers continuing to execute the same tasks, pointing to the role of histone acetyltransferase in altering gene expression. HAT activity keeps young workers in a “brood caring mode”, possibly to prevent them from leaving the nest prematurely. We established a ChIP-seq protocol and identified histones with worker task-specific acetylation in the brain, which are associated with differentially expressed genes. We also obtained microRNA sequences, which we currently analyse to detect differences between worker castes and their link to brain gene expression.
PhD project: Studying the role of gene regulation in the division of labour in ants
We now will deepen our understanding of the molecular regulation of division of labour in ants by experimentally influencing gene regulation using various epigenetic inhibitors, followed by behavioural, transcriptome and epigenetic readouts. For the latter, we will focus on ChIP-seq and CUT&RUN), DNA methylation (Bisulfite-Seq) and miRNA to link regulatory mechanisms to the behavioural phenotype and gene expression (RNAseq). Not only are we interested in how fast these epigenetic processes work and how they interact, but also which tissues play a major role. This could be the antenna, where social cues are perceived or the mushroom body or antennal lobes of the brain, where information is processed. Peter Baumann and Susanne Gerber will continue to contribute their expertise on Chip Seq and bioinformatic analysis. This project is linked to other projects investigating multiple regulatory mechanisms, their interactions and dynamics and their link to an organismic phenotype.
Publications relevent to this project
Libbrecht, R, Nadrau D., Foitzik, S. (2020) A role of histone acetylation in the regulation of circadian rhythm in ants. IScience, 23: 100846 Kohlmeier P, Feldmeyer B and Foitzik S. (2018). Vitellogenin-like A associated shifts in social cue responsiveness regulate behavioral task specialization in an ant. PLOS Biol, 16: e2005747.
Kohlmeier, P., Alleman, A., Libbrecht, R., Foitzik S.* Feldmeyer, B.*, (2019) Gene expression is more strongly associated with behavioural specialization than with age or fertility in ant workers. Molecular Ecology, 28: 658-670.
Simola DF, Graham RJ, Brady CM, … Berger SL. (2016). Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science, 351.