Molecular regulation of lifespan extension in fertile ant workers

Abstract

The evolution of sociality in insects caused a divergence in lifespan between reproductive and non-reproductive castes. Ant queens can live for decades, while most workers survive only weeks to a few years. In most organisms, longevity is traded-off with reproduction, but in social insects, these two life-history traits are positively linked. Once fertility is induced in workers, e.g. by queen removal, worker lifespan increases. The molecular regulation of this positive link between fecundity and longevity and generally the molecular underpinnings of caste-specific senescence are not well understood. Here, we investigate the transcriptomic regulation of lifespan and reproduction in fat bodies of three worker groups in the ant Temnothorax rugatulus . In a long-term experiment, workers that became fertile in the absence of the queen showed increased survival and upregulation of genes involved in longevity and fecundity pathways. Interestingly, workers that re-joined their queen after months exhibited intermediate ovary development, but retained a high expression of longevity and fecundity genes. Strikingly, the queen's presence causes a general downregulation of genes in worker fat bodies. Our findings point to long-term consequences of fertility induction in workers, even after re-joining their queen. Moreover, we reveal longevity genes and pathways modulated during insect social evolution. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

Ageing and sociality: why, when and how does sociality change ageing patterns?

“…Several studies have shown that reproductives live longer than non-reproductives even when they do not differ in ontogeny and morphology, e.g. as in certain species of ants [34,56,57] and reproducing workers of honeybees [58] and ants [37,40,43]. Similarly, highly fecund queens of Cardiocondyla ants live longer than queens that lay only a few eggs per week [59].…”

“…As Negroni et al [43] show, workers of the ant Temnothorax rugatulus, which laid eggs over several months under queenless conditions, do not readily revert to their previous non-reproductive physiology when re-joined with the queen: their transcriptomes suggest that, while their fecundity goes down, they still show signs of increased longevity. In this case, lifespan extension and fertility appear to be reversible only to some extent.…”

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

“…Reproduction has strong effects on the physiology and immunity of workers, who can become more resistant to oxidative stress and often live longer (dos Santos Conceição Lopes, Campbell, & Contrera, 2020;Kohlmeier et al, 2017;Majoe, Libbrecht, Foitzik, & Nehring, 2021;Negroni, Segers, Vogelweith, & Foitzik, 2020). These positive effects of reproduction have been linked to the activation of signaling pathways such as insulin/insulin-like growth factor (IIS), the target of rapamycin (mTOR), and the alpha-ketoglutarate (alpha-KG) (Negroni, Macit, Stoldt, Feldmeyer, & Foitzik, 2021). Indeed, gene expression changes profoundly in workers after queen loss in social wasps (Taylor, Cini, Sumner, Wyatt, & Reuter, 2021), honeybees (Cardoen et al, 2011), and ants (Negroni et al, 2021;Wurm, Wang, & Keller, 2010) and in various tissues from the brain to the fat body.…”

“…These positive effects of reproduction have been linked to the activation of signaling pathways such as insulin/insulin-like growth factor (IIS), the target of rapamycin (mTOR), and the alpha-ketoglutarate (alpha-KG) (Negroni, Macit, Stoldt, Feldmeyer, & Foitzik, 2021). Indeed, gene expression changes profoundly in workers after queen loss in social wasps (Taylor, Cini, Sumner, Wyatt, & Reuter, 2021), honeybees (Cardoen et al, 2011), and ants (Negroni et al, 2021;Wurm, Wang, & Keller, 2010) and in various tissues from the brain to the fat body. Similarly, gene expression differs between reproductive and sterile bumblebee workers (Marshall, Lonsdale, & Mallon, 2019).…”

“…Queens can live over ten years and their gene expression in the brain and fat body changes with age (Negroni, Foitzik, & Feldmeyer, 2019). Following queen loss, T. rugatulus workers are known to develop their ovaries, start laying haploid eggs, live longer, and show transcriptomic changes in the fat body, a physiologically active tissue (Negroni et al, 2021(Negroni et al, , 2020. Here, we asked whether histone acetylation is required for workers to plastically respond to queen loss by altering their ovary development and associated gene expression.…”