The plasticity of lifespan in social insects

Abstract

One of the central questions of ageing research is why lifespans of organisms differ so tremendously among related taxa and, even more surprising, among members of the same species. Social insects provide a particularly pronounced example for this. Here, we review previously published information on lifespan plasticity in social insects and provide new data on worker lifespan in the ant Cardiocondyla obscurior , which because of its relatively short lifespan is a convenient model to study ageing. We show that individual lifespan may vary within species with several reproductive and social traits, such as egg-laying rate, queen number, task, colony size and colony composition. For example, in Cardiocondyla , highly fecund queens live longer than reproductively less active queens, and workers tend to live longer when transferred into a novel social environment or, as we show with new data, into small colonies. We hypothesize that this plasticity of lifespan serves to maximize the reproductive output of the colony as a whole and thus the inclusive fitness of all individuals. The underlying mechanisms that link the social environment or reproductive status with lifespan are currently unresolved. Several studies in honeybees and ants indicate an involvement of nutrient-sensing pathways, but the details appear to differ among species. 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?

“…A role for peroxiredoxins also became evident in several other transcriptome studies in this volume [30,32,33]. Furthermore, Quigley & Amdam [49] also stress the importance of social interactions in modulating senescence in humans, similar to what has been shown in social insects and social rodents [33,40,43,46,47].…”

“…For example, in honeybees, winter bees in colonies without brood live much longer than bees in summer [14], and a similar life extension has been observed in tropical honeybees during the wet season when floral resources are scarce [39]. Heinze & Giehr [40] review how variation in queen number, the onset of foraging, colony composition and, as previously shown in honeybees [41], colony size affect individual longevity. They also emphasize that changes in the tempo of ageing associated with the switch from nursing to foraging can be reversed (see also [14,42]).…”

“…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].…”

“…Similarly, highly fecund queens of Cardiocondyla ants live longer than queens that lay only a few eggs per week [59]. It is presently debated whether this link between reproduction and longevity simply means that individuals developing into reproductives a priori have a higher innate quality than those remaining helpers [50,60] or whether reproduction itself and, for example, the higher care received from others trigger longer life [40]. There is support for both hypotheses, and they are not mutually exclusive.…”

Biomarkers in a socially exchanged fluid reflect colony maturity, behavior, and distributed metabolism

“…If molecules dealing with oxidative stress, or beneficial products of metabolism (nutrient storage proteins) can be spread over the circulatory system, as our results show, certain individuals may bear the costs that others in the network incur. This could account for some of the puzzling results on the plasticity of senescence in social insects ( Kramer et al, 2021 ; Heinze and Giehr, 2021 ; Lucas et al, 2019 ), and provides a new perspective to analyze the regulatory changes of social insect reproductive castes with regard to ageing ( Korb et al, 2021 ; Negroni et al, 2019 ; Elsner et al, 2018 ; Corona et al, 2005 ; Gstöttl et al, 2020 ; Corona et al, 2016 ; von Wyschetzki et al, 2015 ). While most previous work has focused almost exclusively on gene expression, we show that for species that engage in trophallaxis, expression studies are necessary but insufficient to understand where in the colony the relevant genes act.…”