The effect of environmental stress on ageing in a termite species with low social complexity

Abstract

Social insects seem to have overcome the almost universal trade-off between fecundity and longevity as queens can be highly fecund and at the same time reach lifespans of decades. By contrast, their non-reproducing workers are often short-lived. One hypothesis to explain the long lifespan of queens is that they are better protected against stress than their workers. However, evidence is controversial and experimental studies are scarce. We aimed at manipulating environmental stress and ageing by exposing colonies of the less-socially complex termite Cryptotermes secundus to temperature regimes that differed in variance. In contrast with expectation, constant temperatures imposed more stress than variable temperatures. Survival of queens and workers as well as queens' fecundity were partly reduced under constant conditions and both castes showed signs of ageing in the transcriptome signature under constant conditions. There was a clear oxidative stress defence signal under constant conditions that was, surprisingly, stronger for workers than queens. We discuss how our results relate to social complexity. We argue that workers that are totipotent to become reproductives, like in C. secundus , should invest more in ‘anti-ageing' mechanisms than sterile workers because the former can still reproduce and have not reached maturity yet. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

Oxidative stress and senescence in social insects: a significant but inconsistent link?

“…This may be in line with the idea that these workers do not work hard [63] and that workers are totipotent immatures in this species [64]. In fact, a study in which stress was introduced through temperature variation in C. secundus also showed that workers mounted their oxidative stress response by increasing the expression of antioxidant genes under stressful temperature conditions more than queens [65]. This was explained by the fact that, as wood-dwelling, one-piece nesters, C. secundus workers are totipotent immatures that are selected to invest in body maintenance as they have not reached maturity yet.…”

“…This again highlights the view that reproductive division of labour has strong effects on traits that are closely related to longevity. For C. secundus, the results of the temperature stress experiment imply that ROS defence mechanisms are similar across castes but that the castes experience oxidative stress differently [65].…”

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

“…Like several of the former papers, this focuses on oxidative stress and identifies striking similarities, such as the role of peroxiredoxins, antioxidant enzymes, which in mammals appear to play a protective role in neurodegenerative disorders involving stress and seem to improve brain function in old honeybees. 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].…”

“…Additionally, transcriptome analyses reveal a clear oxidative stress defence signal (including Prx3) under constant conditions, which is stronger in workers than queens. These at first sight unexpected results can be explained by the fact that workers of this species are totipotent immatures, which have not yet reached maturity [32].…”

“…Yet the suggested approach is feasible and the study by Rau & Korb [32], based on [67], serves as a proof of principle: Monroy Kuhn et al [67] revealed nonlinear ageing in a termite species, with an abrupt queen death at an age of 12-13 years, associated with striking gene expression signals of physiological upheaval. The study in [32] successfully used the set of old-age genes established in [67] to test whether temperature stress induces ageing. Second, at the ultimate level, we emphasize the need for a comprehensive social life-history theory that addresses sociality and peculiarities of social animals in general and of social insects in particular (for a theory addressing the role of intergenerational transfer in social organisms, see [75]).…”