Disentangling the aging network of a termite queen

Abstract

Background: Most insects are relatively short-lived, with a maximum lifespan of a few weeks, like the aging model organism, the fruit-fly Drosophila melanogaster. By contrast, the queens of social insects (termites, ants, some bees and wasps) can live for more than a decade. This makes social insects promising new models in aging research providing insights into how a long reproductive life can be achieved. Yet, aging studies on social insect reproductives are hampered by a lack of quantitative data on age-dependent survival and time series analyses that cover the whole lifespan of such long-lived individuals. We studied aging in queens of the drywood termite Cryptotermes secundus by determining survival probabilities over more than 15 years and performed transcriptome analyses for queens of known age that covered their whole lifespan. Results: The maximum lifespan of C. secundus queens was 13 years with a median maximum longevity of 11.0 years. Time course and co-expression network analyses of gene expression patterns over time indicated a non-gradual aging pattern. It was characterized by networks of genes that became differentially expressed only late in life, namely after an age of 10 years, which associates well with the median maximum lifespan for queens. These old-age gene networks reflect processes of physiological upheaval. We detected strong signs of stress, decline, defence and repair at the transcriptional level of epigenetic control as well as at the post-transcriptional level with changes in transposable element activity and the proteostasis network. The latter depicts an upregulation of protein degradation, together with protein synthesis and protein folding, processes which are often down-regulated in old animals. The simultaneous upregulation of protein synthesis and autophagy is indicative for a stress-response mediated by the transcription factor cnc, a homolog of human nrf genes. Conclusion: Our results show non-linear senescence with a rather sudden physiological upheaval at old-age. Most importantly, they point to a re-wiring in the proteostatis network as central for explaining the long life of social insect queens.

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

“…To test whether changes in temperature variance affected ageing, we compared the treatment-related DEGs, separately for each caste, with an in-house gene list containing genes characterizing old C. secundus queens that can be considered as ageing markers (old-age genes, hereafter) ( [41]; see electronic supplementary material, table S3). This list comprised genes that are upregulated in the head plus prothorax tissues of old queens (age: 10-11 years) that are likely to die soon (medium maximum longevity: 11 years; max longevity 13 years for C. secundus; [41]). These old-age genes were unrelated to fecundity.…”

“…These old-age genes were unrelated to fecundity. They reflect strong signs of stress, decline, defence and repair, at the transcriptional level of epigenetic control as well as at the posttranscriptional level with changes in TE-activity and the proteostasis network [41]. The latter depicts an upregulation of protein degradation, together with protein synthesis and protein folding, including many ribosomal genes [41].…”

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

“…In fact, there is evidence that reproductives in social animals have negligible mortality rates [65], and ant and termite queens die rather suddenly without showing strong reproductive senescence [59,66,67]. However, information on such life-history data is scarce [68] and is still accumulating only slowly for social insects [67,[69][70][71][72]. If ageing is not a gradual process, then data just comparing 'older' and 'younger' individuals are unlikely to reveal senescence processes.…”

“…Former approaches to identify common ageing markers proved to be difficult [73,74]. 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.…”

“…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]).…”