Disentangling the aging gene expression network of termite queens

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 many social insects (termites, ants and some bees) can live from a few years to decades. This makes social insects promising 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 a period of 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 ten 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, defense 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 of a stress-response mediated by the transcription factor cnc, a homolog of human nrf genes. Conclusions 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 proteostasis network and stress as part of the aging process of social insect queens, shortly before queens die.

Molecular underpinnings of division of labour among workers in a socially complex termite

“…Yet, in the termite C. secundus , at least one of these Vg genes, Neofem3 , is similarly expressed in all body parts (head, thorax, abdomen) 29 . Furthermore, recent results demonstrate that head plus thorax tissues are very well suited to study life history traits 30 , 49 , including expression of all three Vg genes that we detected to be upregulated in builders compared to foragers. Fat body, the main tissue known to synthetize vitellogenin, also occurs in the thorax.…”

“…Transcriptomes were generated from the termites' head plus thorax. Recent studies showed that head plus thorax samples are most suitable for transcriptome studies in termites as major pathways underlying the regulation of life history traits, including the fecundity in queens, are expressed in these tissues 30 , 49 .…”

More effective transposon regulation in fertile, long‐lived termite queens than in sterile workers

“…Workers on the other hand are short‐lived and sterile. Several studies suggest gene transcription plays an important role in this absence of a longevity/fecundity trade‐off in termites (Elsner et al, 2018; Lin et al, 2021; Monroy Kuhn et al, 2019, 2021; Séité et al, 2022). One of these highlights the particular importance of fat body gene transcription in M. natalensis (Séité et al, 2022).…”

Effect of food restriction on survival and reproduction of a termite

“…Like other wood‐dwelling termites, C. secundus has a low level of social complexity with colony sizes of a few 100 workers and mature queens laying around 100 eggs per year (Korb & Lenz, 2004; Korb & Thorne, 2017). Nevertheless, queens can reach a maximum life span of 13 years, with mean longevities of 11.1 (±0.66) years after successful colony foundation (Monroy Kuhn et al, 2021). This is at least twice as long as the longevity of the sister taxon of the termites, the subsocial Cryptocercus woodroaches, which also live in a piece of wood.…”