Dataset Information

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.

SUBMITTER: Monroy Kuhn JM

PROVIDER: S-EPMC8114706 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The analysis of ecological networks is generally bottom-up, where networks are established by observing interactions between individuals. Emergent network properties have been indicated to reflect the dominant mode of interactions in communities that might be mutualistic (e.g., pollination) or antagonistic (e.g., host-parasitoid communities). Many ecological communities, however, comprise species interactions that are difficult to observe directly. Here, we propose that a comparison of the emergent properties from detail-rich reference communities with known modes of interaction can inform our understanding of detail-sparse focal communities. With this top-down approach, we consider patterns of coexistence between termite species that live as guests in mounds built by other host termite species as a case in point. Termite societies are extremely sensitive to perturbations, which precludes determining the nature of their interactions through direct observations. We perform a literature review to construct two networks representing termite mound cohabitation in a Brazilian savanna and in the tropical forest of Cameroon. We contrast the properties of these cohabitation networks with a total of 197 geographically diverse mutualistic plant-pollinator and antagonistic host-parasitoid networks. We analyze network properties for the networks, perform a principal components analysis (PCA), and compute the Mahalanobis distance of the termite networks to the cloud of mutualistic and antagonistic networks to assess the extent to which the termite networks overlap with the properties of the reference networks. Both termite networks overlap more closely with the mutualistic plant-pollinator communities than the antagonistic host-parasitoid communities, although the Brazilian community overlap with mutualistic communities is stronger. The analysis raises the hypothesis that termite-termite cohabitation networks may be overall mutualistic. More broadly, this work provides support for the argument that cryptic communities may be analyzed via comparison to well-characterized communities.