Abstract
BackgroundMost 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.ResultsThe 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.ConclusionsOur 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.
Highlights
Most insects are relatively short-lived, with a maximum lifespan of a few weeks, like the aging model organism, the fruit-fly Drosophila melanogaster
Identifying transcripts that change their expression with age: age‐related differentially expressed transcripts (DETs) To study gene expression changes over the life-time of queens, we generated transcriptomes of head / thorax from twelve queens with different chronological age since the onset of reproduction, from two until 13 years, covering the complete lifespan of C. secundus queens: 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, and 13 years (Additional File 2, Table S2)
Our study revealed a median maximum reproductive longevity of C. secundus queens of years with a maximum lifespan of years when excluding all causes of extrinsic mortality in the laboratory (Fig. 1, Additional File 2, Table S1)
Summary
Most insects are relatively short-lived, with a maximum lifespan of a few weeks, like the aging model organism, the fruit-fly Drosophila melanogaster. Classical model organisms typically have a short lifespan and can be characterized by r-life history strategies (‘live fast, have many offspring and die young’) as exactly these traits make them good model organisms Social insects such as termites, ants, or the honeybee, offer promising new insights into aging because individuals with the same genetic background can differ by orders of magnitudes in lifespan. Quantitative demographic data covering the whole lifespan of queens are inherently rare (for ants: [10,11,12] and references therein; for termites: [13, 14]) and many reports on queen-longevity are more anecdotal It is largely unknown for long-lived queens whether they age gradually or whether aging is a more sudden event
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