Data from: Disentangling the aging network of a termite queen

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. 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 proteostasis network and stress as part of the aging process of social insect queens, shortly before queens die.

研究背景：绝大多数昆虫的寿命相对较短，最长仅为数周，以经典衰老模式生物黑腹果蝇（Drosophila melanogaster）为例。与之形成鲜明对比的是，多数社会性昆虫（白蚁、蚂蚁及部分蜂类）的蚁后寿命可达数年至数十年。这使得社会性昆虫成为衰老研究中极具潜力的模式生物，为解析如何实现长期生殖寿命提供了关键视角。然而，针对社会性昆虫生殖个体的衰老研究却因缺乏基于年龄的存活定量数据，以及覆盖此类长寿命个体完整生命周期的时间序列分析而进展受限。本研究以干木白蚁（Cryptotermes secundus）蚁后为研究对象，通过15年的追踪观测获取其存活概率数据，并对已知年龄、覆盖完整生命周期的蚁后开展转录组（transcriptome）分析。

研究结果：干木白蚁蚁后的最大寿命为13年，中位最大寿命为11.0年。对随时间变化的基因表达模式开展的时间进程分析与共表达网络分析显示，该蚁后的衰老模式并非渐进式。该模式以仅在生命后期（即10年之后）出现差异表达的基因网络为核心特征，这与蚁后的中位最大寿命高度契合。这些老龄相关基因网络反映了机体生理剧变的过程。我们在表观遗传调控的转录水平，以及转座因子（transposable element）活性与蛋白稳态（proteostasis）网络的转录后水平，均检测到显著的应激、衰退、防御与修复相关分子信号。其中，蛋白稳态网络呈现出蛋白质降解、蛋白质合成与蛋白质折叠的协同上调——这类过程在衰老动物体内通常会被下调。蛋白质合成与自噬（autophagy）的协同上调，表明存在由转录因子cnc（人类nrf基因同源物）介导的应激反应。

研究结论：本研究结果揭示了非线性衰老模式：老龄阶段会出现相当突然的生理剧变。尤为关键的是，研究结果表明，在蚁后即将死亡前不久，其蛋白稳态网络与应激反应发生了重编程，这一过程是社会性昆虫蚁后衰老进程的重要组成部分。