The gut microbiome can influence life history traits associated with host fitness such as fecundity and longevity. In most organisms, these two life history traits are traded-off, while they are positively linked in social insects. In ants, highly fecund queens can live for decades, while their non-reproducing workers exhibit much shorter lifespans. Yet, when fertility is induced in workers by death or removal of the queen, worker lifespan can increase. It is unclear how this positive link between fecundity and longevity is achieved and what role the gut microbiome and the immune system play in this. To gain insights into the molecular regulation of lifespan in social insects, we investigated fat body gene expression and gut microbiome composition in workers of the ant Temnothorax rugatulus in response to an experimental induction of fertility and an immune challenge. Fertile workers upregulated several molecular repair mechanisms, which could explain their extended lifespan. The immune challenge altered the expression of several thousand genes in the fat body, including many immune genes, and, interestingly, this transcriptomic response depended on worker fertility. For example, only fertile, immune-challenged workers upregulated genes involved in the synthesis of alpha-ketoglutarate, an immune system regulator, which extends the lifespan in Caenorhabditis elegans by down-regulating the TOR pathway and reducing oxidant production. Additionally, we observed a dramatic loss in bacterial diversity in the guts of the ants within a day of the immune challenge. Yet, bacterial density did not change, so that the gut microbiomes of many immune challenged workers consisted of only a single or a few bacterial strains. Moreover, the expression of immune genes was linked to the gut microbiome composition, suggesting that the ant host can regulate the microbiome in its gut. Immune system flare-ups can have negative consequence on gut microbiome diversity, pointing to a previously underrated cost of immunity. Moreover, our results provide important insights into shifts in the molecular regulation of fertility and longevity associated with insect sociality.

中文翻译：

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免疫挑战减少了肠道昆虫的肠道微生物多样性，并触发了依赖于生育力的基因表达变化

肠道微生物组可以影响与宿主适应性相关的生活史特征，例如生殖力和寿命。在大多数生物中，这两个生命史特征是相互取舍的，而在社交昆虫中却是正相关的。在蚂蚁中，高度繁殖力的女王可以生活数十年，而其非繁殖力工人的寿命要短得多。但是，如果因死亡或女王的离职而导致工人生育，则工人的寿命会增加。目前尚不清楚如何实现生殖力和寿命之间的这种积极联系，以及肠道微生物组和免疫系统在其中的作用。为了深入了解社交昆虫的寿命分子调控，我们调查了实验性诱导的繁殖力和免疫应答，研究了皱纹蚁（Temnothorax rugatulus）工人的脂肪体基因表达和肠道微生物组组成。肥沃的工人上调了几种分子修复机制，这可以解释其延长的寿命。免疫挑战改变了脂肪体内数千个基因的表达，包括许多免疫基因，有趣的是，这种转录组反应取决于工人的生育能力。例如，只有受精的，受到免疫挑战的工人才能上调参与α-酮戊二酸（一种免疫系统调节剂）合成的基因，该基因通过下调TOR途径并减少氧化剂的产生来延长秀丽线虫的寿命。另外，我们观察到在免疫攻击的一天之内，蚂蚁肠道中细菌多样性的急剧下降。然而，细菌的密度没有改变，因此许多受到免疫挑战的工人的肠道微生物群仅由一个或几个细菌菌株组成。而且，免疫基因的表达与肠道微生物组组成有关，这表明蚂蚁宿主可以调节肠道中的微生物组。免疫系统爆发可能会对肠道微生物组多样性产生负面影响，这表明以前低估了免疫成本。此外，我们的结果为昆虫与社会相关的生育力和寿命的分子调控转变提供了重要的见识。因此，许多受到免疫挑战的工人的肠道微生物群仅由一个或几个细菌菌株组成。而且，免疫基因的表达与肠道微生物组组成有关，这表明蚂蚁宿主可以调节肠道中的微生物组。免疫系统爆发可能会对肠道微生物组多样性产生负面影响，这表明以前低估了免疫成本。此外，我们的结果为昆虫与社会相关的生育力和寿命的分子调控转变提供了重要的见识。因此，许多受到免疫挑战的工人的肠道微生物群仅由一个或几个细菌菌株组成。而且，免疫基因的表达与肠道微生物组组成有关，这表明蚂蚁宿主可以调节肠道中的微生物组。免疫系统爆发可能会对肠道微生物组多样性产生负面影响，这表明以前低估了免疫成本。此外，我们的结果为昆虫与社会相关的生育力和寿命的分子调控转变提供了重要的见识。指出以前被低估的免疫成本。此外，我们的结果为昆虫与社会相关的生育力和寿命的分子调控转变提供了重要的见识。指出以前被低估的免疫成本。此外，我们的结果为昆虫与社会相关的生育力和寿命的分子调控转变提供了重要的见识。