Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect

Background: 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. Results: 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. Conclusions: 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

Life history evolution in social insects:a female perspective

Social insects are known for their unusual life histories with fecund, long-lived queens and sterile, short-lived workers. We review ultimate factors underlying variation in life history strategies in female social insects, whose social life reshapes common trade-offs, such as the one between fecundity and longevity. Interspecific life history variation is associated with colony size, mediated by changes in division of labour and extrinsic mortality. In addition to the ratio of juvenile to adult mortality, social factors such as queen number influence life history trajectories. We discuss two hypotheses explaining why queen fecundity and lifespan is higher in single-queen societies and suggest further research directions on the evolution of life history variation in social insects

Extreme lifespan extension in tapeworm-infected ant workers

Social insects are hosts of diverse parasites, but the influence of these parasites on phenotypic host traits is not yet well understood. Here, we tracked the survival of tapeworm-infected ant workers, their uninfected nest-mates and of ants from unparasitized colonies. Our multi-year study on the ant Temnothorax nylanderi, the intermediate host of the tapeworm Anomotaenia brevis, revealed a prolonged lifespan of infected workers compared with their uninfected peers. Intriguingly, their survival over 3 years did not differ from those of (uninfected) queens, whose lifespan can reach two decades. By contrast, uninfected workers from parasitized colonies suffered from increased mortality compared with uninfected workers from unparasitized colonies. Infected workers exhibited a metabolic rate and lipid content similar to young workers in this species, and they received more social care than uninfected workers and queens in their colonies. This increased attention could be mediated by their deviant chemical profile, which we determined to elicit more interest from uninfected nest-mates in a separate experiment. In conclusion, our study demonstrates an extreme lifespan extension in a social host following tapeworm infection, which appears to enable host workers to retain traits typical for young workers