Parasite prevalence in a social host has colony-wide impacts on transcriptional activity and survival

Parasites pose significant challenges not only to individual hosts but also to entire social groups. We investigated the effects of parasitism by the cestode Anomotaenia brevis on colonies of its intermediate host, the ant Temnothorax nylanderi. We evaluated changes in worker and queen survival rates and transcriptional activity in the fat body of infected and uninfected workers, as well as in the parasite itself, in relation to infected worker prevalence and colony size. Cestode-infected workers are known to exhibit a significantly extended lifespan compared with uninfected workers. Here, we demonstrate that the survival rates of infected workers, uninfected queens, and uninfected workers decrease with increasing infected worker prevalence and increase with colony size. Transcriptomic analysis revealed stress-related signatures in all workers, regardless of infection status, as infection prevalence increased. Moreover, gene expression patterns, particularly in uninfected workers, were strongly influenced by colony size. The transcriptional activity of the parasitic cestode also shifted with infected worker prevalence, highlighting the complex dynamics of host-parasite interactions. These results demonstrate that parasites in social species impose colony-wide impacts that extend beyond infected individuals, even in the absence of direct cross-nestmate infection risks. Moreover, the consequences of parasitism can be modulated by colony size.