Cestode infection is linked to transcriptional shifts in neuropeptide signalling and caste-specific ageing pathways in a social insect

Abstract

Social insects are key models for phenotypic plasticity, as queens and workers show striking differences in behaviour and lifespan despite sharing the same genome. Neuropeptides are central regulators of behavioural plasticity, and caste-specific ageing is governed by the insulin/insulin-like growth factor 1 signalling–target of rapamycin–juvenile hormone network. Parasites that manipulate host behaviour and lifespan may exploit these regulators by targeting conserved neuropeptides or by altering ageing pathways. Here, we examine a host–parasite system in which the cestode Anomotaenia brevis extends lifespan and alters behaviour in its intermediate host, the ant Temnothorax nylanderi. In the fat body, queens and infected workers showed a higher degree of overlap in gene expression, consistent with a queen-like transcriptional shift in infected workers. This overlap was characterised by genes involved in ageing regulation, indicating that parasites affect components of conserved metabolic and longevity pathways typically associated with the queen phenotype. Parasite-derived peptides did not resemble host neuropeptides, which argues against classical neuropeptide mimicry based on sequence similarity. The parasite may affect host signalling through alternative mechanisms, including indirect modulation of host neuropeptide pathways. Ant neuropeptide and receptor expression varied strongly with caste and infection, with the latter associated with broad downregulation of neuropeptides in the brain, including tachykinin, short neuropeptide-F, allatostatin-A, orcokinin, CAPA, and diuretic hormones. In contrast, caste-related differences were more pronounced in the fat body, where infected workers resembled uninfected queens. This suggests that infection affects neural and peripheral regulatory pathways, reducing worker-like signalling and partially activating queen-like metabolic programmes. Our results reveal that parasites can exploit caste-specific plasticity and identify the molecular pathways used to reprogram host phenotypes.