Worker survival and egg production, but not transcriptional activity, respond to queen number in the highly polygynous, invasive ant

In social animals, reproductive activity and ageing are influenced by group composition. In monogynous (single-queen) insect societies, queen presence affects worker fecundity and longevity, but less is known about worker responses to queen number variation in highly polygynous (multi-queen) species or how queens age in these systems. We created queenless, one-queen, and two-queen colonies of the invasive polygynous ant Tapinoma magnum to examine worker survival, ovary and oocyte development, oxidative stress resistance, and fat body gene expression. We also compared the fecundity and brain and fat body transcriptomes of young and old queens. Queenless workers experienced the highest mortality, contrasting with monogynous species, where queen removal typically extends lifespan. Workers lived longer and had more developing oocytes in their ovaries in single-queen than in two-queen colonies. Queen number did not directly affect oxidative stress resistance or fat body transcription, though the latter depended on an interaction with worker task. Furthermore, younger nurses produced more oocytes, showed higher oxidative stress resistance, and upregulated antioxidant genes compared to older foragers. Minimal shifts in fecundity and transcription with queen age indicated physiological stability. Our research highlights distinct caste- and tissue-specific ageing patterns in this supercolonial species, deviating from typical monogynous ants.