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

Abstract

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 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 the effect of queen number on 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 between 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 gene expression, though its effect on the latter differed between inside and outside workers. Furthermore, inside—likely younger—workers produced more oocytes, showed higher oxidative stress resistance and upregulated antioxidant genes compared to outside—likely older—workers. Minimal shifts in fecundity and gene expression of differently aged queens indicated their physiological stability. Our research highlights distinct caste- and tissue-specific responses to varying queen numbers in workers of a highly polygynous species.