Queen number shapes worker longevity, fecundity and gene expression in the invasive, highly polygynous ant Tapinoma magnum

Abstract

In social animals, reproductive activity and ageing patterns are influenced by group composition. A well-documented phenomenon in monogynous (one-queen) insect societies is that queen presence affects worker fecundity and longevity. Little is known about whether and how workers respond to queen number variation in polygynous (multi-queen) species and how their queens age. We created queenless, one-queen, and two-queen colonies of the invasive, polygynous ant Tapinoma magnum to examine worker survival, fecundity, oxidative stress resistance, and fat body gene expression. Additionally, we compared 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 in single-queen colonies lived longer and were more fertile 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 demonstrated higher fecundity, oxidative stress resistance and upregulated antioxidant genes compared to older foragers. Absent or minor shifts in fecundity and transcription with queen age, respectively, indicated physiological stability with age. Our research highlights distinct caste- and tissue-specific ageing patterns in this supercolonial species, deviating from typical monogynous ants.