Microsporidian parasite impairs colony fitness in bumblebees

Emerging infectious diseases can have a major impact on the fitness of novel hosts, thereby contributing to ongoing species declines. In social insects, collaborative brood care by workers and successful mating of male sexuals are key to colony fitness. The microsporidian endoparasite, Nosema ceranae, has spread almost globally, shifting across honeybee species and now to bumblebees. However, despite N. ceranae being linked to recent population declines, its possible impact on bumblebee colony fitness remains poorly understood. Here, we show that N. ceranae infections can significantly impact Bombus terrestris worker feeding glands, as well as the longevity, sperm quality, and mating abilities of drones. In the laboratory, workers and drones were exposed to either the parasite or not. Then, parasite infection rates and loads, as well as lethal and sublethal parameters were assessed. Infected drones revealed higher parasite infection rates and spore titres as well as mortality compared to female workers, suggesting sex-specific susceptibility. Furthermore, infections impaired feeding glands, sperm traits, and altered mating behaviour - all of which are key to colony fitness. Our findings provide a mechanistic explanation on how N. ceranae contributes to the ongoing decline of wild bumblebee populations, calling for respective mitigation measures.