Strong context‐dependent virulence in a host–parasite system: reconciling genetic evidence with theory

Abstract

Summary: Parasites can have dramatic effects on the ecology of their hosts. Such strong host–parasite interactions are the result of either parasites with generally high virulence, or generally benign parasites that nevertheless express context‐dependent virulence. Theoretically, one indication that an apparently benign parasite nevertheless has a large impact on its host should be the existence of strong genotypic interactions between host and parasite. Crithidia bombi (Trypanosomatidae) is a highly prevalent but generally benign gut parasite of the bumble‐bee Bombus terrestris. The demonstration of strong genotypic interactions between C. bombi and B. terrestris, however, suggests that context‐dependent virulence may have a large impact on the host population. We thus investigated the effects of C. bombi across the entire life cycle of its host, including the stressful times of hibernation and colony‐founding. Owing to the high prevalence and rates of transmission of the parasite in field populations, we used a large‐scale laboratory experiment. Under stressful hibernation, infected queens lost more mass. Infection also significantly reduced colony‐founding success, colony size, male production and overall fitness, by up to 40%. These findings show that strong genotypic host–parasite interactions may indeed be a reliable indicator that apparently benign and highly prevalent parasites are nevertheless exerting a dramatic impact on their host populations.