Host evolutionary history predicts virus prevalence across bumblebee species

Abstract

Why a pathogen associates with one host but not another is one of the most important questions in disease ecology. Here we use transcriptome sequencing of wild-caught bumblebees from 13 species to describe their natural viruses, and to quantify the impact of evolutionary history on the realised associations between viruses and their pollinator hosts. We present 37 novel virus sequences representing at least 30 different viruses associated with bumblebees. We verified 17 of them by PCR and estimate their prevalence across species in the wild. Through small RNA sequencing, we demonstrate that at least 10 of these viruses form active infections in wild individuals. Using a phylogenetic mixed model approach, we show that the evolutionary history of the host shapes the current distribution of virus/bumblebee associations. Specifically, we find that related hosts share viral assemblages, viruses differ in their prevalence averaged across hosts and the prevalence of infection in individual virus-host pairings depends on precise characteristics of that pairing. Authors SummaryDespite the importance of disease in the regulation of animal populations, our understanding of the distribution of pathogen burden across wild communities remains in its infancy. In this study, we investigated the distribution of viruses across natural populations of 13 different bumblebee species in Scotland. We first searched for viruses using a metatranscriptomic approach, finding at least 30 new viruses of bumblebees, and assayed a subset of them for their presence and absence in different host species. Then, in the first application of these methods to an animal-virus system, we used co-phylogenetic mixed models to investigate the factors that lead to species being having different prevalences for a subset of these viruses. While much of the variation in the prevalence of the viruses can be explained by the idiosyncrasies of individual bumblebee-virus pairings, there is a phylogenetic signal with related bumblebee species being infected at similar frequencies by the same sets of viruses. Consistent with previous work, our study indicates that, while in general the interaction between a host and a virus may be unpredictable, closely related species are more likely to exhibit similar patterns of infection.