Vector-mediated viral transmission favours less virulent viruses

Abstract

While it is well-established that the ectoparasitic mite Varroa destructor is largely responsible for the widely-reported decline of populations of the Western honeybee Apis mellifera, the exact role the mite plays in honeybee health remains unclear. The last few years have seen a surge in studies associating RNA viruses vectored by the mite with the death of honeybee colonies. Varroa facilitates the spread of RNA viruses because it feeds on developing bee brood and transfers haemolymph from bee-to-bee. Such a change in transmission, from horizontal and vertical to vector-based, is predicted to lead to an increase in virulence of RNA viruses, thus potentially providing an explanation for the observed association between Varroa and certain viruses. Here we document the effect of changing the route of transmission of honeybee viruses contained in the haemolymph of honeybee pupae. We find that a change in mode of transmission rapidly increases viral titres of two honeybee viruses, Sacbrood virus (SBV) and Black queen cell virus (BQCV). This increase in viral titre is accompanied by an increase in virulence. In contrast, the virus most often associated with Varroa, Deformed wing virus (DWV), shows a reduction in viral titre in the presence of SBV and BQCV. In addition, DWV does not cause mortality to honeybee pupae in isolation. Most likely a change in mode of transmission due to the arrival of a vector quickly eliminates the most virulent honeybee viruses resulting in an association between Varroa and less virulent viruses such as DWV. Our work therefore provides empirical evidence for an alternative explanation for the widely-observed association between Varroa and DWV.