Promiscuous feeding on multiple adult honey bee hosts amplifies the vectorial capacity of Varroa destructor

Abstract

Varroa destructor is a cosmopolitan pest and leading cause of colony loss of the European honey bee. Historically described as a competent vector of honey bee viruses, this arthropod vector is the cause of a global pandemic of Deformed wing virus, now endemic in honeybee populations in all Varroa-infested regions. Our work shows that viral spread is driven by Varroa actively switching from one adult bee to another as they feed. Assays using fluorescent microspheres were used to indicate the movement of fluids in both directions between host and vector when Varroa feed. Therefore, Varroa could be in either an infectious or naïve state dependent upon the disease status of their host. We tested this and confirmed that the relative risk of a Varroa feeding depended on their previous host’s infectiousness. Varroa exhibit remarkable heterogeneity in their host-switching behavior, with some Varroa infrequently switching while others switch at least daily. As a result, relatively few of the most active Varroa parasitize the majority of bees. This multiple-feeding behavior has analogs in vectorial capacity models of other systems, where promiscuous feeding by individual vectors is a leading driver of vectorial capacity. We propose that the honeybee-Varroa relationship offers a unique opportunity to apply principles of vectorial capacity to a social organism, as virus transmission is both vectored and occurs through multiple host-to-host routes common to a crowded society. Author summary Varroa destructor is an ectoparasitic mite implicated in historical colony losses of the managed honey bee Apis mellifera and is responsible for the global pandemic of Deformed wing virus (DWV). Varroa has long been described as a competent vector of DWV, but surprisingly little is known about its feeding and subsequent vectoring of viruses on adult honey bees. Through a series of experiments, we found Varroa actively switch from one adult bee host to another to feed. Mites exhibit a large degree of heterogeneity in their host-switching behavior, with some mites switching frequently and others not nearly at all. Our results mirror an observation in other vector-host-pathogen relationships: a relatively small number of mites contributed to a majority of parasitized hosts. These high-frequency biters are most likely to not only transmit, but also acquire infectious pathogens as they switch from host to host. The ability to parasitize and infect multiple adult bees provides the best explanation to date for the maintenance and subsequent host-to-host spread of viruses among the long-lived worker bees common in these crowded and vulnerable colony populations.