Emily J. Remnant

The ectoparasitic mite Varroa destructor is the leading threat to the health of Western honey bees ( Apis mellifera ) primarily through its action as a vector of viruses. However, it is unclear which of the viruses transmitted by V. destructor actively infect and replicate in mites, which could facilitate increased transmission. To better understand the role of V. destructor as a vector, we took advantage of differences between bee and mite antiviral RNA interference pathways to identify the host specificity of replicating viruses. We used small RNA sequencing of individual V. destructor mites to examine viral small interfering RNA (vsiRNA) profiles of deformed wing virus genotypes (DWV-A and DWV-B), associated with colony declines, as well as nine other viruses present in our samples. We found active replication of six V. destructor -associated viruses, including a novel virus, Varroa destructor virus 9 (VDV-9), and replication of two honey bee-associated viruses, including both DWV-A and -B genotypes, confirming that mites are biological vectors for important bee pathogens. We show that the antiviral RNAi response can be used to define the host range of viruses in host-parasite interactions, such as honey bees and their parasites, enabling a better understanding of the role of a vector in the evolution and spread of honey bee pathogens. IMPORTANCE The parasitic mite Varroa destructor is a significant driver of worldwide colony losses of our most important commercial pollinator, the Western honey bee Apis mellifera . Declines in honey bee health are frequently attributed to the viruses that mites vector to honey bees, yet whether mites passively transmit viruses as a mechanical vector or actively participate in viral amplification and facilitate replication of honey bee viruses is debated. Our work investigating the antiviral RNA interference response in V. destructor demonstrates that key viruses associated with honey bee declines actively replicate in mites, indicating that they are biological vectors, and the host range of bee-associated viruses extends to their parasites, which could impact virus evolution, pathogenicity, and spread.