Since the emergence of the parasitic mite Varroa destructor, the viral landscape of honeybees (Apis mellifera) has changed dramatically due to the increased spread of virulent viral strains, resulting in widespread loss of wild and managed honeybees. However, in various pockets of the world, populations of honeybees have naturally evolved or been selected for resistance to Varroa mites. These Varroa-tolerant populations provide a unique opportunity to capture the process of host-parasite adaptation as it develops in multiple locations, and to investigate the interrelationship between viruses, mite vectors and their honeybee hosts.
Using whole transcriptome sequencing, we examined the viral landscape of Varroa-tolerant honeybees from three locations in Europe, Africa and the Pacific. Almost all of the known honeybee viruses characterised thus far are positive-sense, single stranded RNA viruses of the Picornavirales order. Along with many of these common honeybee viruses, we found genomic evidence of seven previously undetected viruses, including four novel, negative sense RNA viruses. Two of these viruses belong to a common class of arthropod viruses, the Rhabdoviridae. Both Rhabdoviruses were found in all three of our geographically diverse locations and were also present in Varroa mites parasitising the bees. Small RNA profiles in infected bees indicated active Dicer-mediated degradation of both Rhabdoviruses. Varroa mites showed a different small RNA degradation profile suggesting that an alternate form of viral processing that occurs in mites.
These discoveries signify new classes of negative sense RNA viruses in honeybees, and raise the possibility that there are a multitude of undescribed viruses found in both Varroa and A. mellifera that may be adequately suppressed by innate immune pathways to prevent pathology.