Host-parasite interactions between the honey bee, Apis mellifera, and the mite Varroa destructor: Insights into virus infections and Varroa Sensitive Hygiene

Abstract

The ectoparasite Varroa destructor is currently considered the greatest threat to the beekeeping industry and to honey bee health worldwide. Since its transfer from the Asian honey bee, the mite has been responsible for heavy colony losses in European honey bee populations (Apis mellifera). The ultimate goal of the work described in this thesis is to find long-term solutions that prevent colony losses and provide an alternative to the chemical treatments on which the beekeepers currently depend.

The association of Varroa with several honey bee viruses complicates the host-parasite interactions between bees and mites. This thesis first reveals that the arrival of Varroa dramatically affects the viral landscape of bee colonies, increasing the number of viral species that infect colonies and leaving deformed wing virus as the predominant species in long-term infested regions. The thesis then investigates key aspects of Varroa sensitive hygiene (VSH), a behavioural trait that can confer natural survival abilities to Varroa-infested colonies, and which relies on the ability of worker bees to selectively detect brood cells infested with Varroa. Results of this thesis strongly support the hypothesis that bees use olfactory cues to identify mite-infested cells, and that removal of parasitised pupae depends on the presence of mite offspring in the targeted cells. Several factors associated with the initiation of VSH behaviour are described, including Kashmir bee virus and brood ester pheromone. Five compounds that are specific to Varroa-parasitised brood cells are also identified. These results suggest for the first time that factors triggering removal of prepupae may be different from those associated with removal of pupae brood cells. Finally, gene expression associated with VSH behaviour is identified in the antennae of worker bees, and discussed as potential biomarkers of VSH. Altogether, the results of this thesis provide new insights into host-parasite interactions between the honey bee and Varroa, and they emphasise the need to include honey bee viruses as a critical player in these host-parasite interactions. The thesis also provides a deeper understanding of VSH behaviour and suggests avenues for applying the knowledge gained in this study to breeding programs selecting bees for their ability to survive Varroa infestations with little or no treatment against the mite.