Kleptocytosis: A Novel Parasitic Strategy for Accelerated Reproduction via Host Protein Stealing in Varroa destructor

The rapid reproductive capacity of Varroa destructor is among the most significant adaptations underpinning its success as a parasite. To exploit their honey bee host, the parasite must rapidly produce offspring that fully develop into adults and mate in an inflexible 9-day window. Inability to meet this deadline brings the foundress mites fitness to zero establishing heavy evolutionary pressure to accelerate reproduction & subsequent development of offspring. Our work fills in gaps in our understanding of a key pathway in this process. Varroa have a poorly-understood ability to pass heretofore unidentified host proteins through their body with minimal digestion/degradation. Via Native-PAGE, we were able to confirm that nine proteins shared with honey bee fat body tissue accumulate intact in the eggs of the foundress mite. As such, we hypothesized that the proteins were several egg yolk precursors synthesized and stored in the fat body. Using antibodies raised against honey bee vitellogenin (Vg) we positively identified this egg yolk precursor via SDS-PAGE and subsequent Western Blot. We then analyzed samples of honey bee fat body tissue, gravid Varroa, so called "phoretic" Varroa, and Varroa eggs via HPLC MS/MS to identify the remaining host proteins and determine their relative abundance. We detected egg yolk precursors in the large lipid transfer protein superfamily, in addition to hexamerin storage proteins, and miscellaneous motor/transfer proteins integral to embryonic development (transferrin, myosin heavy chain, and heat shock protein 60). Varroa lack the capacity to produce some of these proteins and instead employ kleptoparasitism on a molecular level to provision their developing ova, a pathway not described in any other host/parasite relationship, hereafter referred to as kleptocytosis. These different families of proteins are normally produced by the female and conveyed to the vitellogenic egg cell through protein specific receptor-mediated pathways. Such pathways would exclude foreign proteins. We hypothesize that the need to rely on a receptor-mediated pathway is circumvented via the specialized nutritive reproductive tissue, the lyrate organ. Through microCT imaging we detail the connection between the developing ovum and this dual-lobed organ. Better understanding of this pathway presents a novel target for Varroa management as the treatment need only accomplish slowing acquisition or deposition of host proteins thereby disrupting the mites ability to meet the temporal demand of its host.