Bidirectional Transfer of RNAi between Honey Bee and Varroa destructor: Varroa Gene Silencing Reduces Varroa Population

Abstract

The mite Varroa destructor is an obligatory ectoparasite of the honey bee (Apis mellifera) and is one of the major threats to apiculture worldwide. We previously reported that honey bees fed on double-stranded RNA (dsRNA) with a sequence homologous to that of the Israeli acute paralysis virus are protected from the viral disease. Here we show that dsRNA ingested by bees is transferred to the Varroa mite and from mite on to a parasitized bee. This cross-species, reciprocal exchange of dsRNA between bee and Varroa engendered targeted gene silencing in the latter, and resulted in an over 60% decrease in the mite population. Thus, transfer of gene-silencing-triggering molecules between this invertebrate host and its ectoparasite could lead to a conceptually novel approach to Varroa control. Acquisition of RNAi components (dsRNA, siRNA) by ingestion and their spread within the recipient organism has been previously reported by us and others. Here we extend such observations, demonstrating cross-species horizontal transmission of dsRNA which, upon transmission from one organism to another still retains its biological activity. We show that dsRNA ingested by honey bees is further transmitted to the parasitic mite Varroa destructor that feeds on the honey bee's hemolymph. Reciprocally, dsRNA-carrying Varroa transmits the dsRNA back to bees. Furthermore, we demonstrate that bees ingesting dsRNA of Varroa gene sequences become vectors of dsRNAs, transmitting the signals to the Varroa, thus engendering silencing of mite genes and resulting in a significant phenotype, Varroa mortality. The exchange of active silencing signals between the honey bee and the mite suggests a potential RNA-based interaction between invertebrate hosts and parasites. Furthermore, our results offer a potentially conceptually new control measure for the mite Varroa destructor, which is one of the greatest threats to apiculture.