The miRNAome of the honey bee parasite, Varroa destructor, shows sex-specific expression of miRNA clusters across life stages

The honey bee mite, Varroa destructor, is one of the biggest threats to the western honey bee, Apis mellifera. MicroRNAs (miRNAs) are important regulators of gene expression, playing roles in development, sex differentiation, and reproduction, yet little is known about their expression throughout the Varroa mite lifecycle. Here we identify the complete set of miRNAs in V. destructor throughout its lifecycle by sequencing the small RNAs of male and female mites. We identify 170 precursor miRNAs, including 88 novel miRNAs that appear specific to mites. miRNA expression varies significantly between life stages, revealing miRNAs specific to developmental stage and sex. Reproductive adult females (foundresses) show an expression pattern that is distinct from other adult females, with similarities to eggs and early juvenile stages, indicating a significant role for miRNA regulation in reproduction and early development. This expression is largely driven by three miRNA clusters (vde-miR-92, vde-miR-279/35, vde-miR-35/nov-7) containing 16 miRNAs that are significantly upregulated in foundress mites. Additionally, a cluster of three miRNAs from a novel miRNA family (vde-miR-nov-1) are significantly upregulated in all female life stages compared to males. The expression patterns of the vde-miR-nov-1 family suggest a potential role for miRNA regulation in sex differentiation and female development. Our results indicate that miRNA regulation has an important role in the biology and development of V. destructor. Characterising the downstream impacts of miRNAome expression will enable a better understanding of mite development and reproductive processes. The identification of novel, Varroa-specific miRNAs may provide targets for future control methods.