Vector-virus interaction affects viral loads and co-occurrence

BACKGROUND: Vector-borne viral diseases threaten human and wildlife worldwide. Vectors are often viewed as a passive syringe injecting the virus. However, to survive, replicate and spread, viruses must manipulate vector biology. While most vector-borne viral research focuses on vectors transmitting a single virus, in reality, vectors often carry diverse viruses. Yet how viruses affect the vectors remains poorly understood. Here, we focused on the varroa mite (Varroa destructor), an emergent parasite that can carry over 20 honey bee viruses, and has been responsible for colony collapses worldwide, as well as changes in global viral populations. Co-evolution of the varroa and the viral community makes it possible to investigate whether viruses affect vector gene expression and whether these interactions affect viral epidemiology. RESULTS: Using a large set of available varroa transcriptomes, we identified how abundances of individual viruses affect the vector’s transcriptional network. We found no evidence of competition between viruses, but rather that some virus abundances are positively correlated. Furthermore, viruses that are found together interact with the vector’s gene co-expression modules in similar ways, suggesting that interactions with the vector affect viral epidemiology. We experimentally validated this observation by silencing candidate genes using RNAi and found that the reduction in varroa gene expression was accompanied by a change in viral load. CONCLUSIONS: Combined, the meta-transcriptomic analysis and experimental results shed light on the mechanism by which viruses interact with each other and with their vector to shape the disease course. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01463-4.