microRNAs shape social immunity: a potential target for biological control of the termite Reticulitermes chinensis

Eusocial insects can employ various behavioural and physiological disease defences to avoid, resist and tolerate pathogen infections in their closely related and packed colonies, termed social immunity. Recent studies have shown that several molecules serve insect social immunity, including chemical odours, insect venoms, immune-related proteins, etc. However, whether and how microRNAs (miRNAs), whose precursors are processed by Dicer-1 , drive social immunity in insect colonies is still unknown. Here, we used a ‘host–pathogen’ system (host: Reticulitermes chinensis ; pathogen: Metarhizium anisopliae ) to explore the impact of miRNAs on social immunity in termite colonies. We found that RNAi-mediated silencing of Dicer-1 led to decreased miRNA concentration, significantly inhibited carbohydrate and energy metabolism and affected other life processes, such as the immune response and oxidation–reduction reactions, in whole body of the termite. In behavioural defence, silencing Dicer-1 significantly diminished defensive social behaviours such as locomotion, grooming, cannibalism and burial in termite groups when encountering fungal contamination. In physiological defence, Dicer-1 silencing and miR-71-5 stimulation resulted in significantly decreased antifungal activities of termites. Furthermore, both Dicer-1 -silenced and miR-71-5 stimulant-treated termite groups exhibited a high level of mortality during fungal contamination. Our findings demonstrated the important role of miRNAs in shaping social immunity in termite colonies, providing insights necessary to understand the potential mechanisms underlying behavioural and physiological disease defences in insects and hence laying the groundwork for miRNA-based pest control.