Entomopathogenic fungus as well as their toxins is a natural threat surrounding social insect colonies. To defend against them, social insects have evolved a series of unique disease defenses at the colony level, which consists of behavioral and physiological adaptations. These colony-level defenses can reduce the infection and poisoning risk and improve the survival of societal members, and is known as social immunity. In this review, we discuss how social immunity enables the insect colony to avoid, resist and tolerate fungal pathogens. To understand the molecular basis of social immunity, we highlight several genetic elements and biochemical factors that drive the colony-level defense, which needs further verification. We discuss the chemosensory genes in regulating social behaviors, the antifungal secretions such as some insect venoms in external defense and the immune priming in internal defense. To conclude, we show the possible driving force of the fungal toxins for the evolution of social immunity. Throughout the review, we propose several questions involved in social immunity extended from some phenomena that have been reported. We hope our review about social ‘host–fungal pathogen’ interactions will help us further understand the mechanism of social immunity in eusocial insects.

Eusocial insects have evolved specific defensive strategies to protect their colonies. In termite colonies, soldiers perform a colony-level defense by displaying mechanical biting, head-banging and mandible opening–closing behaviors. However, few studies have been reported on the factors modulating defensive behaviors in termites. Owing to JH (juvenile hormone) being involved in soldier differentiation, JH was speculated to affect defensive behaviors in termite soldiers. To determine the effect of JH on the defensive behaviors of termite soldiers, we performed a JHA-feeding and RaSsp1-silencing experiment and then tested the changes in defense-related behaviors, alarm pheromones and key JH signaling genes. The observed result was that after feeding workers with JHA, soldiers displayed the following: (1) decreased biting events and increased head-banging events; (2) a reduced expression of RaSsp1 and increased expression of Met (methoprene-tolerant, the nuclear receptor of JH) and Kr-h1 (the JH-inducible transcription factor Krüppel homolog 1); and (3) a decreased concentration of alarm pheromones, including α-pinene, β-pinene and limonene (+, −). Further study showed that soldiers silenced for RaSsp1 also exhibited (1) decreased biting events and increased head-banging events and (2) increased expression of Met and Kr-h1. In addition, soldiers stimulated by the alarm pheromone limonene displayed an increase in the frequency of mandible opening–closing and biting behavior. All of these results show that JHA influenced the defensive behaviors of termite soldiers, possibly via downregulating RaSsp1 expression, up-regulating Met and Kr-h1 and stimulating the secretion of alarm pheromones, suggesting that the JH pathway plays important roles in modulating social behaviors in termite colonies.

MiR-71 has been determined to enhance the efficacy of biological control agents against termites. However, it is not clear how miR-71 functions in enhancing the termite control. In this study, we tested the effects of termite miR-71 on the transcriptional and translational profiles of termites via the commercial product miR-71 agomir, and meanwhile developed a cost-effective method using T7 RNA polymerase to synthesize a miR-71 mimic, comparing the effects of the T7-synthesized miR-71 mimic versus the commercial miR-71 agomir on the gene expressions and infection mortality of termites. Comparative bioassays demonstrated that both miR-71 mimic and agomir significantly increased fungus-induced termite mortality with equivalent bioactivity. Mechanistically, transcriptomic and proteomic analyses revealed that commercial miR-71 agomir modulated the expression of defense-related genes, such as hexamerin-1, neuroligin-4, and probable chitinase-10. Meanwhile, RT-qPCR confirmed that T7-synthesized miR-71 mimic induced similar expression changes in the same target genes. Additionally, the dsRNA-mediated silencing of hexamerin-1, neuroligin-4, and probable chitinase-10 made termites more vulnerable to the fungus, respectively. Our study establishes in vitro-transcribed miRNA mimics as potent and cost-effective tools for studying ‘miRNA–mRNA’ interaction, and meanwhile lays the foundation for the microbe-mediated expression of small-RNA mimics in enhancing termite biocontrol.