Bioallethrin activates specific olfactory sensory neurons and elicits spatial repellency in Aedes aegypti

Abstract

BACKGROUND: Use of pyrethroid insecticides is a pivotal strategy for mosquito control globally. Commonly known for its insecticidal activity by acting on voltage-gated sodium channels, volatile pyrethroids, such as bioallethrin and transfluthrin, are used in mosquito coils, emanators, and other vaporizers to repel mosquitoes and other biting arthropods. However, whether specific olfactory receptor neurons are activated by pyrethroids to trigger spatial repellency remains unknown. RESULTS: We took behavioral and electrophysiological approaches to elucidate the mechanism of bioallethrin repellency in Aedes aegypti, a major vector of dengue, yellow fever, Zika and chikungunya viruses. We found that bioallethrin elicits spatial (i.e., non-contact) repellency and activates a specific type of olfactory receptor neurons in mosquito antennae. Furthermore, bioallethrin repellency is significantly reduced in a mosquito mutant of Orco, an obligate olfactory co-receptor that is essential for the function of odorant receptors (Ors). These results indicate that activation of specific Or(s) by bioallethrin contributes to bioallethrin repellency. In addition, bioallethrin repellency was reduced in a pyrethroid-resistant strain which carries two mutations in the sodium channel gene that are responsible for knockdown resistance (kdr) to pyrethroids, indicating a role of activation of sodium channels in bioallethrin repellency. CONCLUSION: Results from this study show that bioallethrin repellency is likely the result of co-activation of Or(s) and sodium channels. These findings not only contribute to the understanding of the modes of action of volatile pyrethroids in spatial repellency, but also provide a framework for developing new repellents based on the dual-target mechanism revealed.