Permethrin elicits chemoreceptive responses on different Anopheles gambiae sensory appendages

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ABSTRACT BACKGROUND Non-contact detection of pyrethroid insecticides by malaria mosquitoes has been unveiled and may contribute to the evolution of mosquito behavioral modifications against vector control tools. However, the mechanisms underlying this detection are not yet fully understood. It has been hypothesized that the spatial repellency of pyrethroids may be mediated by chemosensory receptors and/or via the activation of voltage-gated sodium channels (VGSCs). This study aimed to explore these two hypotheses by identifying which chemosensory appendages in Anopheles gambiae are involved in the non-contact detection of permethrin, a widely used pyrethroid in malaria control. RESULTS Behavioral responses to permethrin headspace were recorded in female An. gambiae , in which specific sensory appendages were either removed or coated with resin to impair their chemosensory function. Additionally, electrophysiological recordings were performed on different sensory appendages: antennae, palpi and tarsi, to characterize their electrophysiological activity after permethrin stimulation. The behavioral assays revealed that tarsi were primarily responsible for mediating mosquito takeoff responses after permethrin headspace delivery. This finding was supported by significant electrophysiological tarsal responses to the insecticide. In contrast, removal of the antennae did not alter behavioral responses, although electroantennogram recordings indicated neural activity in response to permethrin. The palps showed neither behavioral nor electrophysiological responses. CONCLUSION These findings indicate that permethrin is detected through two distinct sensory appendages, tarsi and antennae, but with varying behavioral output. Such appendage-specific detection favors the hypothesis that permethrin detection and the associated behavioral output is mediated by chemosensory receptors rather than by VGSCs. Nonetheless, further investigations are needed to identify the chemosensory receptors and pathways involved in pyrethroid insecticide detection in malaria mosquitoes.

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