Transcriptional profiling of Dermacentor variabilis (Acari: Ixodidae) provides insights into the role of the Haller's organ in spatial DEET recognition

Abstract

DEET is the most common active ingredient in commercial repellents, providing effective protection against blood-sucking insects and ticks. However, its mode of action is not fully understood, with several theories put forward to explain its repellency effect. Unique to ticks, the Haller's organ recognizes a variety of external stimuli through non-contact mechanisms, yet the extent to which the organ plays a role in tick chemoreception is not fully known. We previously found that DEET inhibited the expression/activity of cytochrome P450s and cholinesterases in Dermacentor variabilis, however, our experimental design could not distinguish between sexes (males/females), method of exposure (volatile/tactile) or the roles of chemosensory tissues (Haller's organ). In this study, we used RNA sequencing to assess changes in transcript expression induced by volatile DEET in D. variabilis males/females with/without intact Haller's organs. Male ticks showed much greater transcriptional responses to DEET than females, which may be at least partially attributed to the sexual dimorphism of the Haller's organ. Female transcript expression profiles were most influenced by condition (i.e., intact/excised Haller's organs) with minimal changes due to repellent exposure. On the other hand, removal of the Haller's organs caused DEET treated male ticks to exhibit similar expression profiles as control (ethanol) ticks with intact Haller's organs. Consequently, the transcript-level responses to spatial DEET exposure appears largely based on males possessing their Haller's organs. The molecular signature of this response included the suppression of a large number of transcripts involved in detoxification, lipid metabolism and immunity. Taken collectively, this study furthers our understanding of the Haller's organ role in volatile DEET recognition.