Regulation of tick attachment and rapid engorgement via dopamine receptors in the Asian longhorned tick Haemaphysalis longicornis

Abstract

Dopamine plays multifaceted roles in the physiology of insects and ticks, acting as a key neurotransmitter and modulator of various biological processes. In ticks, it plays a particularly important role in regulating salivary gland function, which is essential for successful tick feeding on hosts. Salivary secretion in ticks is orchestrated by the collection of saliva in the acinar lumen mediated by the dopamine receptor (D1) and the expulsion of collected saliva into the salivary duct mediated by the invertebrate specific D1-like dopamine receptor (InvD1L). However, the function of dopamine receptors in different feeding stages and other tissues remains unclear. In this study, D1 and InvD1L of Haemaphysalis longicornis (Haelo-D1 and Haelo-InvD1L, respectively) were found to be involved in tick attachment and the rapid phase of blood feeding. Both receptors were identified and profiled in the synganglion, salivary glands, and midgut of H. longicornis females across different feeding stages. Functional analyses revealed that both receptors were activated by dopamine in a concentration-dependent manner with distinct sensitivities. RNA interference (RNAi) targeting these receptors significantly reduced dopamine-mediated salivation and delayed tick attachment and blood feeding. Furthermore, RNAi prolonged rapid engorgement phases and reduced the final body weight of replete ticks. These results highlight the crucial roles of D1 and InvD1L in regulating salivary secretion in ixodid ticks and facilitating their attachment and rapid engorgement, thereby offering potential targets for novel tick control strategies aimed at disrupting feeding and reducing pathogen transmission.