Roles of spermary-specific carboxylesterases in Nilaparvata lugens reproduction: Opposite between insecticide-induced upregulation and resistance-associated overexpression.

Seminal fluid proteins (SFPs) in insect males are critical for reproduction, being transported into female ovary. In Nilaparvata lugens, a significant rice pest, seven spermary-specific carboxylesterases (CarEs) were found abundantly in SFPs, with over-expression in males of an imidacloprid-resistant (RES) strain compared to a susceptible (SUS) strain. This study aimed to evaluate roles of spermary-specific CarEs in N. lugens reproduction, especially in the reproduction disadvantage in RES. Sublethal doses of three insecticides significantly impacted N. lugens reproduction, concomitant with up-regulation of these CarE genes in males. When RNAi against these CarE genes in SUS males did not affect reproduction, RNAi suppression of insecticide-induced up-regulation worsened the reproductive decline caused by insecticides, indicating a reproduction benefit from the transient up-regulation induced by insecticides. However, constitutive overexpression of these CarEs in RES males did not enhance reproduction and instead imposed a fitness cost. RNAi against part CarE genes in RES males increased reproduction. Collectively, the transient up-regulation and constitutive overexpression of these spermary-expressed CarE genes had the opposite effects on N. lugens reproduction. We need to find a balance between these opposite effects in insect pest control and insecticide resistance management, especially for insecticides targeting reproduction.