Pesticide-induced resurgence of the brown planthopper is mediated by diverse actors that promote juvenile hormone biosynthesis and female fecundity

Abstract Pesticide-induced resurgence, increases in pest insect populations following pesticide application, is a serious threat to the sustainable control of many highly damaging crop pests. Resurgence can result from pesticide-enhanced pest reproduction, however, the molecular mechanisms mediating this process remain unresolved. Here we show that brown planthopper (BPH) resurgence following emamectin benzoate (EB) exposure results from the coordinated action of a diverse suite of actors that regulate juvenile hormone (JH) levels, resulting in increased JH titer in adult females and enhanced fecundity. Following reports of BPH resurgence in rice crops when this species is exposed to EB, we demonstrate that EB treatment results in profound changes in female BPH fitness including enhanced ovarian development and elevated egg production. This enhanced reproductive fitness results from the EB-mediated upregulation of key genes involved in the regulation of JH, including JHAMT, Met and Kr-h1 and the downregulation of allatostatin ( AstA ) and allatostatin receptor ( AstAR ) expression. The remodulation of gene expression following EB exposure is dependent on the action of this insecticide on its molecular target the glutamate-gated chloride channel (GluCl) receptor. Collectively, these results provide mechanistic insights into the regulation of negative pesticide-induced responses in insects and reveal the key actors involved in the JH-signaling pathway that underpin pesticide resurgence. Significance Pesticides remain a key means of controlling many of the world’s insect pests, however, in some cases, pesticide applications can result in resurgence of pest populations due to pesticide-induced increases in fecundity. In the current study we show that pesticide resurgence in the brown planthopper (BPH) following exposure to the insecticide emamectin benzoate results from the transcriptional reprogramming of a diverse suite of positive and negative regulators of juvenile hormone (JH), a critical regulator of insect development and reproduction. This in turn leads to profound increases in female BPH reproductive fitness and enhanced fecundity. Our findings unravel the molecular mechanisms mediating pesticide-induced pest resurgence and inform the development of novel strategies to control highly damaging crop pests.