Comparison of the signaling pathways of wing dimorphism regulated by biotic and abiotic stress in the brown planthopper

Wing polymorphism is an evolutionary trait that is widely present in various insects and provides a model system for studying the evolutionary significance of insect dispersal. The brown planthopper (BPH, Nilaparvata lugens) can alter its wing morphs under biotic and abiotic stress. However, whether differential signaling pathways are induced by the 2 types of stress remain largely unknown. Here, we screened a number of candidate genes through weighted gene co‐expression network analysis (WGCNA) and found that ornithine decarboxylase (NlODC), a key enzyme in the synthesis of polyamines, was associated with wing differentiation in BPH and mainly responded to abiotic stress stimuli. We analyzed the Kyoto Encyclopedia of Genes and Genomes enrichment pathways of differentially expressed genes under the 2 stresses by transcriptomic comparison, and found that biotic stress mainly influenced insulin‐related signaling pathways while abiotic stress mainly influenced hormone‐related pathways. Moreover, we found that insulin receptor 1 (NlInR1) may regulate wing differentiation of BPH by responding to both biotic and abiotic stress, but NlInR2 only responded to biotic stress. Similarly, the juvenile hormone epoxide hydrolase associated with juvenile hormone degradation and NlODC may regulate wing differentiation mainly through abiotic stress. A model based on the genes and stresses to modulate the wing dimorphism of BPH was proposed. These findings present a comprehensive molecular mechanism for wing polymorphism in BPH induced by biotic and abiotic stress. Graphical Brown planthopper can be induced to differentiate toward long wings under both biotic and abiotic stress, but the in vivo molecular mechanisms associated with this plastic phenotypic change induced by stresses are distinct. The response to biotic stress was mainly through the insulin signaling pathway, while the response to abiotic stress was mainly through the juvenile hormone signaling pathway. Although further definitive and in‐depth testing of the 2 signaling pathways is necessary, the results of the current study are important for understanding the molecular mechanisms underlying the changes in phenotypic plasticity of species in response to environmental stresses.