Serotonin-mediated wing dimorphism in Nilaparvata lugens: A survival strategy triggered by host plant senescence

The molecular mechanisms by which insects perceive and behaviorally adapt to host plant nutritional variation constitute a fundamental question in insect-plant coevolution. The brown planthopper (Nilaparvata lugens, BPH), a monophagous pest of rice (Oryza sativa), exhibits striking wing dimorphism that directly governs its outbreak patterns: long-winged morphs (LW) initiate migration to escape low-quality hosts, while short-winged morphs (SW) drive local population explosions, thriving in high-quality hosts. However, the mechanism underlying this migration-residence behavior in response to host plant senescence remains unclear. Here, we identified early 4th and early 5th instars as sensitive stages in response to the yellow-ripe rice, a phenological stage marking the onset of host plant senescence that must be promptly avoided. High-performance liquid chromatography (HPLC) revealed that serotonin (5-HT) levels were significantly increased in BPHs during the sensitive stages. Exogenous administration of 5-HT and its precursor 5-hydroxytryptophan (5-HTP) significantly promoted long-winged morph development, whereas pharmacological inhibition with α-methyltryptophan (AMTP, a serotonin synthesis inhibitor) attenuated the wing dimorphism response to yellow-ripe rice. Identification and functional analysis of 5-HT synthesis pathway enzymes suggested that tryptophan hydroxylase (NlTRH) and aromatic L-amino acid decarboxylase (NlAADC) regulated the expression of insulin-like peptide 3 (NlIlp3), subsequently regulating the expression of insulin receptors 1 and 2 (NlInR1, NlInR2), which control wing dimorphism. In contrast, phenylalanine hydroxylase (NlPAH) showed no involvement. This study highlights the vital role of serotonin in wing dimorphism of BPH in response to host plant senescence and offers new targets for sustainable control of the pest.