Population density triggers wing dimorphism via NlNompC-mediated insulin signaling in Nilaparvata lugens

The Nilaparvata lugens employs wing dimorphism as a key adaptive strategy to environmental heterogeneity. While hormonal pathways and transcription factors governing nutrient-induced wing plasticity are known, how population density triggers developmental divergence remains unresolved. Here, we mechanistically dissect density-dependent wing morph determination, revealing tactile inter-individual contact as the primary signal. High-density conditions amplify gentle-touch frequency, which is detected by mechanosensitive ion channels NlNompC and NlNMDARs. Genetic silencing or pharmacological inhibition of these channels abolished density-induced long-winged morphogenesis. The conserved role of NlNompC in gentle-touch sensation was validated by rescuing tactile perception deficits in Drosophila nompC mutants. Crucially, NlNompC integrates tactile cues into insulin/insulin-like growth factor signaling (IIS): crowding-driven mechanical stimuli upregulate NlIlp3, while suppressing NlInR2, to activate wing elongation programs. Epistasis experiments confirmed IIS as the key downstream pathway, with co-silencing NlInR2 or NlFoxO rescuing the short-winged phenotype induced by NlNompC knockdown or low population density, silencing NlIlp3 or NlInR1 rescuing the long-winged phenotype induced by high population density. Our work uncovers a mechano-endocrine axis linking tactile perception to developmental plasticity, bridging ecological cues with molecular pathways. These findings redefine density sensing beyond chemical modalities and offer actionable targets for disrupting pest dispersal strategies, advancing sustainable agriculture.