Long-Term Selection with α-Solanine Enhances Tolerance and Drives Multilevel Physiological Remodeling in Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae).

The fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), is a polyphagous pest exposed to plant defensive chemicals. We tested whether sustained selection by the potato steroidal glycoalkaloid α-solanine induces changes in tolerance, life-history performance, and physiology. A potato-sprout-derived preparation was standardized for α-solanine content by targeted LC-ESI-MS/MS, and a selected line was maintained for 12 generations on a diet containing 1.0 mg α-solanine g-1. Selected and unselected lines were compared across normal artificial diet, α-solanine diet, and potato foliage using bioassays, life-history analyses, detoxification-enzyme assays, untargeted metabolomics, and RT-qPCR. By generation 12, the selected line reached a tolerance ratio of 3.52. Under α-solanine exposure, selection shortened larval, pupal, adult, and total development and increased pupation, adult emergence, and egg hatch, while pupal mass and fecundity did not differ significantly between lines. The selected line showed faster demographic turnover. Carboxylesterase activity differed between lines, whereas CYP450 and GST responses were diet-dependent. Metabolomic contrasts indicated a reduced feature-level response to α-solanine in the selected line, and RT-qPCR revealed constitutive and diet-dependent shifts in detoxification- and stress-related genes. Thus, sustained α-solanine selection generated coordinated multilevel remodeling that improved performance under α-solanine exposure and altered responses to potato foliage.