Multigenerational feeding increases adaptability to alternative hosts by shifting protective enzyme profiles and...

Host plant adaptability drives the ecological plasticity and global expansion of Spodoptera frugiperda (J.E. Smith, 1797). However, the mechanisms underlying the long-term adaptation of its maize ecotype to alternative hosts remain unclear, hindering host-shift risk predictions. We evaluated the host-shift risk of the maize ecotype of S. frugiperda across four generations of continuous rearing on maize (Zea mays L.), wheat (Triticum aestivum L.), rice (Oryza sativa L.), and green bristlegrass (Setaria viridis (L.) P. Beauv.) by analyzing biological performance, feeding and oviposition behaviours feeding/oviposition preferences, and protective enzyme dynamics. Prolonged monophagous feeding significantly accelerated developmental cycles across generations. Wheat emerged as the most suitable host under laboratory conditions, shortening immature stages to 22.86 d (F₃) and increasing pupal weight by 40.7%, whereas S. viridis resulted in the lowest fitness, with 32.31-d immature period and 59.33% survival rate (F₄). Larval feeding and adult oviposition preferences consistently aligned with multigenerational feeding on the same host. Enzymatic profiling showed maize-fed larvae maintained the lowest catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD), whereas S. viridis-reared larvae exhibited peak enzyme activities. Notably, adaptation to wheat was associated with reduced enzymatic stress responses, with CAT and POD activities decreasing by 21.8% and 17.5%, respectively, from F₁ to F₃, indicating physiological acclimation. These findings suggest that multigenerational feeding can enhance population fitness and promote host preference through physiological and behavioural plasticity. This laboratory study indicates the potential for the maize ecotype to pose threat to wheat production, providing a basis for managing.