The effect of population density on the phenotype, metabolic and immunological adaptations in the cuticle of Spodoptera litura larvae.

Background: Species that experience outbreaks and those that display density-dependent phase polymorphism demonstrate density-dependent prophylaxis (DDP) by increasing their immune investment in response to increasing densities. Despite this phenomenon, the mechanisms of DDP remain largely unexplored.

Results: Here, we showed that Spodoptera litura exhibited heightened cuticular melanization and enhanced cuticular immune responses when reared at higher population density. Transcriptomic analysis identified differentially expressed genes (DEGs) associated with immune responses, nutritional metabolism, and cuticular synthesis in the cuticle, revealing the molecular underpinnings of density-dependent plasticity in larval cuticles. Gregarious S. litura larvae exhibited significant up-regulation of immune-related genes, particularly those in the Toll and immune deficiency (IMD) signaling pathways and tyrosine metabolism, suggesting a strategic enhancement of immune defenses. Concurrently, a reduced lipid metabolism was observed in the cuticle of gregarious larvae, with suppressed expression of key genes in the fatty acid synthesis, leading to a decrease in integument triglyceride content. The immune defense of gregarious larvae was further amplified by increased expression of cuticle- and melanin formation-related genes, and reduced chitin degradation, reinforcing the cuticle as a physical barrier against pathogens.

Conclusion: Our findings clarify that shifts in phenotypic plasticity, metabolic pathways, and immune response mechanisms underscore the adaptability of insects to population density changes and their consequent vulnerability to pathogens, offering new directions and insights for uncovering the mechanisms underlying pest outbreaks and for enhancing the effectiveness of biological control measures by targeting gregarious immunity. © 2025 Society of Chemical Industry.