Symbiont community assembly shaped by insecticide exposure and feedback on insecticide resistance of Spodoptera frugiperda

Abstract

Abstract Exploring the mechanism of microbiota assembly and its ecological consequences is crucial for connecting microbiome variation to ecosystem function. However, the influencing factors underlying microbiota assembly in the host-microbe system and their impact on the host phenotype remain unclear. Through investigating the prevalent and worsening ecological phenomenon of insecticide resistance in global agriculture, we found that insecticide exposure significantly changed the gut microbiota assembly patterns of a major agricultural invasive insect pest, Spodoptera frugiperda. The relative importance of various microbiota assembly processes significantly varied with habitat heterogeneity and heterogeneous selection serving as a potential predictor of the host’s insecticide resistance in field populations. Moreover, disturbance of the gut microbiota assembly through antibiotics was revealed to significantly affect the rate and heritability of insecticide resistance evolution, leading to a delay in insecticide resistance evolution in this insect pest. These findings indicate that the gut microbiota assembly process of the insect host is influenced by persistent exposure to habitat conditions, particularly insecticides. This variation in insecticide exposure-related community assembly process subsequently influences the insect host’s insecticide resistance phenotype. This study provides insights into gut microbiota assembly processes from a symbiotic perspective and underscores the significant impact of symbiotic community changes on host phenotypic variation.