Adaptive evolution of invasive fall armyworms to maize with potential involvement of Cytochrome P450 genes

• Published in: BMC genomics 2024-10, Vol.25 (1), p.949-12, Article 949
• Main Authors: Yainna, Sudeeptha, Hilliou, Frédérique, Haenniger, Sabine, d'Alençon, Emmanuelle, Brévault, Thierry, Nam, Kiwoong
• Format: Article
• Language: English
• Subjects: Adaptation (Biology); Adaptation, Physiological - genetics; Adaptive sampling; Agricultural production; Animals; Army-worms; Control; Corn; Cytochrome; Cytochrome P-450 Enzyme System - genetics; Cytochrome P450; Cytochromes P450; Datasets; Diseases and pests; Environmental aspects; Evolution; Evolution & development; Evolution, Molecular; Evolutionary genetics; Fall armyworm; Gene expression; Genes; Genetic analysis; Genetic aspects; Genomes; Genomic analysis; Genomics; Grasses; Growth; Host-plant adaptation; Identification and classification; Indigenous species; Insecticides; Insects; Introduced Species; Invasive species; Invasive success; Larva - genetics; Life Sciences; Metabolites; Phylogenetics; Population genetics; Principal components analysis; Rice; Sorghum; Spodoptera - genetics; Spodoptera frugiperda; Strain analysis; Success; Survival; Transcriptome; Transcriptomics; Zea mays - genetics; Zea mays - parasitology
• ISSN: 1471-2164; 1471-2164
• DOI: 10.1186/s12864-024-10845-7

An invasion occurs when introduced species establish and maintain stable populations in areas outside of their native habitat. Adaptive evolution has been proposed to contribute to this process. The fall armyworm (Spodoptera frugiperda) is one of the major pest insects infesting maize in both invaded and native areas. The invasion of this species was reported from West Africa in 2016, followed by spreading across the Old World. We tested adaptive evolution to maize using 56 native samples from the USA and 59 invasive samples from Senegal, based on genomic and transcriptomic analyses. Principal component analysis revealed that the Senegalese population originated from corn strain. Three genetic loci were identified as targets of selective sweeps in the Senegalese population. These loci include four Cytochrome P450 genes (CYP321B1, CYP321B3, CYP321B4, and CYP337B5), as well as 12 genes of which the function is unclear. Transcriptomic analysis showed an overexpression of CYP321B1 and CYP321B3 genes in sfC samples compared to sfR samples. Additionally, these two genes were overexpressed when corn strain samples were exposed to maize. In larval feeding assays, the Senegalese population exhibited higher survival rates than a Floridan population across all four tested maize varieties. These results suggest that the analyzed Senegalese population experienced adaptive evolution involving loci containing CYP genes, potentially associated with an increase in the survival rates on maize. We argue that the invasive success of the fall armyworm is contributed by stabilizing selection to maize.