Parent-of-origin effect on global gene expression and host-plant adaptation in Spodoptera frugiperda (Lepidoptera: Noctuidae)

Abstract

Spodoptera frugiperda (Fall armyworm, FAW), is a major pest that adapt to many host plants and cause significant economic losses. There are two genetically differentiated FAW strains with different food preferences, the "corn strain" (SfC) and the "rice strain" (SfR). Large transcriptional differences between the strains have been previously documented, which suggested a shift in metabolic homeostasis. In this study, we investigated how parental inheritance can influence FAW metabolism by comparing the larval performance as well as gene expression between FAW strains and their reciprocal hybrids. We recorded life history traits of these genotypes, including larval weight and larval survival rate, when reared on artificial diet or on corn leaves. We observed a previously documented heterosis effect with hybrids gaining more weight than parental lines on both diets. With corn diet, we also observed a significant maternal influence on fitness between the hybrids. We then performed whole genome sequencing and RNA-sequencing on individuals from the same artificial rearing conditions to correlate these differences in fitness with variations on gene expression. We found that the heterosis effect is potentially associated with differentially expressed genes predominantly engaged in immune response and metabolism. The two different hybrid genotypes differed in the expression of RNA gene silencing and oxidative phosphorylation, suggesting a strong effect of parent-of-origin variations on global metabolic homeostasis, as well as a potential involvement of transposable element silencing in compatibilities between the FAW strains genomes, which might explain the differences in FAW plant adaptation.