Divergent Selection Promotes Intraspecific Genomic Differentiation in Spodoptera littoralis With Possible Involvement in Detoxification

Abstract

The cotton leafworm, Spodoptera littoralis (Lepidoptera: Noctuidae), is a major agricultural pest affecting crops like cotton, maize, tomatoes, and wheat across southern Europe, Africa, the Middle East, and western Asia. Whole genome analyses have revealed adaptive evolution in chemosensation and detoxification genes in S. littoralis. However, the extent of intraspecific diversity influenced by recent adaptive evolutionary forces remains unclear. In this study, we conducted a population genomics analysis using 31 S. littoralis individuals from sub-Saharan Africa, northern Africa, and southern Europe to assess the existence of intraspecific population divergence and identify the underlying evolutionary forces. We show whole genome differentiation between populations based on geographic origin from the analyzed samples. Phylogenetic analyses indicate that sub-Saharan and southern European populations share a common ancestor, distinct from several northern African populations. F_ST and d_XY statistics along the chromosomes reveal loci with restricted gene flow among populations. These loci are associated with population-specific selective sweeps, indicating the role of divergent natural selection in limiting gene flow. Notably, these loci are enriched with detoxification genes, including cytochrome P450, multidrug resistance, and xanthine dehydrogenase genes, all of which are potentially associated with detoxification. These results demonstrate that divergent selection limits gene flow among geographically distinct populations with the possibility of the involvement of detoxification as a key trait. We argue that this genetic heterogeneity can be considered in pest monitoring and management, as strategies tailored to specific populations may not be relevant for others.