Positive Selection Drives Mitochondrial Gene Rearrangement in Sternorrhyncha (Insecta: Hemiptera)

Sternorrhyncha, a suborder of Hemiptera, comprises sap-feeding insects with piercing-sucking mouthparts, most of which are important agricultural and forestry pests, including aphids, psyllids, whiteflies, and scale insects. While the mitochondrial genome is a highly accessible molecular source for high-level and large-scale phylogenetic studies, a comprehensive mitochondrial phylogenomic investigation of Sternorrhyncha has been lacking. This deficiency is primarily attributable to the challenges associated with obtaining mitochondrial genomes from Coccoidea. We have constructed the largest mitochondrial dataset for Sternorrhyncha to establish phylogenetic relationships, to examine the interrelationships, and to assess the phylogenetic results. Based on phylogenetic trees and mitogenomic gene arrangement synapomorphies, our findings confirm a sister-group relationship between Coccoidea and Aphidoidea, and demonstrate the affiliation of Aclerdidae with Coccidae. Additionally, we have examined the mitochondrial gene rearrangements in Sternorrhyncha. Mitochondrial genes in Coccoidea and Aleyrodoidea display a notable prevalence of translocation and a high proportion of positive selection pressures, which correlates with their large species diversity. Conversely, most aphid genes are under negative selection pressure, and pairwise identity analysis reveals relatively modest low variation among aphid lineages, highlighting a paradox of species diversification underlain by conserved mitochondrial genomic changes.