Mitochondrial variation inAnopheles gambiaeandAn. coluzzii: phylogeographic legacy of species isolation and mito-nuclear associations with metabolic resistance to pathogens and insecticides

Abstract

AbstractMitochondrial DNA (mtDNA) has been a popular marker in phylogeography, phylogeny, and molecular ecology, but its complex evolution is increasingly recognized. Here, we investigated mtDNA variation inAn. gambiaeandAn. coluzzii, in perspective with other species in theAnopheles gambiaecomplex (AGC), by assembling the mitogenomes of 1219 mosquitoes across Africa. The mtDNA phylogeny of the AGC was consistent with a previously reported highly reticulated evolutionary history, revealing important discordances with the species tree. The three most widespread species (An. gambiae, An. coluzzii, An. arabiensis), known for extensive historical introgression, could not be discriminated based on mitogenomes. Furthermore, a monophyletic clustering of the three salt-water tolerant species (An. merus, An. melas, An. bwambae) in the AGC also suggested that introgression and possibly selection shaped mtDNA evolution. MtDNA variation inAn. gambiaeandAn. coluzziiacross Africa revealed significant partitioning among populations and species. A peculiar mtDNA lineage found predominantly inAn. coluzziiand in the hybrid taxon of the African “far-west”exhibited divergence comparable to the inter-species divergence in the AGC, with a geographic distribution matching closelyAn. coluzzii’s geographic range. This phylogeographic relict of theAn. coluzziiandAn. gambiaesplit was associated with population and species structuration, but not withWolbachiaoccurrence. The lineage was significantly associated with SNPs in the nuclear genome, particularly in genes associated with pathogen and insecticide resistance. These findings underline the mito-nuclear coevolution history and the role played by mitochondria in shaping metabolic responses to pathogens and insecticide inAnopheles.