Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, Groningen 9747 AG, Netherlands.
MIVEGEC, University of Montpellier, CNRS, IRD, Montpellier, France.
Genome Biol Evol. 2024 Sep 3;16(9). doi: 10.1093/gbe/evae172.
Mitochondrial DNA has been a popular marker in phylogeography, phylogeny, and molecular ecology, but its complex evolution is increasingly recognized. Here, we investigated mitochondrial DNA variation in Anopheles gambiae and Anopheles coluzzii, in relation to other species in the Anopheles gambiae complex, by assembling the mitogenomes of 1,219 mosquitoes across Africa. The mitochondrial DNA phylogeny of the Anopheles gambiae complex was consistent with previously reported highly reticulated evolutionary history, revealing important discordances with the species tree. The three most widespread species (An. gambiae, An. coluzzii, and Anopheles arabiensis), known for extensive historical introgression, could not be discriminated based on mitogenomes. Furthermore, a monophyletic clustering of the three saltwater-tolerant species (Anopheles merus, Anopheles melas, and Anopheles bwambae) in the Anopheles gambiae complex also suggested that introgression and possibly selection shaped mitochondrial DNA evolution. Mitochondrial DNA variation in An. gambiae and An. coluzzii across Africa revealed significant partitioning among populations and species. A peculiar mitochondrial DNA lineage found predominantly in An. coluzzii and in the hybrid taxon of the African "far-west" exhibited divergence comparable to the interspecies divergence in the Anopheles gambiae complex, with a geographic distribution matching closely An. coluzzii's geographic range. This phylogeographic relict of the An. coluzzii and An. gambiae split was associated with population and species structure, but not with the rare Wolbachia occurrence. The lineage was significantly associated with single nucleotide polymorphisms in the nuclear genome, particularly in genes associated with pathogen and insecticide resistance. These findings underline potential mitonuclear coevolution history and the role played by mitochondria in shaping metabolic responses to pathogens and insecticides in Anopheles.
线粒体 DNA 一直是系统地理学、系统发育学和分子生态学中的热门标记，但人们越来越认识到其复杂的进化过程。在这里，我们通过组装非洲 1219 只蚊子的线粒体基因组，研究了冈比亚按蚊和库蚊的线粒体 DNA 变异，以及与冈比亚按蚊复合体中的其他物种的关系。冈比亚按蚊复合体的线粒体 DNA 系统发育与之前报道的高度网状进化历史一致，显示出与种系发生树的重要不和谐。三个分布最广的物种（冈比亚按蚊、库蚊和 A. arabiensis），因其广泛的历史基因渗入而闻名，不能根据线粒体基因组来区分。此外，三种耐盐性物种（冈比亚按蚊、淡色按蚊和 A. bwambae）在冈比亚按蚊复合体中的单系聚类也表明基因渗入和可能的选择塑造了线粒体 DNA 的进化。非洲各地冈比亚按蚊和库蚊的线粒体 DNA 变异显示出种群和物种之间存在显著的分化。在库蚊中主要发现的一个特殊的线粒体 DNA 谱系，以及在非洲“远西部”的杂交分类群中发现的一个特殊的线粒体 DNA 谱系，其分化程度与冈比亚按蚊复合体中的种间分化相当，其地理分布与库蚊的地理范围非常吻合。这种冈比亚按蚊和库蚊分化的线粒体 DNA 地理残余与种群和物种结构有关，但与罕见的沃尔巴克氏体无关。该谱系与核基因组中的单核苷酸多态性显著相关，特别是与病原体和杀虫剂抗性相关的基因。这些发现强调了潜在的核质协同进化历史以及线粒体在塑造对病原体和杀虫剂的代谢反应方面在按蚊中的作用。
