Data from: Chromosomal inversions and ecotypic differentiation in Anopheles gambiae: the perspective from whole-genome sequencing

The molecular mechanisms and genetic architecture that facilitate adaptive radiation of lineages remain elusive. Polymorphic chromosomal inversions, due to their recombination-reducing effect, are proposed instruments of ecotypic differentiation. Here we study an ecologically diversifying lineage of An. gambiae, known as the Bamako chromosomal form based on its unique complement of three chromosomal inversions, to explore the impact of these inversions on ecotypic differentiation. We used pooled and individual genome sequencing of Bamako, typical (non-Bamako) An. gambiae, and the sister species An. coluzzii to investigate evolutionary relationships and genome-wide patterns of nucleotide diversity and differentiation among lineages. Despite extensive shared polymorphism and limited differentiation from the other taxa, Bamako clusters apart from the other taxa, and forms a maximally supported clade in neighbor-joining trees based on whole genome data (including inversions) or solely on collinear regions. Nevertheless, FST outlier analysis reveals that the majority of differentiated regions between Bamako and typical An. gambiae are located inside chromosomal inversions, consistent with their role in the ecological isolation of Bamako. Exceptionally differentiated genomic regions were enriched for genes implicated in nervous system development and signaling. Candidate genes associated with a selective sweep unique to Bamako contain substitutions not observed in sympatric samples of the other taxa, and several insecticide resistance gene alleles shared between Bamako and other taxa segregate at sharply different frequencies in these samples. Bamako represents a useful window into the initial stages of ecological and genomic differentiation from sympatric populations in this important group of malaria vectors.

推动物种谱系适应性辐射的分子机制与遗传结构，迄今仍未得到清晰阐释。多态性染色体倒位（polymorphic chromosomal inversions）因其能够抑制重组的特性，被学界视作生态型分化的关键介导因子。本研究以一条正经历生态分化的冈比亚按蚊（An. gambiae）谱系为研究对象——该谱系因携带三套独特的染色体倒位而被命名为巴马科染色体型——以探究此类倒位对生态型分化的影响。本研究对巴马科型、典型（非巴马科型）冈比亚按蚊以及姊妹种科卢齐按蚊（An. coluzzii）开展了混合样本与单样本基因组测序，以解析各谱系间的演化关系，以及全基因组范围的核苷酸多样性与分化模式。尽管巴马科型与其他类群间存在广泛的共享多态性，且分化程度有限，但在基于全基因组数据（包含倒位区域）或仅基于共线性区域构建的邻接进化树中，巴马科型均单独聚为一支，并形成了支持度最高的单系演化支。然而，FST遗传分化系数（FST）离群值分析结果显示，巴马科型与典型冈比亚按蚊之间的多数分化区域均位于染色体倒位区域内，这与其在巴马科型生态隔离中发挥的作用相符。分化程度极高的基因组区域显著富集于与神经系统发育及信号传导相关的基因中。与巴马科型特有的选择性清除相关的候选基因，携带了其他类群同域样本中未出现的碱基替换；而巴马科型与其他类群共享的数种杀虫剂抗性基因等位基因，在这些样本中的等位基因频率却存在显著差异。作为一类重要的疟疾传播媒介，巴马科型为解析其与同域种群间生态与基因组分化的早期阶段提供了极佳的研究窗口。