Evolutionary Genomics of Culex pipiens: Global and Local Adaptations Associated with Climate, Life History Traits and Anthropogenic Factors

We present the first genome-wide study of recent evolution in Culex pipiens species complex focusing on the genomic extent, functional targets and likely causes of global and local adaptations. We resequenced pooled samples of six populations of C. pipiens and two populations of the outgroup C. torrentium. We used Principal Component Analysis to systematically study differential natural selection across populations and developed a phylogenetic scanning method to analyze admixture without haplotype data. We found evidence for the prominent role of geographical distribution in shaping population structure and specifying patterns of genomic selection. Multiple adaptive events, involving genes implicated with autogeny, diapause and insecticide resistance were limited to specific populations. We estimate that about 5-20% of the genes (including several histone genes) and almost half of the annotated pathways were undergoing selective sweeps in each population. The high occurrence of sweeps in nongenic regions and in chromatin-remodeling genes indicated the adaptive importance of gene expression changes. We hypothesize that global adaptive processes in the Culex pipiens complex are potentially associated with South to North range expansion, requiring adjustments in chromatin conformation. Strong local signature of adaptation and emergence of hybrid bridge vectors necessitate genomic assessment of populations before specifying control agents.

我们首次开展了致倦库蚊（Culex pipiens）物种复合体近期进化的全基因组研究，聚焦于其全球与局部适应的基因组范围、功能靶点及潜在成因。我们对6个致倦库蚊种群的混合样本及2个外群物种洪流库蚊（C. torrentium）种群的混合样本进行了重测序。我们采用主成分分析（Principal Component Analysis）系统研究了种群间的差异自然选择，并开发了一种系统发育扫描方法，可在无单倍型数据的情况下分析基因流（admixture）。我们发现，地理分布在塑造种群结构及决定基因组选择模式方面发挥着显著作用。涉及孤雌生殖（autogeny）、滞育及抗药性相关基因的多项适应性事件仅局限于特定种群。我们估计，每个种群中约5-20%的基因（包括若干组蛋白基因）及近半数注释通路正经历选择性清除（selective sweeps）。非基因区域及染色质重塑基因中选择性清除的高发生率，表明基因表达变化具有重要的适应性意义。我们推测，致倦库蚊物种复合体的全球适应性过程可能与由南向北的分布范围扩张相关，这需要染色质构象发生调整。强烈的局部适应特征及杂交桥媒介的出现，使得在确定防控媒介前对种群进行基因组评估成为必要。