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.