Distinct Genetic Footprint of Adaptation Observed Within Anopheles gambiae Taxa from The Gambia

Emerging evidence suggests presence of novel or unclassified taxa within the Anopheles gambiae s.l. species complex, the principal vector of malaria in sub-Saharan Africa. The response of these new lineages to standard vector control tools and/or adaptation to selection pressure is currently unknown, underscoring the need for further characterization. We performed a genome-wide selective scan (GWSS) analysis to gain genomic insights into the local adaptation of An. gambiae Bissau molecular form (hereafter "Bissau"), a recently described taxon from The Gambia.

Genomic regions under selection in Bissau primarily code for clusters of gene families associated with metabolic resistance mechanisms against insecticides, specifically Cyp6aa/Cyp6p, Cyp9K, and Gste. Notably, a distinct signal of selection for the Choline acetyltransferase gene (ChAT) was detected in the chromosome arm 2R of Bissau. In the sibling taxa An. coluzzii, two distinctive signals of selection overlapping E-ubiquitin protein and N-acetyltransferase genes were evident. These unique genes warrant further functional validation and monitoring to confirm their potential role as molecular markers for target site resistance. A selective sweep spanning clusters of odorant receptor (OR) genes, usually associated with chemosensory, was also unique to Bissau. Diplotype clustering of OR regions revealed six groups with low heterozygosity and non-synonymous mutations, suggesting local adaptation to fundamental biological traits such as host seeking and habitat selection. Haplotype clustering analysis ruled out adaptive sharing of OR alleles, depicting ongoing independent evolution of chemosensory perception in Bissau population. Contrastingly, the sharing of adaptive alleles was evident between An. gambiae s.s and Bissau in regions coding metabolic resistance genes, potentially facilitating the spread of insecticide resistance across taxa.

Common and taxon-specific signatures of selection are evolving in An. gambiae s.l. needing further studies and monitoring to guide targeted vector control efforts.