Genomic diversity, evolution, and adaptation of Anopheles bwambae to the extreme thermal spring waters in Uganda
Résumé
The closely related and partially interfertile mosquito species of the Anopheles gambiae complex (AGC) include the major vectors of human malaria in Africa. While these have attracted much attention, little is known about minor vectors like An. bwambae. This species is highly specialized to the thermal springs in Bwambae County (Uganda), in close vicinity with other major vectors (e.g., An. gambiae). Previously reported potential introgression between them raised questions about how such species remain adapted despite the homogenizing effects of gene flow. Here we investigated the genomic diversity and evolutionary history of An. bwambae, together with its extreme adaptations tothermal spring waters. We first de novo assembled the reference genome for this species and compared it to those from other species of the AGC. Then, using whole genome sequencing, bioinformatics, population genomics, and phylogenomics approaches, we investigated the genetic diversity, evolutionary history, and adaptation of An. bwambae (n=42) compared to An. gambiae (n=25). Analyses of 13.5 million SNPs across the genomes of the two species revealed major genomic heterogeneity including a new inversion system on the X chromosome of An. bwambae. Genetic structure confirmed that the two species are well distinct, with no evidence of recent gene flow. Nevertheless, historical introgrossion was detected not only with An. gambiae, but also with other species of the AGC. In contrast to An. gambiae, An. bwambae displayed low diversity, strong inbreeding, and autozygosity, indicative of a very small population. Meanwhile, while genome scans revealed strong positive selection signals on known insecticide resistance loci in An. gambiae, no such signal was identified in An. bwambae. Genome scans revealed a few genomic regions potentially undergoing introgression, while the majority did not. How An. bwambae persisted and adapted despite its small population size and strong inbreeding remains a paradox warranting further investigation.