Chromosomal inversions drive chromosome arm specific patterns of polymorphism in the major African malaria vector, Anopheles funestus

Chromosomal inversions facilitate local adaptation of beneficial mutations and modulate genetic polymorphism, but the extent of their effects within the genome is not fully resolved. The genome of Anopheles funestus, a malaria mosquito endemic to sub-Saharan Africa, contains an impressive number of paracentric polymorphic inversions, which are unevenly distributed among chromosomes and provide an excellent framework for investigating the genomic impacts of chromosomal rearrangements. Here we present results of a fine-scale analysis of genetic variation within the genome of two Anopheles funestus ecotypes present in Cameroon. Specifically, we used FST outlier and population genomic analyses to highlight the strong relationship that exists between the presence of inversions and the genomic patterns of divergence and polymorphism in this mosquito. We found evidence that local adaptation in this geographic area is driven by divergent selection within three polymorphic chromosomal inversions, which segregate between savannah and forest ecosystems. Importantly, in contrast to the 2L chromosome arm, which is collinear, nucleotide diversity is significantly reduced along the entire length of three autosome arms bearing multiple overlapping chromosomal rearrangements. These findings support the idea that interactions between reduced recombination and selection within chromosomal rearrangements contribute to sculpt nucleotide polymorphism across entire chromosomes in An. funestus.