Genomics of Natural Populations: Gene Conversion Events Reveal Selected Genes within the Inversions of Drosophila pseudoobscura

When adaptive phenotypic variation maps within an inverted segment of a chromosome, researchers often despair because it is thought that the suppression of crossing over will prevent the discovery of selective target genes through fine scale genetic mapping. If an inversion polymorphism is old enough, then the accumulation of gene conversion tracts offers the promise that QTLs or selected loci within inversions can be identified. This study uses the inversion polymorphism of Drosophila pseudoobscura as a model system to determine if gene conversion analysis can be a useful tool for mapping adaptive loci within inversions. D. pseudoobscura has over 30 different chromosomal arrangements on the third chromosome (Muller C) in natural populations and their frequencies vary with changes in environmental habitats. Statistical tests identified outlier genes within inverted regions based on local clusters of fixed SNP differences. These outlier genes also had potentially selectable variation, either fixed amino acid differences or differential expression patterns among arrangements. Here, we use genome sequences of the inverted third chromosome (Muller C) to infer 98,443 gene conversion tracts for a total coverage of 142 Mb. We tested whether the frequency of gene conversion tracts in outlier versus non-outlier genes were equal. Gene conversion tracts occur less frequently in outlier versus non-outlier genes suggesting that selection removes exchanged DNA from multiple outlier genes. These data support the hypothesis that these inversions captured adaptive alleles and that strong epistatic selection removes recombinants generated through gene conversion. The pattern and organization of genetic diversity in the third chromosome in D. pseudoobscura is consistent with the capture of locally adapted combinations of alleles prior to inversion mutation events.