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Natural environments expose organisms to multifarious selective pressures involving numerous aspects of the overall phenotype, therefore eliciting a response from multiple correlated loci. It has been hypothesized that chromosomal rearrangements can play a role in facilitating local adaptation by establishing new linkage relationships and modifying the recombination patterns between the different chromosomal forms, allowing coordinated adaptation of several loci. The central aim of the work presented here is to test this hypothesis using Drosophila americana as a model system. This species segregates several inversions and an X-4 centromeric fusion which makes it an excellent model to study the role of chromosomal rearrangements on local adaptation.
This hypothesis was tested using several approaches. The geographic distribution of the chromosomal rearrangements was determined through sampling of wild populations from a broad geographic range. It was found that several of the chromosomal rearrangements exhibit clinal variation. Furthermore, many of these are found in high linkage disequilibrium. The X-4 fusion is highly associated with inversions on the X and 4th chromosome. Also, two inversions on chromosome 5 are in strong negative linkage disequilibrium.
The sequence variation associated with rearrangements of the X was studied using inbred lines. The results show that the inversion and the fusion strongly influence variation on this chromosome. Regions of significant population differentiation and linkage with the rearrangements are found interspersed with loci showing neutral variation indicating that in spite of recombination, allelic associations are maintained on this chromosome.
The analysis was also extended to flies directly collected from the wild sampled from a region encompassing a large part of the species' range. Loci throughout chromosome X and 4 were genotyped. Sites in high linkage disequilibrium with the rearrangements and with other assayed sites were found in close proximity with sites that did not show this pattern.
In conclusion, the clinal distribution of chromosomal rearrangements and associated genetic variation in conjunction with the detection of islands of linkage disequilibrium among the rearrangements and loci on both chromosomes indicate that chromosomal rearrangements are facilitating local adaptation in D. americana.