Summary:

Paracentric inversions are very common structural variants in many species of the genus Drosophila. Despite a large body of literature, still very little is known about the genetic mechanisms underlying inversion polymorphisms. Recent advances in sequencing technology now allow studying the distribution of genetic variation on a genome-wide level, which has reignited interest in the genomic basis of inversion evolution. To extend previous efforts we have combined karyotyping of polytene chromosomes with whole-genome sequencing in order to identify polymorphic inversions and examine associated haplotype structure in populations derived from a laboratory natural selection experiment in D. melanogaster. In addition, we combined information from 110 D. melanogaster genomes of known karyotype from Africa, Europe and North America to investigate patterns and distribution of fixed differences linked to different inversions. We used this novel dataset to estimate inversion frequencies from pooled next generation sequencing data (“Pool-Seq”) in our selection experiment and in populations collected along the North American and Australian latitudinal cline. Among six polymorphic inversions segregating in the experimental populations, two rare cosmopolitan inversions, In(3R)C and In(3R)Mo, showed a frequency increase consistent with non-neutral evolution. Genetic variation in and around In(3R)Mo was strongly reduced, consistent with previous findings from North America, and we found evidence for gene flux between this inversion and the non-inverted standard arrangement. Moreover, we identified a previously unknown latitudinal cline for In(3R)Mo in our Pool-Seq data from the North America east coast. Our novel data highlight the impact of inversions on patterns genetic variation and underline the importance of considering structural variants when attempting to detect patterns of adaptation.