Inversions shape the divergence of Drosophila pseudoobscura and Drosophila persimilis on multiple timescales

By shaping meiotic recombination, chromosomal inversions can influence genetic exchange between hybridizing species. Despite the recognized importance of inversions in evolutionary processes such as divergence and speciation, teasing apart the effects of inversions over time remains challenging. For example, are their effects on sequence divergence primarily generated through creating blocks of linkage disequilibrium prespeciation or through preventing gene flux after speciation? We provide a comprehensive look into the influence of inversions on gene flow throughout the evolutionary history of a classic system: Drosophila pseudoobscura and Drosophila persimilis. We use extensive whole-genome sequence data to report patterns of introgression and divergence with respect to chromosomal arrangements. Overall, we find evidence that inversions have contributed to divergence patterns between D. pseudoobscura and D. persimilis over three distinct timescales: (1) segregation of ancestral polymorphism early in the speciation process, (2) gene flow after the split of D. pseudoobscura and D. persimilis, but prior to the split of D. pseudoobscura subspecies, and (3) recent gene flow between sympatric D. pseudoobscura and D. persimilis, after the split of D. pseudoobscura subspecies. We discuss these results in terms of our understanding of evolution in this classic system and provide cautions for interpreting divergence measures in other systems.

Automated summary

Inversions play a significant role in shaping divergence patterns between Drosophila pseudoobscura and Drosophila persimilis over different timescales. They contribute to segregation of ancestral polymorphism early in speciation, gene flow after the split of the two species but before the split of D. pseudoobscura subspecies, and recent gene flow between sympatric populations. These findings provide insights into the evolution of this classic system and caution for interpreting divergence measures in other systems.