Hybrid incompatibility is stronger in the presence of transposable elements in the Drosophila virilis clade

Abstract

AbstractMismatches between parental genomes in selfish elements are frequently hypothesized to underlie hybrid dysfunction and drive speciation. However, because the genetic basis of most hybrid incompatibilities is unknown, testing the contribution of selfish elements to reproductive isolation is difficult. Here we evaluated the role of transposable elements (TEs) in hybrid incompatibilities between Drosophila virilis and D. lummei by experimentally comparing hybrid incompatibility in a cross where active TEs are present in D. virilis (TE+) and absent in D. lummei, to a cross where these TEs are absent from both D. virilis (TE−) and D. lummei genotypes. Using genomic data, we confirmed copy number differences in TEs between the D. virilis (TE+) strain and a D. virilis (TE−) strain and D. lummei. We observed F1 postzygotic reproductive isolation specifically in the interspecific cross involving TE+ D. virilis but not in the cross involving TE-D. virilis. A series of backcross experiments, designed to account for alternative models of hybrid incompatibility, showed that expression of this F1 hybrid incompatibility is consistent with the action of TEs rather than other, genic, interactions. A further Y-autosome interaction contributes to additional, sex-specific, inviability in one direction of this cross combination. These experiments demonstrate that TEs can increase reproductive isolation between closely related lineages, thereby adding to the processes that accelerate speciation.