P-elements strengthen reproductive isolation within the Drosophila simulans species complex

Abstract

Determining mechanisms that underlie reproductive isolation is key to understanding how species boundaries are maintained in nature. Transposable elements (TEs) are ubiquitous across eukaryotic genomes. However, the role of TEs in modulating the strength of reproductive isolation between species is poorly understood. Several species of Drosophila have been found to harbor P-elements (PEs), yet only D. simulans is known to be polymorphic for their presence in wild populations. PEs can cause reproductive isolation between PE-containing (P) and PE-lacking (M) lineages of the same species. However, it is unclear whether they also contribute to the magnitude of reproductive isolation between species. Here, we use the simulans species complex to assess whether differences in PE status between D. simulans and its sister species, which do not harbor PEs, contribute to multiple barriers to gene flow between species. We show that crosses involving a P D. simulans father and an M mother from a sister species exhibit lower F1 female fecundity than crosses involving an M D. simulans father and an M sister-species mother. Our results suggest that the presence of PEs in a species can strengthen isolation from its sister species, providing evidence that transposable elements can play a role in reproductive isolation and facilitate the process of speciation. IMPACT SUMMARYTransposable elements (TEs) are repetitive genetic units found across the tree of life. They play a fundamental role on the evolution of each species genome. TEs have been implicated in diversification, extinction, and the origin of novelty. However, their potential role in contributing to the maintenance of species boundaries remains largely understudied. Using whole genome sequences, we compared the relative content of TEs across the three species of the Drosophila simulans complex. We find that the presence of one TE, P-element, in D. simulans, and its absence in the sister taxa, differentiates the three species. P-elements (PEs) cause a suite of fitness defects in Drosophila pure-species individuals if their father has PEs but their mother does not, a phenomenon known as hybrid dysgenesis (HD). We thus studied the possibility that PEs enhance isolation between recently-diverged species. In particular, we studied whether the progeny from interspecific crosses were more prone to suffer from HD than pure species. We found that the presence of paternal PEs reduces hybrid female fecundity, mirroring observations of HD described within species. The effect of PEs is stronger in the interspecific hybrids than in pure species. Our results suggest that PEs can strengthen reproductive isolation in well-formed sister species that still hybridize in nature and pose the question of whether other TEs are involved in the formation of species or in their persistence over time.