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

Abstract

Determining mechanisms that underlie reproductive isolation (RI) 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 RI 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 currently polymorphic for their presence in wild populations. PEs can cause RI 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 RI 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. We also find that another TE, I‐element, might play a minor role in determining the frequency of dysgenesis between species. Our results suggest that the presence of PEs in a species can strengthen isolation from its sister species, providing evidence that TEs can play a role in RI.

Hybrid incompatibility between Drosophila virilis and D. lummei is stronger in the presence of transposable elements

“…Similar studies that examine lineages at a range of stages of TE differentiation could address the contribution of TEs to the accumulation of hybrid incompatibilities over evolutionary time, especially in comparison to ‘ordinary’ genic incompatibilities. At present, our and other recent (Serrato‐Capuchina, D'Agostino, et al, 2021 ), findings suggest that the rapid lineage‐specific evolution of TEs could potentially explain the frequent observation of polymorphic incompatibilities in species that experience dynamic changes in selfish genetic elements, and could therefore represent one of the earliest arising mechanisms of postzygotic reproductive isolation in these groups.…”

“…The generality of these results could be assessed by focussing on other a priori cases where species are known to vary in the number or identity of TEs. For instance, increased reproductive isolation caused by TEs was recently reported in crosses between D. simulans , that are polymorphic for P‐elements , and a sister species, D. sechellia , that completely lack P‐elements (Serrato‐Capuchina, D'Agostino, et al, 2021 ). Similar studies that examine lineages at a range of stages of TE differentiation could address the contribution of TEs to the accumulation of hybrid incompatibilities over evolutionary time, especially in comparison to ‘ordinary’ genic incompatibilities.…”

Hybrid incompatibility between D. virilis and D. lumei is stronger in the presence of transposable elements

“…Similar studies that examine lineages at a range of stages of TE differentiation could address the contribution of TEs to the accumulation of hybrid incompatibilities over evolutionary time, especially in comparison to ‘ordinary’ genic incompatibilities. At present, our and other recent (Serrato-Capuchina et al 2020a), findings suggest that the rapid lineage-specific evolution of TEs could potentially explain the frequent observation of polymorphic incompatibilities in species that experience dynamic changes in selfish genetic elements, and could therefore represent one of the earliest arising mechanisms of postzygotic reproductive isolation in these groups.…”

“…The generality of these results could be assessed by focusing on other a priori cases where species are known to vary in the number or identity of TEs. For instance, increased reproductive isolation caused by TEs was recently reported in crosses between D. simulans , that are polymorphic for P-elements , and a sister species, D. sechellia , that completely lack P-elements (Serrato-Capuchina et al 2020a). Similar studies that examine lineages at a range of stages of TE differentiation could address the contribution of TEs to the accumulation of hybrid incompatibilities over evolutionary time, especially in comparison to ‘ordinary’ genic incompatibilities.…”

Enrichment of hard sweeps on the X chromosome compared to autosomes in sixDrosophilaspecies

“…For D. simulans we downloaded data from 170 inbred lines from a North American population (Signor et al 2018) available at https://zenodo.org/record/154261#.YzMzty2z3jC. For the remaining four species, we obtained genomes from NCBI's RefSeq and short read data from NCBI's Short Read Archive (Garrigan et al 2014;Turissini and Matute 2017;Meany et al 2019;Serrato-Capuchina et al 2021) (Table S1). HaplotypeCaller.…”