Adaptive Evolution Leads to Cross-Species Incompatibility in the piRNA Transposon Silencing Machinery

Publication date: Available online 14 September 2017
Source:Developmental Cell
Author(s): Swapnil S. Parhad, Shikui Tu, Zhiping Weng, William E. Theurkauf
Reproductive isolation defines species divergence and is linked to adaptive evolution of hybrid incompatibility genes. Hybrids between Drosophila melanogaster and Drosophila simulans are sterile, and phenocopy mutations in the PIWI interacting RNA (piRNA) pathway, which silences transposons and shows pervasive adaptive evolution, and Drosophila rhino and deadlock encode rapidly evolving components of a complex that binds to piRNA clusters. We show that Rhino and Deadlock interact and co-localize in simulans and melanogaster, but simulans Rhino does not bind melanogaster Deadlock, due to substitutions in the rapidly evolving Shadow domain. Significantly, a chimera expressing the simulans Shadow domain in a melanogaster Rhino backbone fails to support piRNA production, disrupts binding to piRNA clusters, and leads to ectopic localization to bulk heterochromatin. Fusing melanogaster Deadlock to simulans Rhino, by contrast, restores localization to clusters. Deadlock binding thus directs Rhino to piRNA clusters, and Rhino-Deadlock co-evolution has produced cross-species incompatibilities, which may contribute to reproductive isolation.

Graphical abstract

Teaser

Parhad et al. observe that swapping two rapidly evolving piRNA pathway genes, rhino and deadlock, between Drosophila species makes them non-functional. The species-specific interaction between Rhino and Deadlock supports the idea that these proteins are co-evolving in response to a host-pathogen arms race with transposons, with transposons exhibiting molecular mimicry.


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