Evidence for the Robustness of Protein Complexes to Inter-Species Hybridization
Despite the tremendous efforts devoted to the identification of genetic incompatibilities underlying hybrid sterility and inviability, little is known about the effect of inter-species hybridization at the protein interactome level. Here, we develop a screening platform for the comparison of protein–protein interactions (PPIs) among closely related species and their hybrids. We examine in vivo the architecture of protein complexes in two yeast species (Saccharomyces cerevisiae and Saccharomyces kudriavzevii) that diverged 5–20 million years ago and in their F1 hybrids. We focus on 24 proteins of two large complexes: the RNA polymerase II and the nuclear pore complex (NPC), which show contrasting patterns of molecular evolution. We found that, with the exception of one PPI in the NPC sub-complex, PPIs were highly conserved between species, regardless of protein divergence. Unexpectedly, we found that the architecture of the complexes in F1 hybrids could not be distinguished from that of the parental species. Our results suggest that the conservation of PPIs in hybrids likely results from the slow evolution taking place on the very few protein residues involved in the interaction or that protein complexes are inherently robust and may accommodate protein divergence up to the level that is observed among closely related species. Independently evolving lineages accumulate mutations that are compatible within lineage but that may be incompatible among lineages. These incompatibilities are expected to accumulate among gene products that act together to produce a phenotype or that interact with each other physically. Genes coding for proteins that assemble into protein complexes co-evolve with each other in order to maintain these interactions over evolutionary time. These protein complexes are therefore potential hotspots for the accumulation of molecular incompatibilities. Because of the lack of molecular tools, this question has not been systematically addressed. Here, we develop a platform to measure, in vivo, the divergence of protein complexes in different yeast species and their perturbation in their F1 hybrids. We find that, despite a level of protein divergence that is as high as that observed between birds and mammals, most protein–protein interactions are highly conserved between species and are not perturbed in hybrids. Contrary to our expectations, our results show that protein complexes may be robust to inter-species hybridization and may not be a major contributor of incompatibilities to the reproductive isolation of recently formed species.