A pair of centromeric proteins mediates reproductive isolation in Drosophila species

Speciation involves the reproductive isolation of natural populations due to the sterility or lethality of their hybrids. However, the molecular basis of hybrid lethality and the evolutionary driving forces that provoke it, remain largely elusive. The hybrid male rescue (Hmr) and the lethal hybrid rescue (Lhr) genes serve as a model to study speciation in Drosophilids as their interaction causes lethality in male hybrid offspring. Here we show that HMR and LHR form a centromeric complex necessary for proper chromosome segregation. We find that the Hmr expression level is substantially higher in D. melanogaster whereas Lhr expression levels are increased in D. simulans. The resulting elevated amount of HMR/LHR complex in hybrids results in an extensive mislocalisation of the complex, an interference with the regulation of transposable elements and an impairment of cell proliferation. Our findings provide evidence for a major role of centromere divergence in the generation of biodiversity. Raw data were analysed using the MaxQuant 1.2.2.5 software package. Identified proteins were considered as interation partners if their MaxQuant iBAQ values displayed a greater than 16fold enrichment compared to control anti-FLAG purifications from Schneider cell nuclear extracts not expressing any FLAG-tagged protein.