Gametic specialization of centromeric histone paralogs in insect species

Abstract

The centromere is a specialized chromatin region that is critical for faithful chromosome segregation. Centromere function is conferred epigenetically, by the presence of a histone H3 variant called CenH3 that replaces H3 in nucleosomes at centromeres. Since CenH3 was identified as a centromere-specific histone, countless studies have demonstrated the deleterious consequences of CenH3 perturbation. Paradoxically, numerous studies have also demonstrated that CenH3 evolves rapidly. The centromere drive hypothesis posits that CenH3 evolves rapidly because it is engaged in a co-evolutionary arms race with centromeric DNA. As evidence supporting the molecular mechanisms of centromere drive grows, it seems likely that CenH3’s function as a drive suppressor may require rapid evolution. However, rapid evolution may also be at odds with CenH3’s essential mitotic role. Therefore, encoding both the mitotic and drive suppressor functions of CenH3 in a single gene creates an intralocus conflict – the evolutionary tension resulting from simultaneous optimization of multiple functions encoded by one gene. CenH3 gene duplication and specialization is one way to resolve this intralocus conflict. Here, I examined the evolution and cytological localization of CenH3 paralogs in Drosophila and mosquitoes. Although CenH3 is typically thought of as a single copy gene, I found that most Drosophila and mosquito species encode more than one CenH3 paralog. Furthermore, my analyses suggest that these CenH3 paralogs have acquired specialized germline functions. My characterization of CenH3 paralogs provides an opportunity to dissect how evolution has shaped the fundamental process of chromosome segregation in unanticipated ways.