Concurrent duplication of the Cid and Cenp-C genes in the Drosophila subgenus with signatures of subfunctionalization and male germline-biased expression

Abstract

The constitutive centromeric proteins CenH3 and Cenp-C are interdependent in their role of establishing centromere identity and function. In a recent paper, Kursel and Malik (February 2017; doi: 10.1093/molbev/msx091) reported that the Drosophila CenH3 homologue Cid underwent four independent duplication events during evolution. Particularly interesting is the duplication that took place in the common ancestor of the Drosophila subgenus and led to the subfunctionalization and high divergence of the Cid1 and Cid5 paralogs. Here, we describe another independent Cid duplication (Cid1 leading to Cid6) in the buzzatii cluster (repleta group) of the Drosophila subgenus. Moreover, we found that, in addition to the Cid1/Cid5 duplication, Cenp-C was also duplicated (Cenp-C1, Cenp-C2) in the common ancestor of the Drosophila subgenus. Analyses of expression and tests for positive selection indicate that both Cid5 and Cenp-C2 are male germline-biased and evolved adaptively, indicating subfunctionalization of the Cid and Cenp-C paralogs. Our findings further highlight the strong interdependence between CenH3 and Cenp-C, paving the way to new perspectives by which centromere function and evolution can be addressed.