Adaptive evolution of cid, a centromere-specific histone in drosophila

Centromeric DNA is generally composed of large blocks of tandem satellite r epeats that change rapidly due to loss of old arrays and expansion of new r epeat classes. This extreme heterogeneity of centromeric DNA is difficult t o reconcile with the conservation of the eukaryotic chromosome segregation machinery. Histone H3-like proteins, including Cid in Drosophila melanogast er; are a unique chromatin component of centromeres. In comparisons between closely related species of Drosophila, we find an excess of replacement ch anges that have been fixed since the separation of D. melanogaster and D. s imulans, suggesting adaptive evolution. The last adaptive changes appear to have occurred recently, as evident from a reduction in polymorphism in the melanogaster lineage. Adaptive evolution has occurred both in the long N-t erminal tail as well as in the histone fold of Cid. In the histone fold, th e replacement changes have occurred in the region proposed to mediate bindi ng to DNA. We propose that this rapid evolution of Cid is driven by a respo nse to the changing satellite repeats at centromeres. Thus, centromeric MS- like proteins map act as adaptors between evolutionarily labile centromeric DNA and the conserved kinetochore machinery.