Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers

Abstract

Under the selfish centromere model, costs associated with female meiotic drive by centromeres select on interacting kinetochore proteins to restore Mendelian inheritance. We directly test this model in yellow monkeyflowers (Mimulus guttatus), which are polymorphic for a costly driving centromere (D). We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years. Quantitative genetic analyses reveal that variation in the strength of drive primarily depends on the identity of the non-D centromere, but also identified an unlinked modifier coincident with kinetochore protein Centromere-specific Histone 3 A (CenH3A). CenH3A has also experienced a recent (<1000 years) selective sweep in our focal population, consistent with ongoing interactions with D shaping its evolution. Together, our results demonstrate an active co-evolutionary arms race between the DNA and protein components of the meiotic machinery, with important consequences for individual fitness and molecular divergence.