Abstract
Centromeres are essential mediators of chromosomal segregation, but both centromeric DNA sequences and associated kinetochore proteins are paradoxically diverse across species. The selfish centromere model explains rapid evolution by both components via an arms-race scenario: centromeric DNA variants drive by distorting chromosomal transmission in female meiosis and attendant fitness costs select on interacting proteins to restore Mendelian inheritance. Although it is clear than centromeres can drive and that drive often carries costs, female meiotic drive has not been directly linked to selection on kinetochore proteins in any natural system. Here, we test the selfish model of centromere evolution in a yellow monkeyflower (Mimulus guttatus) population 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. We use quantitative genetic mapping to demonstrate that context-dependence in the strength of drive (from near-100% D transmission in interspecific hybrids to near-Mendelian in within-population crosses) primarily reflects variable vulnerability of the non-driving competitor chromosomes, but also map an unlinked modifier of drive coincident with kinetochore protein Centromere-specific Histone 3 A (CenH3A). Finally, CenH3A exhibits a recent (<1000 years) selective sweep in our focal population, implicating local interactions with D in ongoing adaptive evolution of this kinetochore protein. Together, our results demonstrate an active co-evolutionary arms race between DNA and protein components of the meiotic machinery in Mimulus, with important consequences for individual fitness and molecular divergence.
Highlights
Centromeres, which mediate the conserved and essential processes of chromosomal segregation during eukaryotic mitosis and meiosis, are paradoxically diverse
We show that the D haplotype is structurally and genetically distinct and swept to a high stable frequency within the past 1500 years
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
Summary
We use whole genome sequencing and genetic crossing experiments to demonstrate active evolutionary interactions between a selfish centromere and a key kinetochore protein (CenH3A) in the wildflower Mimulus guttatus. We show that both inter-specific and intra-population differences in CenH3A affect centromeric drive in hybrids, and that adaptive evolution of CenH3A has followed the recent and costly spread of the driver in a wild population. This work provides novel empirical support for the proposed antagonistic co-evolution of the DNA and protein components of centromeres, with important consequences for understanding cellular function, individual fitness, and species divergence
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