Selfishly evolving centromeres bias their transmission by exploiting the asymmetry of female meiosis and preferentially segregating to the egg. Such female meiotic drive systems have the potential to be supergenes, with multiple linked loci contributing to drive costs or enhancement. Here, we explore the supergene potential of a selfish centromere ( D ) in Mimulus guttatus , which was discovered in the Iron Mountain (IM) Oregon population. In the nearby Cone Peak population, D is still a large, non-recombining and costly haplotype that recently swept, but shorter haplotypes and mutational variation suggest a distinct population history. We detected D in five additional populations spanning more than 200 km; together, these findings suggest that selfish centromere dynamics are widespread in M. guttatus . Transcriptome comparisons reveal elevated differences in expression between driving and non-driving haplotypes within, but not outside, the drive region, suggesting large-scale cis effects of D 's spread on gene expression. We use the expression data to refine linked candidates that may interact with drive, including Nuclear Autoantigenic Sperm Protein (NASP SIM3 ), which chaperones the centromere-defining histone CenH3 known to modify Mimulus drive. Together, our results show that selfishly evolving centromeres may exhibit supergene behaviour and lay the foundation for future genetic dissection of drive and its costs. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.
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Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers
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.
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- Award ID(s):
- 1736249
- NSF-PAR ID:
- 10283364
- Editor(s):
- Malik, Harmit S.
- Date Published:
- Journal Name:
- PLOS Genetics
- Volume:
- 17
- Issue:
- 4
- ISSN:
- 1553-7404
- Page Range / eLocation ID:
- e1009418
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Journal Article:
- https://doi.org/10.1371/journal.pgen.1009418
