Selfish chromosomal drive shapes recent centromeric histone evolution in monkeyflowers

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. 

Methods
These are F2 genotype-phenotype data used for mapping of loci contributing to differences in the strength of heterospecific vs. conspecific centromere-associated drive by the driving D haplotype at MDL11 in Mimulus nasutus x M. guttatus hybrids. The %Dfem phenotype is the inferred female transmission of D allele (vs. nondriving d from M. nasutus or D- from M. guttatus) to selfed F3 progeny, assuming Mendelian transmission through male function. Only F2s with at least 12 F3 progeny genotyped were included in our analyses, but all genotyped individuals were used for estimation of D transmission to F2s and are included for completeness. The CenH3A genotype (NN, GG, NG767 and NG160 for the two classes of interspecific heterozygotes) are from an exon-primed intron-spanning PCR marker that could distinguish all 3 parental alleles. The genome-wide mapped genotypes (coded as N, G, H) were derived from multiplex-shotgun-genotyping, window-calling, and mapping protocols described in Flagel et al. 2018 (PLOS Computational Biology). Sheet 1 has the genotype-phenotype matrix, sheet 2 the marker positions on the genetic linkage map and the v1 contigs of M. guttatus, and v1 windows can be matched to v2 and newer genome assemblies (with gene annotations) via the information in sheet 3.