More than just a centromere: evolution of a structural supergene causing female meiotic drive in monkeyflowers

Abstract Meiotic drivers capitalize on vulnerabilities in eukaryotic meiosis and gametogenesis to gain greater-than-equal transmission to the next generation. In most plants and animals, asymmetric female meiosis presents an arena for meiotic drive, as centromeric variants may bias their segregation to the one egg cell. Although centromeric drive is predicted to be pervasive, its mechanisms and consequences remain obscure. Here, we build on representative chromosome-scale assemblies of yellow monkeyflowers (Mimulus guttatus species complex) to compare three functionally distinct haplotypes at Meiotic Drive Locus on Chromosome 11 (MDL11). The driving D allele at MDL11 was previously shown to be centromere-containing, costly, and maintained as a balanced polymorphism in wild M. guttatus populations. D has diverged from nondrivers via at least two major rearrangements (including a hemicentric inversion creating linked arrays of centromeric satellite Cent728 separated by > 200 trapped genes), massive expansions of a novel MDL11-specific subfamily of satellite repeats (Cent728D) that increase the length of the driver chromosome by >50% over homologues, and the build-up of a 2Mb D-exclusive pericentromeric region containing ∼37 extra D-associated genes duplicated and translocated from diverse genomic sources. Differences in centromeric satellite arrays, particularly the recent expansion of Cent728D are primary candidates for generating female meiotic drive. However, substantial divergence in gene content and sequence among the three haplotypes also points to candidate genic modifiers that may enhance D drive and contribute to differences in drive-susceptibility among non-drivers. Overall, our findings support the sequential buildup of this model centromeric driver, reveal intriguing parallels with other selfish supergenes, and provide a strong platform for understanding the mechanisms of its dramatic violation of Mendelian rules.