Centromere-associated meiotic drive and female fitness variation in Mimulus

Abstract

Female meiotic drive, in which chromosomal variants preferentially segregate to the egg pole during asymmetric female meiosis, is a theoretically pervasive but still mysterious form of selfish evolution. Like other selfish genetic elements, driving chromosomes may be maintained as balanced polymorphisms by pleiotropic or linked fitness costs. A centromere-associated driver (D) with a ∼58:42 female-specific transmission advantage occurs at intermediate frequency (32-40%) in the Iron Mountain population of the yellow monkeyflower, Mimulus guttatus. Previously determined male fertility costs are sufficient to prevent the fixation of D, but predict a higher equilibrium frequency. To better understand the dynamics and effects of D, we developed a new population genetic model and measured genotype-specific lifetime female fitness in the wild. In three of four years, and across all years, D imposed significant recessive seedset costs, most likely due to hitchhiking by deleterious mutations. With both male and female costs as measured, and 58:42 drive, our model predicts an equilibrium frequency of D (38%) very close to the observed value. Thus, D represents a rare selfish genetic element whose local population genetic dynamics have been fully parameterized, and the observation of equilibrium sets the stage for investigations of coevolution with suppressors.

Keywords: Balancing selection; centromere; genetic conflict; polymorphism; seedset; selfish genetic element; standing variation.

Figure 1

Mean (±SE) of female fitness components in each Drive Locus genotype over four years in the Iron Mountain population of Mimulus guttatus.

Figure 2

Frequency of Drive Locus genotypes in Iron Mountain M. guttatus sampled over the four-year study period. Numbers on bars show sample numbers in each category.

Figure 3

Equilibrium frequency of D is predicted as a function of the recessive female fitness cost for three outcrossing rates. Previous estimates for the strength of drive and the male fitness cost were assumed (s_M = 0.20, δ = 0.58, h_M = h_F = 0; Fishman and Saunders 2008). The vertical line indicates the mean female cost across our four-year study period and the horizontal lines bracket field estimates of D frequency.