Fitness Costs and Variation in Transmission Distortion Associated with the Abnormal Chromosome 10 Meiotic Drive System in Maize

Abstract

Meiotic drive describes a process whereby selfish genetic elements are transmitted at levels greater than Mendelian expectations. Maize abnormal chromosome 10 (Ab10) encodes a meiotic drive system that exhibits strong preferential segregation through female gametes. We performed transmission assays on nine Ab10 chromosomes from landraces and teosinte lines and found a transmission advantage of 62-79% in heterozygotes. Despite this transmission advantage, Ab10 is present at low frequencies in natural populations, suggesting that it carries large negative fitness consequences. We measured pollen transmission, the percentage of live pollen, seed production, and seed size to estimate several of the possible fitness effects of Ab10. We found no evidence that Ab10 affects pollen transmission,, Ab10 and N10 pollen are transmitted equally from heterozygous fathers. However, at the diploid (sporophyte) level, both heterozygous and homozygous Ab10-I-MMR individuals show decreased pollen viability, decreased seed set, and decreased seed weight. The observed fitness costs can nearly but not entirely account for the observed frequencies of Ab10. Sequence analysis shows a surprising amount of molecular variation among Ab10 haplotypes, suggesting that there may be other phenotypic variables that contribute to the low but stable equilibrium frequencies.

Modeling the Evolution of Female Meiotic Drive in Maize

“…To gain insight into the relative likelihood of the above four outcomes, the leading eigenvalues were calculated for randomly drawn parameter values in the general case (0 ≤ h , h f , h s , h m , v , f , s , and m ≤ 1) and for situations in which selection was assumed to be relatively weak (0 ≤ v , f , s, and m ≤ 0.1), or the Ab10 driver was assumed to be fully recessive ( h = h f = h s = h m = 0), additive ( h = h f = h s = h m = 1/2), or fully dominant ( h = h f = h s = h m = 1) in all of its fitness effects. In addition, we considered the situation in which the drive parameter is constrained to be between 0.2 and 0.6, equivalent to a frequency of the driver allele between 0.6 and 0.8 in gametes of heterozygotes, which is the observed range of drive in Ab10 ( Higgins et al 2017 ). Equations (1) were also used to determine the number of internal equilibria for every combination of randomly chosen parameter values using the numerical solving capabilities of Mathematica (version 9; Wolfram Research, Inc. 2012 ).…”

“…We wished to determine whether fitness values associated with the three genotypes (Ab10/Ab10, Ab10/N10, and N10/N10) are sufficient to explain the observed range of population frequencies. In a field experiment containing all three genotypes, seed production, seed weight, and pollen viability were measured, as was the degree of drive of nine different Ab10 strains ( Higgins et al 2017 ). Ab10 had a modest effect on pollen viability, causing a 1 and 6% reduction in Ab10/N10 heterozygotes and Ab10/Ab10 homozygotes, respectively, though the heterozygous effect was not significantly different from the N10/N10 homozygote.…”

“… Predicted frequency of Ab10 in ovules at the stable equilibrium using fitness parameters from a field experiment. The solid line is equilibrium for the average values of seed set, seed size (seed viability), and pollen viability measured in Higgins et al (2017) ( f = 0.650, s = 0.190, m = 0.063, h f = 0.212, h s = 0.327, and h m = 0.176). The dashed line is the equilibrium after including hypothetical reductions in seed viability due to offspring genotype ( v = 0.3 and h = 0.238) to illustrate how the predicted equilibrium changes.…”

“…A recent companion study ( Higgins et al 2017 ) has examined multiple components of fitness for maize plants heterozygous or homozygous for the Ab10 chromosome. Fitness costs have been found for pollen viability, ovule viability, and seed size.…”

Gene drives in plants: opportunities and challenges for weed control and engineered resilience

“…While the mechanisms that facilitate biased transmission are multipartite [37], in essence, the knob structures bias transmission by enabling Ab10 to actively migrate along meiotic spindles to the fertile egg cell ahead of N10 chromosomes. This results in strong preferential segregation, such that Ab10 is transmitted to 60-80% of progeny [38]. A second well-characterized example of female meiotic drive in plants is the monkey flower (Mimulus guttatus) centromere-associated distorter (D) locus [39,40].…”