Fitness consequences of a non-recombiningsex-ratiodrive chromosome can explain its prevalence in the wild

Abstract

Understanding the pleiotropic consequences of gene drive systems on host fitness is essential to predict their spread through a host population. Here, we study sex-ratio (SR) X-chromosome drive in the fly Drosophila recens , where SR causes the death of Y-bearing sperm in male carriers. SR males only sire daughters, which all carry SR, thus giving the chromosome a transmission advantage. The prevalence of the SR chromosome appears stable, suggesting pleiotropic costs. It was previously shown that females homozygous for SR are sterile, and here, we test for additional fitness costs of SR. We found that females heterozygous for SR have reduced fecundity and that male SR carriers have reduced fertility in conditions of sperm competition. We then use our fitness estimates to parametrize theoretical models of SR drive and show that the decrease in fecundity and sperm competition performance can account for the observed prevalence of SR in natural populations. In addition, we found that the expected equilibrium frequency of the SR chromosome is particularly sensitive to the degree of multiple mating and performance in sperm competition. Together, our data suggest that the mating system of the organism should be carefully considered during the development of gene drive systems.

Gene drive: progress and prospects

“…Lea & Unckless [25] found no reduced immune function associated with male meiotic drive, and Dyer & Hall [24] found no effects on female mating preferences or on longevity. Larner et al [23] and Dyer & Hall [24] then used the quantified fitness costs to parametrize population genetic models to predict equilibrium frequencies in nature. These predicted frequencies came close to observed frequencies.…”

“…These drivers act during sperm development to eliminate their competition, namely, non-driver carrying sperm, which promotes their own transmission. Finnegan et al [22], Larner et al [23], Dyer & Hall [24] and Lea & Unckless [25] measured fitness costs in males and females associated with their speciesspecific meiotic driver, in stalk-eyed flies Teleopsis dalmanni, in the fruit fly Drosophila pseudoobscura, in Drosophila recens and in Drosophila melanogaster, Drosophila affinis and Drosophila neotestacea, respectively. These fitness costs are apparent as reduced egg-to-adult viability [22], reduced offspring production in females [23,24] and reduced sperm competition success [24].…”

Linked supergenes underlie split sex ratio and social organization in an ant

“…Under the "reduction principle" (16), this is also expected to occur around sex-ratio distorters. In line with this prediction, sexratio distorter loci often occur in regions of low recombination (17)(18)(19)(20), but we lack evidence for the direction of causality. The reduction principle is also expected to contribute to the formation of autosomal supergenes controlling other complex traits that involve epistatic interactions between two or more loci.…”

Resistance to natural and synthetic gene drive systems

“…One possibility is that the locus that confers susceptibility to drive is small, providing a small mutational target. However, many drivers impose broad costs across the genome (Dyer & Hall, 2019; Finnegan et al., 2019; Hamilton, 1967; Larner, Price, Holman, & Wedell, 2019; Zanders & Unckless, 2019), so loci throughout the genome are predicted to evolve to resist costly gene drives. Here, the lack of resistance mechanisms cannot be due to the small size of the mutational target, suggesting the involvement of other evolutionary constraints.…”

“…Drivers may themselves have a range of harmful pleiotropic effects, or be in linkage with deleterious alleles (Burt & Trivers, 2006). Fitness loss is often observed in both males and females, especially when drivers are homozygous (Dyer & Hall, 2019; Finnegan et al., 2019; Hamilton, 1967; Larner et al., 2019; Zanders & Unckless, 2019).…”