Novel stressors and trait variation determine X-linked meiotic drive frequency

Sex ratio meiotic drive alleles bias their transmission by impairing the viability of non-drive gametes, leading to skewed population sex ratios. Despite theoretical predictions that drive alleles should reach fixation causing population extinction, meiotic drive persists at intermediate frequencies in wild populations, though the reasons for this are unclear. Here, we investigate how novel environmental stress and genotype-specific fitness costs contribute to drive frequency. Using a suppression-free X-linked meiotic drive system in Drosophila pseudoobscura, we exposed flies to varying doses of the pesticide permethrin and measured mortality and fecundity across genotypes. We found that drive-bearing males (SR) and drive-homozygous females (SRSR) exhibited heightened mortality, both in the presence and absence of pesticide, while heterozygous (SRST) females exhibited superior fecundity. Using a mathematical model parametrized with our empirical findings, we explored the long-term population dynamics of meiotic drive under different conditions. Our model predicts that drive frequency has a concave relationship with pesticide dose and is strongly modulated by genotype-specific female fecundity. These results suggest that novel environmental stressors and drive-induced fitness effects play key roles in determining meiotic drive frequencies. Our findings improve our understanding of drive frequencies in the wild and have direct implications for drive-based pest control.