Hoisted with his own petard: How sex-ratio meiotic drive in Drosophila affinis creates resistance alleles that limit its spread

Meiotic drivers are selfish genetic elements that tinker with gametogenesis to bias their own transmission into the next generation of offspring. Such tinkering can have significant consequences on gametogenesis and end up hampering the spread of the driver. In Drosophila affinis, sex-ratio meiotic drive is caused by an X-linked complex that, when in males with a susceptible Y chromosome, results in broods that are typically more than 95% female. Interestingly, D. affinis males lacking a Y chromosome (XO) are fertile and males with the meiotic drive X and no Y produce only sons-effectively reversing the sex-ratio effect. Here, we show that meiotic drive dramatically increases the rate of nondisjunction of the Y chromosome (at least 750X), meaning that the driver is creating resistant alleles through the process of driving. We then model how the O might influence the spread, dynamics and equilibrium of the sex-ratio X chromosome. We find that the O can prevent the spread or reduce the equilibrium frequency of the sex-ratio X chromosome, and it can even lead to oscillations in frequency. Finally, with reasonable parameters, the O is unlikely to lead to the loss of the Y chromosome, but we discuss how it might lead to sex-chromosome turnover indirectly.

Automated summary

Meiotic drivers manipulate gametogenesis to bias their own transmission. In the fruit fly Drosophila affinis, a sex-ratio meiotic drive results in highly female-biased offspring. Interestingly, males with the meiotic drive X and no Y produce only sons, reversing the sex-ratio effect. The drive dramatically increases the rate of nondisjunction of the Y chromosome, creating resistant alleles. The O gene can prevent the spread or reduce the equilibrium frequency of the sex-ratio X chromosome, and may lead to frequency oscillations.