Abstract

Meiotic drivers are selfish alleles that subvert gametogenesis to increase their transmission into progeny. Drivers impose a fitness cost, putting pressure on the genome to evolve suppressors. Here we investigate the wtf gene family from Schizosaccharomyces pombe, previously shown to contain meiotic drivers in wild isolates. We discovered that wtf13 found in lab stocks is a meiotic driver. wtf13 kills spores that do not inherit it by generating both a diffusible poison and a spore-specific antidote. Additionally, we demonstrate that wtf13 is suppressed by another wtf gene, wtf18-2, that arose spontaneously in the lab and makes only an antidote. Wtf18-2 does not act indiscriminately to prevent spore destruction. Instead, it rescues only the spores that inherit wtf18-2. In this way, wtf18-2 selfishly gains a transmission advantage of its own while dampening the drive of wtf13. This establishes a novel paradigm for meiotic drive suppressors and provides insight into the mechanisms and evolution of drive systems.

Highlights

  • A founding principle of genetics is that the two alleles carried by a diploid are transmitted at Mendelian frequencies into the gametes [1]

  • Because of the significant fitness cost that these killer meiotic drivers impose to the organism, suppressors of drive are expected to evolve

  • We and others recently discovered that members of the wtf gene family in natural isolates of fission yeast are killer meiotic drivers

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Summary

Introduction

A founding principle of genetics is that the two alleles carried by a diploid are transmitted at Mendelian (equal) frequencies into the gametes [1]. The mechanisms of meiotic chromosome segregation and gametogenesis are often assumed to be unbiased and to guarantee Mendelian transmission. These processes, are not perfect and are vulnerable to exploitation by ‘selfish’ genetic parasites that can bias their own transmission to the generation, often at the expense of the rest of the genome [2]. These selfish alleles are known as meiotic drivers. While the true prevalence of meiotic drivers is unknown (and perhaps underappreciated), the detection of meiotic drive has accelerated in recent years, as generation sequencing enabled the detection of drivers not linked to obvious phenotypes [7,8,9,10,11]

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