A suppressor of a wtf poison-antidote meiotic driver acts via mimicry of the driver’s antidote

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.

Author summary

Killer meiotic drivers are selfish genes that cause infertility by destroying the gametes (e.g. sperm) that do not inherit them. This allows them to be transmitted into up to 100% of the surviving gametes. 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. These genes generate a poison to kill gametes, but rescue those that inherit the driver with an antidote. In this work, we discovered that an additional wtf gene, wtf13 found in intensely studied lab strains is also a meiotic driver. This driver is only capable of driving in the absence of another wtf gene, wtf18-2, which works by mimicking the antidote of wtf13. By protecting only the spores that inherit the gene, wtf18-2 selfishly gains a transmission advantage of its own, establishing a novel paradigm for drive suppressors.