Abstract

Meiotic drivers are selfish alleles that can force their transmission into more than 50% of the viable gametes made by heterozygotes. Meiotic drivers are known to cause infertility in a diverse range of eukaryotes and are predicted to affect the evolution of genome structure and meiosis. The wtf gene family of Schizosaccharomyces pombe includes both meiotic drivers and drive suppressors and thus offers a tractable model organism to study drive systems. Currently, only a handful of wtf genes have been functionally characterized and those genes only partially reflect the diversity of the wtf gene family. In this work, we functionally test 22 additional wtf genes for meiotic drive phenotypes. We identify eight new drivers that share between 30–90% amino acid identity with previously characterized drivers. Despite the vast divergence between these genes, they generally drive into >85% of gametes when heterozygous. We also identify three wtf genes that suppress other wtf drivers, including two that also act as autonomous drivers. Additionally, we find that wtf genes do not underlie a weak (64% allele transmission) meiotic driver on chromosome 1. Finally, we find that some Wtf proteins have expression or localization patterns that are distinct from the poison and antidote proteins encoded by drivers and suppressors, suggesting some wtf genes may have non-meiotic drive functions. Overall, this work expands our understanding of the wtf gene family and the burden selfish driver genes impose on S. pombe.

Highlights

  • During meiosis, diploid cells divide to produce haploid gametes

  • To test the ability of class 1 and class 2 wtf genes to drive autonomously, we cloned untested genes representing unique subclasses from four isolates that largely reflect the range of S. pombe diversity: Sp, S. kambucha (Sk), FY29033, and CBS5557 (S1 Fig) [23, 24]

  • We crossed each haploid carrying a wtf gene of interest to a wild-type strain from the same background to generate hemizygous diploid strains

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Summary

Introduction

Diploid cells divide to produce haploid gametes (e.g. sperm). This process is generally fair in that each parental allele of a gene is represented in the gametes [1]. Many eukaryotic genomes contain ‘selfish’ elements that bias their own transmission such that they are overrepresented in the viable gametes [2,3,4] These loci are known as meiotic drivers and they can both directly and indirectly reduce fitness through a number of mechanisms (reviewed in [5, 6]). Meiotic drivers can be in conflict with unlinked genes that do not gain a transmission advantage but must bear the fitness burdens often imposed by these selfish elements [7,8,9,10] This genetic conflict is thought to favor the emergence of unlinked allele variants that can suppress the effects of drivers. Arms races caused by meiotic drivers are predicted to affect the evolution of gametogenesis and genome structure [14, 15]

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