Abstract
Natural selection works best when the two alleles in a diploid organism are transmitted to offspring at equal frequencies. Despite this, selfish loci known as meiotic drivers that bias their own transmission into gametes are found throughout eukaryotes. Drive is thought to be a powerful evolutionary force, but empirical evolutionary analyses of drive systems are limited by low numbers of identified meiotic drive genes. Here, we analyze the evolution of the wtf gene family of Schizosaccharomyces pombe that contains both killer meiotic drive genes and suppressors of drive. We completed assemblies of all wtf genes for two S. pombe isolates, as well as a subset of wtf genes from over 50 isolates. We find that wtf copy number can vary greatly between isolates and that amino acid substitutions, expansions and contractions of DNA sequence repeats, and nonallelic gene conversion between family members all contribute to dynamic wtf gene evolution. This work demonstrates the power of meiotic drive to foster rapid evolution and identifies a recombination mechanism through which transposons can indirectly mobilize meiotic drivers.
Highlights
Many genes are maintained in eukaryotic genomes by natural selection because they provide a fitness benefit to the organisms that bear them
We found that 14 of the 24 wtf loci are within 2.5 kb of one or more hotspots. These analyses suggest that close proximity of some genes to double strand breaks (DSBs) hotspots likely contributes to the high levels of recombination within the wtf gene family
Our study extends previous evolutionary analyses to demonstrate extremely dynamic evolution of the wtf gene family in multiple lineages of S. pombe (24)
Summary
Many genes are maintained in eukaryotic genomes by natural selection because they provide a fitness benefit to the organisms that bear them. Analyses of these genes and their molecular functions constitute the bulk of molecular biology research performed today. Killer meiotic drive loci are one such class of parasites that can be harmful to fitness. These selfish loci act when heterozygous to destroy the meiotic products that do not inherit them. Killer meiotic drivers have been observed throughout eukaryotes from plants to mammals, even though their selfish behavior generally decreases overall organismal fitness (3-6). The activity of many suppressors of meiotic drive has been observed, only four suppressor genes have been cloned (8-11)
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