Contrasting mutation patterns in haploid and diploid cells from two yeast species
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There is significant variation in the rate and spectrum of spontaneous mutations among taxa. How this variation is shaped by natural selection remains a subject of debate. The drift barrier hypothesis proposes that selection generally favors lower mutation rates due to the risk of deleterious mutations but acts less effectively against weak mutator alleles in smaller populations, allowing the mutation rate to increase due to genetic drift. Given this model, we propose that mutation rates may also be elevated in cell types that appear rarely in a population, where DNA replication and repair processes are subject to selection less often. We can begin to test this prediction in yeast species, some of which can be grown in either a haploid or diploid cell state. Existing data on the budding yeast Saccharomyces cerevisiae support this prediction, with a higher mutation rate observed in haploids, which is the rare cell type in natural populations. However, this pattern could also appear if haploidy is inherently mutagenic, regardless of the dominant cell type. To test these alternatives, we conducted a mutation accumulation experiment with haploid and diploid cells of the fission yeast Schizosaccharomyces pombe , in which diploidy is the rare cell type. In this species, we found a higher mutation rate in diploids, consistent with our prediction. In both species, the spectrum of mutations is also influenced by ploidy state. Our findings suggest that limits to selection on mutation may be evident as variation within species.
Significance
Spontaneous mutation rates vary among organisms. Natural selection may act to reduce mutation rates; if so, we would expect mutation rates to be elevated in cell types where natural selection has historically had less opportunity to act. We studied mutation patterns in two yeast species when grown in the haploid or diploid form. For the typically diploid species, the mutation rate was higher in the haploid form. For the typically haploid species, the mutation rate was higher in the diploid form. The observation that mutation rates increase when selection is ineffective indicates that selection usually acts to reduce mutation rates.