Mutator dynamics in sexual and asexual experimental populations of yeast

Yevgeniy Raynes,Paul D Sniegowski,Matthew R Gazzara

doi:10.1186/1471-2148-11-158

Abstract

BackgroundIn asexual populations, mutators may be expected to hitchhike with associated beneficial mutations. In sexual populations, recombination is predicted to erode such associations, inhibiting mutator hitchhiking. To investigate the effect of recombination on mutators experimentally, we compared the frequency dynamics of a mutator allele (msh2Δ) in sexual and asexual populations of Saccharomyces cerevisiae.ResultsMutator strains increased in frequency at the expense of wild-type strains in all asexual diploid populations, with some approaching fixation in 150 generations of propagation. Over the same period of time, mutators declined toward loss in all corresponding sexual diploid populations as well as in haploid populations propagated asexually.ConclusionsWe report the first experimental investigation of mutator dynamics in sexual populations. We show that a strong mutator quickly declines in sexual populations while hitchhiking to high frequency in asexual diploid populations, as predicted by theory. We also show that the msh2Δ mutator has a high and immediate realized cost that is alone sufficient to explain its decline in sexual populations. We postulate that this cost is indirect; namely, that it is due to a very high rate of recessive lethal or strongly deleterious mutation. However, we cannot rule out the possibility that msh2Δ also has unknown directly deleterious effects on fitness, and that these effects may differ between haploid asexual and sexual populations. Despite these reservations, our results prompt us to speculate that the short-term cost of highly deleterious recessive mutations can be as important as recombination in preventing mutator hitchhiking in sexual populations.

Highlights

In asexual populations, mutators may be expected to hitchhike with associated beneficial mutations
Mutator dynamics in asexual populations Mutator-carrying strains declined in all haploid asexual populations, approaching extinction in approximately 150 generations (Figure 1A)
Mutator strains rose in frequency at the expense of wild-type strains in all diploid asexual populations after a short initial lag (Figure 1B); the mutators appeared to approach fixation in seven of the ten diploid asexual populations by 150 generations of propagation

Summary

Introduction

Mutators may be expected to hitchhike with associated beneficial mutations. In the absence of significant evidence for direct selection, most theoretical studies of mutation rate evolution have focused on the indirect selection experienced by mutation rate modifiers and its contrasting effects in sexual and asexual populations [reviewed in [2]]. In asexual populations, modifiers that increase the genomic mutation rate (mutators) can rise in frequency if associated with beneficial mutations, and a substantial experimental literature in support of such mutator hitchhiking has developed [4,5,6,7,8]. In sexual populations recombination is expected to erode associations between beneficial mutations and mutator alleles, preventing mutator hitchhiking and leading to mutator decline due to persistent deleterious mutational pressure [[2,9,10,11], but see [12,13,14,15]]

Methods

Results

Discussion

Conclusion