Academic journal article Genetics

A High Frequency of Beneficial Mutations across Multiple Fitness Components in Saccharomyces Cerevisiae

Academic journal article Genetics

A High Frequency of Beneficial Mutations across Multiple Fitness Components in Saccharomyces Cerevisiae

Article excerpt

ABSTRACT

Mutation-accumulation experiments are widely used to estimate parameters of spontaneous mutations affecting fitness. In many experiments only one component of fitness is measured. In a previous study involving the diploid yeast Saccharomyces cerevisiae, we measured the growth rate of 151 mutation-accumulation lines to estimate parameters of mutation. We found that an unexpectedly high frequency of fitness-altering mutations was beneficial. Here, we build upon our previous work by examining sporulation efficiency, spore viability, and haploid growth rate and find that these components of fitness also show a high frequency of beneficial mutations. We also examine whether mutation-acycumulation (MA) lines show any evidence of pleiotropy among accumulated mutations and find that, for most, there is none. However, MA lines that have zero fitness (i.e., lethality) for any one fitness component do show evidence for pleiotropy among accumulated mutations. We also report estimates of other parameters of mutation based on each component of fitness.

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ADAPTATION can occur from standing genetic variation or from newly arising mutations. The relative importance of these two sources of adaptive mutations is affected by a variety of factors, including those that alter standing levels of genetic variation (see Barrett and Schluter 2008) and those that generate new mutations. Predicting how quickly a population will adapt and the type of beneficial mutations that will fuel that adaptation requires estimates of the additive genetic variance in fitness and of the beneficial mutation rate and the distribution of beneficial effects. While additive genetic variance for fitness has been estimated in a variety of organisms (Mousseau and Roff 1987), the beneficial mutation rate and the distribution of beneficial effects have only been estimated in a few studies (Shaw et al. 2002; Joseph and Hall 2004; Perfeito et al. 2007; Dickinson 2008; Hall et al. 2008). Surprisingly, these studies estimate that between 6 (Joseph and Hall 2004) and 50% (Shaw et al. 2002) of fitness-altering mutations are beneficial. In contrast, most mutation-accumulation (MA) experiments identify few, if any, beneficial mutations. Such wildly different estimates have even been generated from studies of the same species in similar environments (Zeyl and Devisser 2001; Joseph and Hall 2004; Dickinson 2008; Hall et al. 2008). If these estimates are correct, then they would suggest that the genotypes used in these experiments have vastly different evolutionary potential with respect to their capacity to exhibit rapid adaptation from new mutations.

A more likely scenario is that much of the variation in estimates of the beneficialmutation rate is due tomethodological differences between studies. One possibility is the fitness component being analyzed. The beneficial mutation rate may be under- or overestimated if the fitness component is under stabilizing selection or subject to antagonistic pleiotropy. Analyses of mutationaccumulation data typically assume that selection is directional. As a result, analyses of phenotypes under stabilizing selection may falsely conclude that mutations that increase a phenotype are beneficial and mutations that lower values are deleterious (see Keightley and Lynch's 2003 criticism of Shaw et al. 2002). Alternatively, the beneficialmutation ratemay be over- (or under) estimated if mutations increase fitness in regard to one component, but lower fitness in regard to lifetime fitness or another fitness component (i.e., antagonistic pleiotropy). Here, we explore these possibilities by investigating whether the high beneficial mutation rates estimated from our previous experiments are specific to the fitness component that we examined.

In two previous studies we accumulated mutations in 152 yeast,MAlines and used measures of their effects on diploid growth rate to estimate parameters of beneficial and deleterious mutations. …

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