The role of pleiotropy in the maintenance of sex in yeast

Abstract

In facultatively sexual species, lineages that reproduce asexually for a period of time can accumulate mutations that reduce their ability to undergo sexual reproduction when sex is favorable. We propagated Saccharomyces cerevisiae asexually for approximately 800 generations, after which we measured the change in sexual fitness, measured as the proportion of asci observed in sporulation medium. The sporulation rate in cultures propagated asexually at small population size declined by 8%, on average, over this time period, indicating that the majority of mutations that affect sporulation rate are deleterious. Interestingly, the sporulation rate in cultures propagated asexually at large population size improved by 11%, on average, indicating that selection on asexual function effectively eliminated most of the mutations deleterious to sporulation ability. These results suggest that pleiotropy between mutations' effects on asexual fitness and sexual fitness was predominantly positive, at least for the mutations accumulated in this experimental evolution study. A positive correlation between growth rate and sporulation rate among lines also provided evidence for positive pleiotropy. These results demonstrate that, at least under certain circumstances, selection acting on asexual fitness can help to maintain sexual function.

Figure 1.—

Mean proportion of asci for 128 ancestral (t = 0), 78 SMA evolved (t = 800), and 50 LMA evolved (t = 800) lines. Dots show all of the data. Box plots represent the 25th, median, and 75th quartiles, with whiskers extending an additional 1.5 times the interquartile range in each direction.

Figure 2.—

Mean growth rates for 128 ancestral (t = 0), 78 SMA evolved (t = 800), and 50 LMA evolved (t = 800) lines. Dots show all of the data. Box plots represent the 25th, median, and 75th quartiles, with whiskers extending an additional 1.5 times the interquartile range in each direction.

Figure 3.—

Correlation between sexual fitness on the y-axis and asexual fitness on the x-axis using all lines. The correlation is significant when all data are included (solid line, Spearman's rank-order correlation, ρ = 0.12, P = 0.0244) and when the poorly sporulating lines (open circles) are excluded (dashed line, ρ = 0.11, P = 0.0365). This positive correlation remains, but is not significant, when LMA lines or SMA lines are analyzed separately.

Figure 4.—

Likelihood estimation of mutational parameters affecting sexual fitness. The program mlgenomeu.c was used to compare the sporulation rates of the 78 SMA evolved lines to those of the 128 ancestral lines. The log-likelihood associated with the ML values of U_sex and s_sex is plotted as a function of the shape parameter β for the gamma distribution (β < 1 corresponds to L-shaped distributions, and β > 1 corresponds to bell-shaped distributions). The straight line lies 2 log-likelihood units below the maximum-likelihood point at β = 0.01. Plots on the right show likelihood profiles for the proportion of beneficial mutations P_sex (top), the mutation rate U_sex (middle), and the average effect on sporulation rate s_sex (bottom), holding β fixed at 0.01.

Figure 5.—

Likelihood estimation of mutational parameters affecting asexual fitness. The program mlgenomeu.c was used to compare the growth rates of the 78 SMA evolved lines to those of the 128 ancestral lines. The log-likelihood associated with the ML values of U_asex and s_asex is plotted as a function of the shape parameter β for the gamma distribution. The straight line lies 2 log-likelihood units below the maximum-likelihood point at β = ∞. Plots on the right show likelihood profiles for the proportion of beneficial mutations P_asex (top), the mutation rate U_asex (middle), and the average effect on sporulation rate s_asex (bottom), holding β fixed at ∞.