Evolution of haploid-diploid life cycles when haploid and diploid fitnesses are not equal

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Abstract

<p class="first" id="d4271120e77">Many organisms spend a significant portion of their life cycle as haploids and as diploids (a haploid-diploid life cycle). However, the evolutionary processes that could maintain this sort of life cycle are unclear. Most previous models of ploidy evolution have assumed that the fitness effects of new mutations are equal in haploids and homozygous diploids, however, this equivalency is not supported by empirical data. With different mutational effects, the overall (intrinsic) fitness of a haploid would not be equal to that of a diploid after a series of substitution events. Intrinsic fitness differences between haploids and diploids can also arise directly, for example because diploids tend to have larger cell sizes than haploids. Here, we incorporate intrinsic fitness differences into genetic models for the evolution of time spent in the haploid versus diploid phases, in which ploidy affects whether new mutations are masked. Life-cycle evolution can be affected by intrinsic fitness differences between phases, the masking of mutations, or a combination of both. We find parameter ranges where these two selective forces act and show that the balance between them can favor convergence on a haploid-diploid life cycle, which is not observed in the absence of intrinsic fitness differences. </p>

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Outcrossing, mitotic recombination, and life-history trade-offs shape genome evolution in Saccharomyces cerevisiae.

Omur Kayikci, Brendan D. Murray, Zackary Scholl … (2011)

We carried out a population genomic survey of Saccharomyces cerevisiae diploid isolates and find that many budding yeast strains have high levels of genomic heterozygosity, much of which is likely due to outcrossing. We demonstrate that variation in heterozygosity among strains is correlated with a life-history trade-off that involves how readily yeast switch from asexual to sexual reproduction under nutrient stress. This trade-off is reflected in a negative relationship between sporulation efficiency and pseudohyphal development and correlates with variation in the expression of RME1, a transcription factor with pleiotropic effects on meiosis and filamentous growth. Selection for alternate life-history strategies in natural versus human-associated environments likely contributes to differential maintenance of genomic heterozygosity through its effect on the frequency that yeast lineages experience sexual cycles and hence the opportunity for inbreeding. In addition to elevated levels of heterozygosity, many strains exhibit large genomic regions of loss-of-heterozygosity (LOH), suggesting that mitotic recombination has a significant impact on genetic variation in this species. This study provides new insights into the roles that both outcrossing and mitotic recombination play in shaping the genome architecture of Saccharomyces cerevisiae. This study also provides a unique case where stark differences in the genomic distribution of genetic variation among individuals of the same species can be largely explained by a life-history trade-off.

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Inferences about the distribution of dominance drawn from yeast gene knockout data.

Aneil Agrawal, Michael C. Whitlock (2011)

Data from several thousand knockout mutations in yeast (Saccharomyces cerevisiae) were used to estimate the distribution of dominance coefficients. We propose a new unbiased likelihood approach to measuring dominance coefficients. On average, deleterious mutations are partially recessive, with a mean dominance coefficient ~0.2. Alleles with large homozygous effects are more likely to be more recessive than are alleles of weaker effect. Our approach allows us to quantify, for the first time, the substantial variance and skew in the distribution of dominance coefficients. This heterogeneity is so great that many population genetic processes analyses based on the mean dominance coefficient alone will be in substantial error. These results are applied to the debate about various mechanisms for the evolution of dominance, and we conclude that they are most consistent with models that depend on indirect selection on homeostatic gene expression or on the ability to perform well under periods of high demand for a protein.

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Fitness landscapes: an alternative theory for the dominance of mutation.

Federico Manna, Guillaume Martin, Thomas Lenormand (2011)

Deleterious mutations tend to be recessive. Several theories, notably those of Fisher (based on selection) and Wright (based on metabolism), have been put forward to explain this pattern. Despite a long-lasting debate, the matter remains unresolved. This debate has focused on the average dominance of mutations. However, we also know very little about the distribution of dominance coefficients among mutations, and about its variation across environments. In this article we present a new approach to predicting this distribution. Our approach is based on a phenotypic fitness landscape model. First, we show that under a very broad range of conditions (and environments), the average dominance of mutation of small effects should be approximately one-quarter as long as adaptation of organisms to their environment can be well described by stabilizing selection on an arbitrary set of phenotypic traits. Second, the theory allows predicting the whole distribution of dominance coefficients among mutants. Because it provides quantitative rather than qualitative predictions, this theory can be directly compared to data. We found that its prediction on mean dominance (average dominance close to 0.25) agreed well with the data, based on a meta-analysis of dominance data for mildly deleterious mutations. However, a simple landscape model does not account for the dominance of mutations of large effects and we provide possible extension of the theory for this class of mutations. Because dominance is a central parameter for evolutionary theory, and because these predictions are quantitative, they set the stage for a wide range of applications and further empirical tests.