Diploidy and the selective advantage for meiosis and sexual reproduction in unicellular organisms

This paper develops mathematical models describing the evolutionary dynamics of both asexually and sexually reproducing populations of diploid unicellular organisms. The asexual and sexual life cycles are based on the asexual and sexual life cycles in Saccharomyces cerevisiae, or Baker’s yeast, which normally reproduces by asexual budding, but switches to sexual reproduction when stressed. The mathematical models consider three reproduction pathways: (1) Asexual reproduction. (2) Self-fertilization (3) Sexual reproduction. We also consider two forms of genome organization. In one case, we assume that the genome consists of two multi-gene chromosomes, while in the second case we consider the opposite extreme and assume that each gene defines a separate chromosome, which we call the multi-chromosome genome. These two cases are considered in order to explore the role that recombination has on the mutation-selection balance and the selective advantage of the various reproduction strategies. We assume that the purpose of diploidy is to provide redundancy, so that damage to a gene may be repaired using the other, presumably undamaged copy (a process known as homologous recombination repair). As a result, we assume that the fitness of the organism only depends on the number of homologous gene pairs that contain at least one functional copy of a given gene. If the organism has at least one functional copy of every gene in the genome, we assume a fitness of 1, and we assume that each homologous gene pair without a functional copy of a given gene induces a fitness penalty of α. For nearly all of the reproduction strategies we consider, we find that the mean fitnesses at mutation-selection balance have a value of max{2e−N −1, 0}, where N is the number of genes in the haploid set of the genome, and is the probability that a given DNA template strand of a given gene produces a mutated daughter during replication. The only exception is the sexual reproduction pathway. This strategy is found to have a mean fitness that exceeds the mean fitness of all of the other strategies. Furthermore, while the other reproduction strategies experience a total loss of viability due to the steady accumulation of deleterious mutations once N exceeds ln 2, no such transition occurs in the sexual pathway. We explicitly allow for mitotic recombination in this work, which, in contrast to previous studies using different models, does not have any advantage over other asexual reproduction strategies. The results of this paper suggest that sex provides a selective advantage by acting on “non-essential” genes, i.e., genes that confer a fitness advantage to the organism, but are not necessary for the organism to grow and reproduce. The more “non-essential” the genes, as measured by how close α is to 1 in our model, the stronger the selective advantage for sex. The selective advantage for sex is far more pronounced in the multichromosomed genome than the two-chromosomed genome, so that the results of this paper provide a basis for understanding the selective advantage of the specific meiotic pathway that is employed by sexually reproducing organisms. The results of this paper also suggest an explanation for why unicellular organisms such as Saccharomyces cerevisiae (Baker’s yeast) switch to a sexual mode of reproduction when stressed. Finally, while the results of this paper are based on modeling mutationpropagation in unicellular organisms, they nevertheless suggest that, in more complex organisms with significantly larger genomes, sex is necessary to prevent the loss of viability of a population due to genetic drift.