Why Bother with Sex? The Evolution of Recombination in an Artificial Gene Network

Sex is ubiquitous in the natural world, but its costs are high and the nature of its benefits remains controversial. Previous studies have suggested that a major advantage of sex is its ability to eliminate interference between selection on linked mutations, a phenomenon known as Hill-Robertson interference. However, those studies may have missed both important advantages and disadvantages of sexual reproduction because they did not allow the distributions of mutational effects and interactions (i.e., the genetic architecture) to evolve. Using an artificial gene network model that incorporates evolution of genetic interactions, we allowed populations of a range of sizes and structures of sexual or asexual individuals to evolve to a mutation-selection-drift equilibrium. Sexual reproduction had a long-term advantage in the form of an equilibrium fitness advantage. This was due to a combination of the evolution of more robust genetic architecture and the elimination of Hill-Robertson interference, with the size of the fitness advantage increasing with genetic drift. To investigate the origin and maintenance of costly sex, we introduced a mutation which switched reproductive mode into equilibrium populations at a range of costs of sex. The principle determinant of the success of sex was the transit time of a new mutation to fixation, but the determinant of the maximum cost sex could support and resist invasion was determined by its equilibrium fitness advantage, and costly sex never successfully originated. This contradicts previous studies which demonstrated that the cost supported by sex increased with time to fixation. The key to this difference is that the evolution of genetic interactions curbed the deleterious impact of Hill-Robertson interference on the asexual population, decreasing the potential benefit of sex. The finite maximum sexual fitness advantage capped the maximum sustainable cost to a similar value. Therefore, while we demonstrated conditions which promote the maintenance of costly sex, the sustainable cost was still relatively modest and unlikely to be substantially increased through further manipulations of population structure in absence of other factors that increase the sexual fitness advantage.Doctor of Philosoph