Sexual reproduction selects for robustness and negative epistasis in artificial gene networks

Abstract

The mutational deterministic hypothesis for the origin and maintenance of sexual reproduction posits that sex enhances the ability of natural selection to purge deleterious mutations after recombination brings them together into single genomes. This explanation requires negative epistasis, a type of genetic interaction where mutations are more harmful in combination than expected from their separate effects. The conceptual appeal of the mutational deterministic hypothesis has been offset by our inability to identify the mechanistic and evolutionary bases of negative epistasis. Here we show that negative epistasis can evolve as a consequence of sexual reproduction itself. Using an artificial gene network model, we find that recombination between gene networks imposes selection for genetic robustness, and that negative epistasis evolves as a by-product of this selection. Our results suggest that sexual reproduction selects for conditions that favour its own maintenance, a case of evolution forging its own path.

On the evolution of epistasis III: The haploid case with mutation

“…Our results appear to differ from those of Azevedo et al (2006), although these authors did not use a modifier gene to alter epistasis. They found that with recombination there should generally be selection towards (negative) synergistic epistasis.…”

“…Thus how the shape of this function evolves is also important. An approximate numerical treatment by Azevedo et al (2006) concluded that when deleterious mutations can recombine there should be selection towards negative (synergistic) epistasis, but without recombination, positive epistasis should evolve. Understanding how epistasis evolves has broader implications, as epistatic interactions are "central to the evolution of genetic recombination" (Michalakis and Roze 2004).…”

Genetic background affects epistatic interactions between two beneficial mutations

“…This dependence, known as epistasis, is important to many areas of developmental and evolutionary biology, including speciation [1][2][3][4], the maintenance of sex [5,6], adaptation [7][8][9], the evolution of ploidy [10] and evolutionary contingency [11 -14]. As the technology to identify and manipulate specific mutations becomes increasingly available, the influence of epistasis can be examined directly.…”

The evolution of genetic architectures underlying quantitative traits

“…where f b is a standard sigmoidal filter function (see Methods; see also electronic supplementary material, figure S4a) [8]. As with the direct effects of loci, the epistatic effects were allowed to mutate and vary within the population, and evolve.…”

“…The resulting genetic architecture of a trait [1] influences its variational properties [2][3][4][5], and therefore affects a population's capacity to adapt to new environmental conditions [1,6,7]. Over longer time scales, genetic architectures of traits have important consequences for the evolution of recombination [8] and of sex [9], and even reproductive isolation and speciation [10].…”