An Evolving Genetic Architecture Interacts with Hill–Robertson Interference to Determine the Benefit of Sex

Abstract

Sex is ubiquitous in the natural world, but 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 HillRobertson interference. However, those studies may have missed both important advantages and important disadvantages of sexual reproduction because they did not allow the distributions of mutational effects and interactions (i.e., the genetic architecture) to evolve. Here we investigate how Hill-Robertson interference interacts with an evolving genetic architecture to affect the evolutionary origin and maintenance of sex by simulating evolution in populations of artificial gene networks. We observed a long-term advantage of sexequilibrium mean fitness of sexual populations exceeded that of asexual populations-that did not depend on population size. We also observed a short-term advantage of sex-sexual modifier mutations readily invaded asexual populations-that increased with population size, as was observed in previous studies. We show that the long-and short-term advantages of sex were both determined by differences between sexual and asexual populations in the evolutionary dynamics of two properties of the genetic architecture: the deleterious mutation rate (U d ) and recombination load (L R ). These differences resulted from a combination of selection to minimize L R ; which is experienced only by sexuals, and Hill-Robertson interference experienced primarily by asexuals. In contrast to the previous studies, in which Hill-Robertson interference had only a direct impact on the fitness advantages of sex, the impact of Hill-Robertson interference in our simulations was mediated additionally by an indirect impact on the efficiency with which selection acted to reduce U d : KEYWORDS evolution of sex; gene network; deleterious mutation rate; recombination load; population size T HE vast majority of organisms alive today have experienced some form of genetic exchange, or sex, in their recent evolutionary history, despite substantial costs (Weismann 1887;Maynard Smith 1978;Bell 1982;Otto and Lenormand 2002). Sex breaks up favorable genetic combinations and increases the risk of transmission of pathogens and selfish genetic elements. Sexual reproduction is often slower than asexual reproduction. In many sexually reproducing eukaryotes, sex involves costs of finding and attracting a mate and of mating in itself; in anisogamous species, if one sex contributes little to progeny production, sexual reproduction carries a twofold cost of producing that sex. The ubiquity of sex implies that it must confer considerable benefits to overcome these costs. However, the nature of these benefits is not well understood. In fact, .20 hypotheses have been proposed to explain the benefits of sex (Bell 1982;Kondrashov 1993;Hurst and Peck 1996;Otto and Lenormand 2002). While hypotheses predicting direct benefits exist [e.g., improved DNA repair (Bernstein et al. 1985)], t...

Population structure promotes the evolution of costly sex in artificial gene networks

“…of Whitlock et al. ). This value is comparable to those estimated for fruit flies (, Haag‐Liautard et al.…”

“…We used the same parameters as in Whitlock et al. (): networks of genes with connectivity density , a genomic mutation rate of per generation, and stabilizing selection . Using these parameters, mutations have a broad range of potential fitness effects, including beneficial, neutral, slightly deleterious, and lethal (Fig.…”

“…; Whitlock et al. ). As in real biological systems, mutations in the gene networks have variable effects that depend on the genetic background in which they appear, so that both magnitude and sign epistasis (Weinreich et al.…”

“…Together, these processes have the potential to create both a long‐term advantage for sexual populations, in the form of higher equilibrium mean fitness (Whitlock et al. ), and a short‐term advantage, in the form of an increased likelihood of resisting invasion by asexual mutants (Hartfield et al. ).…”

“…In panmictic populations of artificial gene networks, the recombination load that results from sign epistasis limited the conditions under which sex was able to evolve and to be maintained, and prevented the origin of costly sex entirely (Whitlock et al. ).…”