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

Abstract

We build on previous observations that Hill–Robertson interference generates an advantage of sex that, in structured populations, can be large enough to explain the evolutionary maintenance of costly sex. We employed a gene network model that explicitly incorporates interactions between genes. Mutations in the gene networks have variable effects that depend on the genetic background in which they appear. Consequently, our simulations include two costs of sex—recombination and migration loads—that were missing from previous studies of the evolution of costly sex. Our results suggest a critical role for population structure that lies in its ability to align the long‐ and short‐term advantages of sex. We show that the addition of population structure favored the evolution of sex by disproportionately decreasing the equilibrium mean fitness of asexual populations, primarily by increasing the strength of Muller's Ratchet. Population structure also increased the ability of the short‐term advantage of sex to counter the primary limit to the evolution of sex in the gene network model—recombination load. On the other hand, highly structured populations experienced migration load in the form of Dobzhansky–Muller incompatibilities, decreasing the effective rate of migration between demes and, consequently, accelerating the accumulation of drift load in the sexual populations.

Natural selection promotes the evolution of recombination 1: between the products of natural selection*

“…That these early studies of inbreeding and heterosis are relevant to the evolution of sex and recombination is not a new idea [11,20,21], and is subsumed under Lewontin's general proclamation that "every discovery in classical and population genetics has depended on some sort of inbreeding experiment" [20,22,23]. Since these early studies, several more recent studies have shown that different kinds of population structure can create conditions that make recombination across locally-evolving subpopulations favorable [10][11][12][24][25][26][27][28][29]. These studies find that population structure can help to maintain the variation without which recombination would be neither advantageous nor disadvantageous, and they identify conditions under which recombination is advantageous.…”

Natural selection and the advantage of recombination

“…Components X (n) and Y (n) , therefore, while not What we have shown so far is that, if recombination occurs across the products of natural selection, such as fixed genotypes in different populations, subpopulations, demes or competing clones, the resulting offspring should be more fit than their parents, on average. This effect provides novel insight into established observations that population structure can favor recombination [29][30][31][32][33] and may even speak to notions that out-crossing can create hybrid vigour (heterosis).…”

Migration promotes mutator alleles in subdivided populations

“…; Whitlock et al. ) and cooperation (Nowak ; Taylor and Nowak ) in sufficiently structured populations. Similar to its effect on mutators, population subdivision allows costly recombiner alleles to persist in a metapopulation despite indirect selection against the recombination load—the cost of unfavorable combinations of alleles.…”