Selection on modifiers of genetic architecture under migration load

Gene flow between populations adapting to differing local environmental conditions might be costly because individuals can disperse to habitats where their survival is low or because they can reproduce with locally maladapted individuals. The amount by which the mean relative population fitness is kept below one creates an opportunity for modifiers of the genetic architecture to spread due to selection. Prior work that separately considered modifiers changing dispersal, recombination rates, or altering dominance or epistasis, has typically focused on the direction of selection rather than its absolute magnitude. We here develop methods to determine the strength of selection on modifiers of the genetic architecture, including modifiers of the dispersal rate, in populations that have previously evolved local adaptation. We consider scenarios with up to five loci contributing to local adaptation and derive a new model for the deterministic spread of modifiers. We find that selection for modifiers of epistasis and dominance is stronger than selection for decreased recombination, and that selection for partial reductions in recombination are extremely weak, regardless of the number of loci contributing to local adaptation. The spread of modifiers that reduce dispersal depends on the number of loci, epistasis and extent of local adaptation in the ancestral population. We identify a novel effect, that modifiers of dominance are more strongly selected when they are unlinked to the locus that they modify. These findings help explain population differentiation and reproductive isolation and provide a benchmark to compare selection on modifiers under finite population sizes and demographic stochasticity. Author Summary When populations of a species are spread over different habitats the populations can adapt to their local conditions, provided dispersal between habitats is low enough. Natural selection allows the populations to maintain local adaptation, but dispersal and gene flow create a cost called the migration load. The migration load measures how much fitness is lost because of dispersal between different habitats, and also creates an opportunity for selection to act on the arrangement and interaction between genes that are involved in local adaptation. Modifier genes can spread in these linked populations and cause functional, local adaptation genes, to become more closely linked on a chromosome, or change the way that these genes are expressed so that the locally adapted gene copy becomes dominant. We modeled this process and found that selection on modifiers that create tighter linkage between locally adapted genes is generally weak, and modifiers that cause gene interactions are more strongly selected. Even after these gene interactions have begun to evolve, further selection for increased gene interaction is still strong. Our results show that populations are more likely to adapt to local conditions by evolving new gene interactions than by evolving tightly linked gene clusters.