The effectiveness of pseudomagic traits in promoting premating isolation

Upon the secondary contact of populations, speciation with gene flow is greatly facilitated when the same pleiotropic loci are both subject to divergent ecological selection and induce non-random mating, leading to loci with this fortuitous combination of functions being referred to as “magic trait” loci. We use a population genetics model to examine whether “pseudomagic trait” complexes, composed of physically linked loci fulfilling these two functions, are as efficient in promoting premating isolation as magic traits. We specifically measure the evolution of choosiness, which controls the strength of assortative mating. We show that, surprisingly, pseudomagic trait complexes, and to a lesser extent also physically unlinked loci, can lead to the evolution of considerably stronger assortative mating preferences than do magic traits, provided polymorphism at the involved loci is maintained. This is because assortative mating preferences are generally favored when there is a risk of producing maladapted recombinants, as occurs with nonmagic trait complexes but not with magic traits (since pleiotropy precludes recombination). Contrary to current belief, magic traits may not be the most effective genetic architecture for promoting strong premating isolation. Distinguishing between magic traits and pseudomagic trait complexes is therefore important when inferring their role in premating isolation. This calls for further fine-scale genomic research on speciation genes.