The effectiveness of pseudomagic traits in promoting premating isolation

Abstract

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 favoured when there is a risk of producing maladapted recombinants, as occurs with non-magic 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. Therefore, distinguishing between magic traits and pseudomagic trait complexes is important when inferring their role in premating isolation. This calls for further fine-scale genomic research on speciation genes.

Times birds need to evolve mating cues under allopatry and parapatry

“…3, but if some individuals mate with others of a different phenotype then the mating cue selection coefficient would be reduced. The evolution of choosiness could be explored using the methods and results of (Aubier et al, 2023) as a starting point, and theoretical equations with which to investigate this and other parameter variants are available in (Sibly and Curnow, 2022), though further work is needed to see what happens when key genes are not dominant. Simulations carried out as in (Sibly and Curnow, 2022).…”

“…It is also assumed that assortative mating has no costs, but being choosy may reduce the chance of mating, reducing the mating cue selection coefficient in the parapatric models (Aubier et al, 2023;Kopp and Hermisson, 2008;Schneider and Burger, 2006). The probability of a mutation arising is 1 െ ሺ1 െ ߤሻ ଶே and this is approximated as 2ܰߤ.…”

Genetic analysis of mate sorting in females and its association with host fruit specialization in interbreeding species of Drosophila

“…Multiple examples of tight linkage and pleiotropy linking loci that confer mate choice and loci that confer adaptive differences exist in the literature (Bay et al, 2017;Hawthorne and Via, 2001b;Rossi et al, 2020). Yet recent models suggest that even the existence of loci that confer assortative mating and loci that confer adaptive traits together in the same genome will be sufficient to facilitate divergence, regardless of the distance between loci for either trait (Aubier, Bürger and Servedio, 2023). So far the literature has only produced one example of long distance coupling between adaptive and mate choice loci (Hench et al, 2019).…”

“…Linkage disequilibrium between assortative mating and ecological traits has also been seen across chromosomes (Hench et al, 2019). Recently, modeling studies that explore how boundaries are maintained after secondary contact show that divergence is favored when genes that influence mate sorting are weakly linked or even unlinked to genes that confer adaptive divergence (Aubier, Bürger and Servedio, 2023;Servedio and Bürger, 2020). Both theoretical and empirical work, therefore, indicate that more complex interactions than just pleiotropy and tight linkage may be effective in coupling adaptation with mate choice.…”

Computer Simulation and Mathematical Modeling of the Interactions Between Ecological and Sexual Selection to Reveal the Mechanism of Sympatric Speciation

“…Our goal is to solve the "hard process" of sympatric speciation [2] by assuming the absence of geographical barriers that can impede mating encounters or gene flow. The expectation is that once we can explain hard sympatric speciation, other "easy processes" of sympatric speciation, such as those due to magic trait [12,50,51], secondary contact [2,52], or limited gene flow [53][54][55][56], become readily solvable.…”