Mathematica notebook from 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 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. 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.

当种群发生二次接触（secondary contact）时，若同一多效基因座（pleiotropic loci）同时受到歧化生态选择（divergent ecological selection）作用并介导非随机交配，便可极大地推动存在基因流的物种形成过程；这类兼具两种偶然功能的基因座被称为‘神奇性状’基因座（magic trait loci）。本研究借助种群遗传学模型（population genetics model），分析由同时承载上述两类功能的物理连锁基因座所构成的‘伪神奇性状复合体’（pseudomagic trait complexes），能否与神奇性状基因座同样高效地促进交配前生殖隔离（premating isolation）。我们着重量化了调控选型交配强度的择偶偏好（choosiness）的演化进程。研究结果出乎意料地显示，只要相关基因座的多态性得以维持，伪神奇性状复合体——乃至在较小程度上物理不连锁的基因座——均可诱导出比神奇性状基因座更强的选型交配偏好演化。究其缘由，当存在产生不适应重组型（maladapted recombinants）的风险时，选型交配偏好通常会受到正向选择；这类风险常见于非神奇性状复合体的场景中，而神奇性状基因座因多效性阻断了重组发生，故而不会出现此类风险。与当前学界的主流观点相悖，神奇性状或许并非实现强交配前生殖隔离的最优遗传架构（genetic architecture）。因此，在推断其在交配前生殖隔离中所扮演的角色时，区分神奇性状与伪神奇性状复合体至关重要，这也呼吁学界针对物种形成基因（speciation genes）开展更为精细的基因组学研究。