Tulchinsky Alexander Y, Johnson Norman A, Porter Adam H
Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts Amherst, Massachusetts 01003
Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts Amherst, Massachusetts 01003 Department of Biology, University of Massachusetts, Amherst, Massachusetts 01003 Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts 01003.
Genetics. 2014 Dec;198(4):1645-54. doi: 10.1534/genetics.114.171397. Epub 2014 Oct 13.
Hybrid incompatibility can result from gene misregulation produced by divergence in trans-acting regulatory factors and their cis-regulatory targets. However, change in trans-acting factors may be constrained by pleiotropy, which would in turn limit the evolution of incompatibility. We employed a mechanistically explicit bioenergetic model of gene expression wherein parameter combinations (number of transcription factor molecules, energetic properties of binding to the regulatory site, and genomic background size) determine the shape of the genotype-phenotype (G-P) map, and interacting allelic variants of mutable cis and trans sites determine the phenotype along that map. Misregulation occurs when the phenotype differs from its optimal value. We simulated a pleiotropic regulatory pathway involving a positively selected and a conserved trait regulated by a shared transcription factor (TF), with two populations evolving in parallel. Pleiotropic constraints shifted evolution in the positively selected trait to its cis-regulatory locus. We nevertheless found that the TF genotypes often evolved, accompanied by compensatory evolution in the conserved trait, and both traits contributed to hybrid misregulation. Compensatory evolution resulted in "developmental system drift," whereby the regulatory basis of the conserved phenotype changed although the phenotype itself did not. Pleiotropic constraints became stronger and in some cases prohibitive when the bioenergetic properties of the molecular interaction produced a G-P map that was too steep. Likewise, compensatory evolution slowed and hybrid misregulation was not evident when the G-P map was too shallow. A broad pleiotropic "sweet spot" nevertheless existed where evolutionary constraints were moderate to weak, permitting substantial hybrid misregulation in both traits. None of these pleiotropic constraints manifested when the TF contained nonrecombining domains independently regulating the respective traits.
杂种不亲和性可能源于反式作用调控因子及其顺式调控靶点的分歧所导致的基因调控异常。然而，反式作用因子的变化可能受到多效性的限制，这反过来又会限制不亲和性的进化。我们采用了一个基因表达的机制明确的生物能量模型，其中参数组合（转录因子分子数量、与调控位点结合的能量特性以及基因组背景大小）决定基因型-表型（G-P）图谱的形状，可变顺式和反式位点的相互作用等位基因变体决定该图谱上的表型。当表型与其最优值不同时，就会发生调控异常。我们模拟了一条多效性调控途径，涉及一个由共享转录因子（TF）调控的正选择性状和一个保守性状，两个种群并行进化。多效性限制将正选择性状的进化转移到其顺式调控位点。然而，我们发现TF基因型经常发生进化，同时保守性状也会发生补偿性进化，并且这两个性状都导致杂种调控异常。补偿性进化导致了“发育系统漂移”，即保守表型的调控基础发生了变化，尽管表型本身没有改变。当分子相互作用的生物能量特性产生的G-P图谱过于陡峭时，多效性限制会变得更强，在某些情况下甚至会起阻碍作用。同样，当G-P图谱过于平缓时，补偿性进化会减缓，杂种调控异常也不明显。然而，存在一个广泛的多效性“甜蜜点”，在那里进化限制适中至较弱，允许两个性状都出现大量杂种调控异常。当TF包含独立调控各自性状的非重组结构域时，这些多效性限制均未表现出来。
