Miller Jeffrey T, Clark Bryan W, Reid Noah M, Karchner Sibel I, Roach Jennifer L, Hahn Mark E, Nacci Diane, Whitehead Andrew
Department of Environmental Toxicology, Center for Population Biology, Coastal and Marine Sciences Institute University of California, Davis Davis California USA.
Present address: Molecular, Cellular, and Biomedical Sciences University of New Hampshire Durham New Hampshire USA.
Evol Appl. 2024 Jan 29;17(1):e13648. doi: 10.1111/eva.13648. eCollection 2024 Jan.
The genetic architecture of phenotypic traits can affect the mode and tempo of trait evolution. Human-altered environments can impose strong natural selection, where successful evolutionary adaptation requires swift and large phenotypic shifts. In these scenarios, theory predicts that adaptation is due to a few adaptive variants of large effect, but empirical studies that have revealed the genetic architecture of rapidly evolved phenotypes are rare, especially for populations inhabiting polluted environments. killifish have repeatedly evolved adaptive resistance to extreme pollution in urban estuaries. Prior studies, including genome scans for signatures of natural selection, have revealed some of the genes and pathways important for evolved pollution resistance, and provide context for the genotype-phenotype association studies reported here. We created multiple quantitative trait locus (QTL) mapping families using progenitors from four different resistant populations, and using RAD-seq genetically mapped variation in sensitivity (developmental perturbations) following embryonic exposure to a model toxicant PCB-126. We found that one to two large-effect QTL loci accounted for resistance to PCB-mediated developmental toxicity. QTLs harbored candidate genes that govern the regulation of aryl hydrocarbon receptor (AHR) signaling. One QTL locus was shared across all populations and another was shared across three populations. One QTL locus showed strong signatures of recent natural selection in the corresponding wild population but another QTL locus did not. Some candidate genes for PCB resistance inferred from genome scans in wild populations were identified as QTL, but some key candidate genes were not. We conclude that rapidly evolved resistance to the developmental defects normally caused by PCB-126 is governed by few genes of large effect. However, other aspects of resistance beyond developmental phenotypes may be governed by additional loci, such that comprehensive resistance to PCB-126, and to the mixtures of chemicals that distinguish urban estuaries more broadly, may be more genetically complex.
表型性状的遗传结构会影响性状进化的模式和速度。人类改变的环境会施加强大的自然选择，在这种情况下，成功的进化适应需要迅速而巨大的表型转变。在这些情况下，理论预测适应是由于少数具有大效应的适应性变异，但揭示快速进化表型遗传结构的实证研究很少，特别是对于生活在污染环境中的种群。鳉鱼多次进化出对城市河口极端污染的适应性抗性。先前的研究，包括对自然选择特征的全基因组扫描，已经揭示了一些对进化出的抗污染能力重要的基因和途径，并为本文报道的基因型-表型关联研究提供了背景。我们使用来自四个不同抗性种群的祖先创建了多个数量性状基因座（QTL）定位家系，并利用RAD-seq对胚胎暴露于模型毒物多氯联苯-126后敏感性（发育扰动）的遗传变异进行定位。我们发现一到两个具有大效应的QTL基因座导致了对多氯联苯介导的发育毒性的抗性。QTL包含控制芳烃受体（AHR）信号调节的候选基因。一个QTL基因座在所有种群中共享，另一个在三个种群中共享。一个QTL基因座在相应的野生种群中显示出近期自然选择的强烈特征，而另一个QTL基因座则没有。从野生种群的基因组扫描中推断出的一些抗多氯联苯的候选基因被确定为QTL，但一些关键候选基因不是。我们得出结论，对通常由多氯联苯-126引起的发育缺陷的快速进化抗性由少数具有大效应的基因控制。然而，发育表型之外的抗性其他方面可能由其他基因座控制，因此对多氯联苯-126以及更广泛地区分城市河口的化学物质混合物的全面抗性可能在遗传上更为复杂。
