Division of Evolutionary Ecology, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland.
Mol Ecol. 2022 Mar;31(5):1476-1486. doi: 10.1111/mec.16335. Epub 2022 Jan 22.
Highly pleiotropic genes are predicted to be used less often during adaptation, as mutations in these loci are more likely to have negative fitness consequences. Following this logic, we tested whether pleiotropy impacts the probability that a locus will be used repeatedly in adaptation. We used two proxies to estimate pleiotropy: number of phenotypic traits affected by a given genomic region and gene connectivity. We first surveyed 16 independent stream-lake and three independent benthic-limnetic ecotype pairs of threespine stickleback to estimate genome-wide patterns in parallel genomic differentiation. Our analysis revealed parallel divergence across the genome; 30%-37% of outlier regions were shared between at least two independent pairs in either the stream-lake or benthic-limnetic comparisons. We then tested whether parallel genomic regions are less pleiotropic than nonparallel regions. Counter to our a priori prediction, parallel genomic regions contained genes with significantly more pleiotropy; that is, influencing a greater number of traits and more highly connected. The increased pleiotropy of parallel regions could not be explained by other genomic factors, as there was no significant difference in mean gene count, mutation or recombination rates between parallel and nonparallel regions. Interestingly, although nonparallel regions contained genes that were less connected and influenced fewer mapped traits on average than parallel regions, they also tended to contain the genes that were predicted to be the most pleiotropic. Taken together, our findings are consistent with the idea that pleiotropy only becomes constraining at high levels and that low or intermediate levels of pleiotropy may be beneficial for adaptation.
高度多效性基因在适应过程中被预测使用的频率较低，因为这些基因座的突变更有可能产生负面的适应度后果。根据这一逻辑，我们测试了多效性是否会影响一个基因座在适应过程中被重复使用的概率。我们使用了两个代理来估计多效性：一个给定基因组区域影响的表型性状数量和基因连通性。我们首先调查了 16 个独立的溪流-湖泊和三个独立的底栖-中上层生态型对三种棘鱼的配对，以估计全基因组范围内平行基因组分化的模式。我们的分析揭示了基因组的平行分化；在溪流-湖泊或底栖-中上层比较中，至少有两个独立对之间共享了 30%-37%的外显子区域。然后，我们测试了平行基因组区域是否比非平行区域的多效性更低。与我们的先验预测相反，平行基因组区域包含的基因具有明显更多的多效性；也就是说，影响更多的性状和更高的连通性。平行区域增加的多效性不能用其他基因组因素来解释，因为在平行和非平行区域之间，基因平均数量、突变或重组率没有显著差异。有趣的是，尽管非平行区域包含的基因连接性较低，平均影响的映射性状较少，但它们也倾向于包含预测最具多效性的基因。总的来说，我们的研究结果与多效性只有在高水平时才会受到限制的观点一致，而低水平或中等水平的多效性可能有利于适应。
