Predicting the strength of urban-rural clines in a Mendelian polymorphism along a latitudinal gradient

AbstractCities are emerging as models for addressing the fundamental question of whether populations evolve in parallel to similar environments. Here, we examine the environmental factors that drive the evolution of parallel urban-rural clines in a Mendelian trait—the cyanogenic antiherbivore defense of white clover (Trifolium repens). Previous work suggested urban-rural gradients in frost and snow depth could drive the evolution of reduced hydrogen cyanide (HCN) frequencies in urban populations. Here, we sampled over 700 urban and rural clover populations across 16 cities along a latitudinal transect in eastern North America. In each population, we quantified changes in the frequency of genotypes that produce HCN, and in a subset of the cities we estimated the frequency of the alleles at the two genes (CYP79D15 and Li) that epistatically interact to produce HCN. We then tested the hypothesis that cold climatic conditions are necessary for the evolution of cyanogenesis clines by comparing the strength of clines among cities located along a gradient of winter temperatures and frost exposure. Overall, half of the cities exhibited urban-rural clines in the frequency of HCN, whereby urban populations evolved lower HCN frequencies. Clines did not evolve in cities with the lowest temperatures and greatest snowfall, supporting the hypothesis that snow buffers plants against winter frost and constrains the formation of clines. By contrast, the strongest clines occurred in the warmest cities where snow and frost are rare, suggesting that alternative selective agents are maintaining clines in warmer cities. Some clines were driven by evolution at only CYP79D15, consistent with stronger and more consistent selection on this locus than on Li. Together, our results demonstrate that urban environments often select for similar phenotypes, but different selective agents and targets underlie the evolutionary response in different cities., MethodsPlants were collected in the field and brought back to the lab for phenotyping. Environmental data was collected from publically available datasets. Phenotype and environmental data were processed in R v3.6.1. All scripts used for data processing and analyses are contained in the ZIP file associated with this repository. Code and data are similarly available in this Github repository, Usage notesSee README files in atached ZIP folder.摘要 城市正逐渐成为研究“群体是否会在相似环境下发生平行演化”这一基础科学问题的理想模型。本研究聚焦于驱动孟德尔性状——白三叶（Trifolium repens）的产氰抗草食动物防御机制——的城乡平行渐变群演化的环境因子。既往研究表明，霜冻与积雪深度的城乡梯度可能推动城市种群中氢氰酸（HCN）产生频率降低的演化过程。本研究沿北美东部的纬度样带，在16座城市中采集了700余个城乡白三叶种群样本。我们对每个种群中产HCN的基因型频率变化进行了定量分析，并在部分城市中估算了两个通过上位互作产生HCN的基因（CYP79D15与Li）的等位基因频率。随后，我们通过比较沿冬季温度与霜冻暴露梯度分布的城市间渐变群的强度，验证了“寒冷气候条件是产氰渐变群演化的必要条件”这一假说。总体而言，半数城市的HCN产生频率呈现城乡渐变群特征，即城市种群的HCN产生频率更低。在温度最低、积雪最多的城市中未出现渐变群，这一结果支持“积雪可缓冲植物冬季霜冻胁迫并限制渐变群形成”的假说。与之相反，最强的渐变群出现在积雪与霜冻均罕见的最温暖城市，这表明存在其他选择因子维持了温暖城市中的渐变群。部分渐变群仅由CYP79D15位点的演化所驱动，这与该位点相较于Li位点受到更强且更持续的选择作用的结论一致。综上，本研究结果表明，城市环境通常会筛选出相似的表型，但不同城市的演化响应背后的选择因子与作用靶点并不相同。 方法 从野外采集植株并带回实验室进行表型鉴定。环境数据取自公开可用的数据集。表型与环境数据均通过R v3.6.1进行处理。所有用于数据处理与分析的脚本均收纳于本研究仓库附带的压缩包中。代码与数据同样可在本GitHub仓库中获取。 使用说明 详见附件压缩包中的README文件。