Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens)

Urbanization is a global phenomenon with profound effects on the ecology and evolution of organisms. We examined the relative roles of natural selection, genetic drift and gene flow in influencing the evolution of white clover (Trifolium repens), which thrives in urban and rural areas. Trifolium repens exhibits a Mendelian polymorphism for the production of hydrogen cyanide (HCN), a potent antiherbivore defence. We quantified the relative frequency of HCN in 490 populations sampled along urban-rural transects in 20 cities. We also characterized genetic variation within 120 populations in eight cities using 16 microsatellite loci. HCN frequency increased by 0.6% for every km from an urban centre, and the strength of this relationship did not significantly vary between cities. Populations did not exhibit changes in genetic diversity with increasing urbanization, indicating that genetic drift is unlikely to explain urban-rural clines in HCN frequency. Populations frequently exhibited isolation-by-distance and extensive gene flow along most urban-rural transects, with the exception of a single city that exhibited genetic differentiation between urban and rural populations. Our results show that urbanization repeatedly drives parallel evolution of an ecologically important trait across many cities that vary in size, and this evolution is best explained by urban-rural gradients in natural selection.

城市化是全球性现象，对生物的生态过程与演化进程具有深远影响。本研究以在城市与乡村生境中均能良好生长的白三叶（Trifolium repens）为研究对象，探究了自然选择、遗传漂变与基因流在其演化过程中的相对作用。白三叶具有与氰化氢（HCN）合成相关的孟德尔式多态性，而氰化氢是一种强效的抗草食动物防御物质。我们对全球20座城市的城乡样带中采集的490个白三叶种群的HCN相对频率进行了定量分析。此外，我们利用16个微卫星位点（microsatellite loci），对其中8座城市的120个白三叶种群的遗传变异进行了解析。距城市中心每远1公里，种群的HCN频率便提升0.6%，且该关联的强度在不同城市间无显著差异。随着城市化水平升高，种群的遗传多样性未发生显著变化，这表明遗传漂变无法解释HCN频率的城乡渐变群（urban-rural clines）现象。在多数城乡样带中，种群普遍呈现距离隔离（isolation-by-distance）模式并存在广泛的基因流，仅一座城市的城乡种群间出现了遗传分化。本研究结果表明，城市化在不同规模的众多城市中反复推动了某一生态重要性状的平行演化，而该演化过程可通过城乡间的自然选择梯度得到最佳解释。