Landscape genetics reveals unique and shared effects of urbanization for two sympatric pool-breeding amphibians

Metapopulation-structured species can be negatively affected when landscape fragmentation impairs connectivity. We investigated the effects of urbanization on genetic diversity and gene flow for two sympatric amphibian species, spotted salamanders (Ambystoma maculatum) and wood frogs (Lithobates sylvaticus), across a large (>35,000 km2) landscape in Maine, USA, containing numerous natural and anthropogenic gradients. Isolation by distance (IBD) patterns differed between the species. Spotted salamanders showed a linear and relatively high variance relationship between genetic and geographic distance (r = 0.057; p < 0.001); whereas, wood frogs exhibited a strongly non-linear and lower variance relationship (r = 0.429; p < 0.001). Scale dependence analysis of IBD found gene flow has its most predictable influence (strongest IBD correlations) at distances up to 9 km for spotted salamanders and up to 6 km for wood frogs. Estimated effective migration surfaces revealed contrasting patterns of high and low genetic diversity and gene flow between the two species. Population isolation, quantified as the mean IBD residuals for each population, was associated with local urbanization and less genetic diversity in both species. The influence of geographic proximity and urbanization on population connectivity was further supported by distance-based redundancy analysis and multiple matrix regression with randomization. Resistance surface modelling found interpopulation connectivity to be influenced by developed land cover, light roads, interstates, and topography for both species, plus secondary roads and rivers for wood frogs. Our results highlight the influence of anthropogenic landscape features within the context of natural features and broad spatial genetic patterns, in turn supporting the premise that while urbanization significantly restricts interpopulation connectivity for wood frogs and spotted salamanders, specific landscape elements have unique effects on these two sympatric species.

当景观破碎化（landscape fragmentation）损害连通性（connectivity）时，集合种群（metapopulation）结构的物种可能会受到负面影响。我们在美国缅因州一片面积逾35000平方千米、涵盖众多自然与人为梯度的景观中，探究了城市化对两种同域两栖动物——斑点钝口螈（Ambystoma maculatum）和林蛙（Lithobates sylvaticus）的遗传多样性与基因流（gene flow）的影响。两种物种的距离隔离（IBD）模式存在显著差异：斑点钝口螈的遗传距离与地理距离呈线性相关，且变异程度相对较高（r=0.057；p<0.001）；而林蛙则表现出强烈的非线性相关，且变异程度较低（r=0.429；p<0.001）。对距离隔离的尺度依赖分析显示，基因流影响的可预测性最强（即距离隔离相关性最显著）的空间尺度分别为：斑点钝口螈不超过9千米，林蛙不超过6千米。估算得到的有效迁移表面（effective migration surfaces）揭示了两种物种在遗传多样性和基因流高低上的截然不同的分布模式。以各种群平均距离隔离残差量化的种群隔离程度，与两种物种的局部城市化水平及较低的遗传多样性均呈显著关联。基于距离的冗余分析（distance-based redundancy analysis）与随机化多重矩阵回归（multiple matrix regression with randomization）进一步证实了地理邻近性和城市化对种群连通性的影响。阻力面建模（resistance surface modelling）结果显示，两种两栖动物的种群间连通性均受开发型土地覆被、轻型道路、州际公路及地形的影响，而林蛙的种群连通性还额外受到次级道路与河流的影响。本研究结果凸显了人为景观特征在自然特征与大空间尺度遗传格局背景下的调控作用，同时支持了如下论点：尽管城市化显著限制了林蛙与斑点钝口螈的种群间连通性，但特定景观要素对这两种同域物种的影响存在特异性。