Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, CO 80309-0334, USA.
Integr Comp Biol. 2019 Sep 1;59(3):503-516. doi: 10.1093/icb/icz113.
Temporal variation is a powerful source of selection on life history strategies and functional traits in natural populations. Theory predicts that the rate and predictability of fluctuations should favor distinct strategies, ranging from phenotypic plasticity to bet-hedging, which are likely to have important consequences for species distribution patterns and their responses to environmental change. To date, we have few empirical studies that test those predictions in natural systems, and little is known about how genetic, environmental, and developmental factors interact to define the "fluctuation niche" of species in temporally variable environments. In this study, we evaluated the effects of hydrological variability on fitness and functional trait variation in three closely related plant species in the genus Lasthenia that occupy different microhabitats within vernal pool landscapes. Using a controlled greenhouse experiment, we manipulated the mean and variability in hydrological conditions by growing plants at different depths with respect to a shared water table and manipulating the magnitude of stochastic fluctuations in the water table over time. We found that all species had similarly high relative fitness above the water table, but differed in their sensitivities to water table fluctuations. Specifically, the two species from vernal pools basins, where soil moisture is controlled by a perched water table, were negatively affected by the stochasticity treatments. In contrast, a species from the upland habitat surrounding vernal pools, where stochastic precipitation events control soil moisture variation, was insensitive to experimental fluctuations in the water table. We found strong signatures of genetic, environmental (plastic), and developmental variation in four traits that can influence plant hydrological responses. Three of these traits varied across plant development and among experimental treatments in directions that aligned with constitutive differences among species, suggesting that multiple sources of variation align to facilitate phenotypic matching with the hydrological environment in Lasthenia. We found little evidence for predicted patterns of phenotypic plasticity and bet-hedging in species and traits from predictable and stochastic environments, respectively. We propose that selection for developmental shifts in the hydrological traits of Lasthenia species has reduced or modified selection for plasticity at any given stage of development. Collectively, these results suggest that variation in species' sensitivities to hydrological stochasticity may explain why vernal pool Lasthenia species do not occur in upland habitat, and that all three species integrate genetic, environmental, and developmental information to manage the unique patterns of temporal hydrological variation in their respective microhabitats.
时间变化是自然种群中对生活史策略和功能特征进行选择的强大来源。理论预测，波动的速度和可预测性应该有利于不同的策略，从表型可塑性到赌注避险，这可能对物种分布模式及其对环境变化的反应产生重要影响。迄今为止，我们在自然系统中进行的测试这些预测的实证研究很少，并且对于遗传、环境和发育因素如何相互作用来定义物种在时间变化环境中的“波动生态位”知之甚少。在这项研究中，我们评估了水文变异性对三种密切相关的 Lasthenia 属植物在春季池塘景观中不同小生境中占据的植物的适应性和功能特征变化的影响。我们使用受控温室实验，通过在相对于共享水位的不同深度种植植物并随时间操纵水位随机波动的幅度来操纵水文条件的平均值和可变性。我们发现，所有物种在水位以上的相对适应性都很高，但对水位波动的敏感性不同。具体来说，来自春季池塘盆地的两个物种，其中土壤湿度由一个停歇水位控制，受到随机处理的负面影响。相比之下，来自春季池塘周围高地栖息地的一个物种，其土壤湿度变化由随机降水事件控制，对水位的实验波动不敏感。我们在四个可能影响植物水文响应的特征中发现了遗传、环境（可塑性）和发育变异的强烈特征。这四个特征中的三个在植物发育过程中发生变化，并在实验处理之间发生变化，与物种之间的组成差异一致，这表明多种变异源可以与春季池塘的水文环境相匹配。我们发现，在可预测和随机环境中分别具有预测的表型可塑性和赌注避险模式的物种和特征中，几乎没有证据表明存在这种模式。我们提出，在春季池塘的水文特征上的发育变化选择减少或改变了在任何特定发育阶段的可塑性选择。总的来说，这些结果表明，物种对水文随机性的敏感性的变化可能解释了为什么春季池塘的 Lasthenia 物种不在高地生境中出现，并且所有三个物种都整合了遗传、环境和发育信息，以管理其各自小生境中独特的时间水文变化模式。
