Intraspecific phytochemical diversity increases with productivity but has mixed effects on herbivory

Resources play an important role in shaping the evolution of plant defensive strategies. How resource availability influences overall phytochemical diversity within species, and how this in-turn affects herbivore damage is not well understood. Using Monarda fistulosa, a species that produces diverse terpene compounds and distinct chemotypes (i.e., thymol or carvacrol), we addressed three questions: 1) How do phytochemical components (i.e., total concentration, Shannon diversity, and chemotypes) vary between distinct populations from two large, widely separated regions that differ in climate and productivity? 2) How do these components influence attack by different herbivore species? 3) What are the growth costs of higher phytochemical levels in different chemotypes? Seeds were collected from 12 populations spread across two regions that differ in precipitation-driven productivity, six from a low-productivity environment in Montana and six from a high-productivity environment in Wisconsin, and grown in a common garden in Wisconsin. We analyzed terpene concentrations, quantified the number of herbivores and damage, and measured plant above-ground biomass. Plants from Montana exhibited higher terpene concentrations but lower diversity, whereas those from Wisconsin displayed lower terpene concentrations but higher diversity. Plants from Wisconsin received more damage from a specialist seed predator and leaf-chewing herbivores, although abundance of a specialist aphid was lower, compared to plants from Montana. Total terpene concentration emerged as the primary predictor of herbivore damage, although some differences were observed between region of origin and with terpene richness. Herbivores exhibited mixed responses to phytochemistry; some herbivores were negatively affected, while a specialized leaf galler responded positively. Costs of producing defenses were evident by negative correlations between plant biomass and total terpene concentration (but not chemical richness or Shannon diversity). Our study revealed that regional differences in productivity can influence the evolution of phytochemical concentration and diversity, which, in turn, affects plant damage and incurs growth-related costs.

Methods
Data was collected in a common garden and laboratory. Data files are raw data and processed with the associated R script. Detailed methods are described in the associated paper.

资源在调控植物防御策略的演化进程中扮演着核心角色。目前学界对于资源可利用性如何影响物种内整体植物化学物质（phytochemical）多样性，以及该过程继而如何作用于植食性危害的认知仍较为有限。本研究以管蜂香薄荷（Monarda fistulosa）为研究对象，该物种可合成多种萜类化合物（terpene）并具有明确的化学型（chemotypes，即麝酚型或香芹酚型），我们旨在解答三个科学问题：1） 来自气候与生产力存在显著差异的两个大型、地理隔离区域的不同种群，其植物化学组分（即总浓度、香农多样性及化学型）存在何种变异？2） 上述植物化学组分如何影响不同植食性物种的攻击行为？3） 不同化学型的植物合成更高水平植物化学物质的生长成本具体为何？

我们从两个受降水驱动的生产力存在差异的区域内的12个种群中采集种子：其中6个种群来自美国蒙大拿州的低生产力生境，另外6个种群来自美国威斯康星州的高生产力生境，并将这些种子种植于威斯康星州的同质种植园（common garden）中。我们对萜类化合物浓度进行了分析，量化了植食性动物的数量与危害程度，并测定了植物的地上生物量。

研究结果显示，来自蒙大拿州的植株萜类化合物总浓度更高，但多样性更低；而来自威斯康星州的植株则呈现出相反的特征：萜类总浓度更低，但多样性更高。与蒙大拿州的植株相比，威斯康星州的植株受到专性种子捕食者与食叶植食性昆虫的危害更为严重，但专性蚜虫的种群丰度更低。植物萜类总浓度是预测植食性危害的核心指标，尽管在起源区域与萜类丰富度之间仍存在部分差异。不同植食类群对植物化学物质的响应存在分化：部分植食类群受到显著的负向影响，而一种专性叶瘿蚊则呈现出正向响应。植物生物量与萜类总浓度之间存在显著负相关（但与化学丰富度或香农多样性无显著关联），这表明合成防御物质存在生长成本。

本研究表明，区域间的生产力差异能够影响植物化学浓度与多样性的演化，进而作用于植株的植食性危害程度，并带来与生长相关的适应性成本。

方法
本研究的数据采集于同质种植园与实验室。数据文件包含原始数据与经配套R脚本处理后的分析结果。详细的实验方法已在相关研究论文中进行了阐述。