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.

资源在塑造植物防御策略的进化过程中发挥着重要作用。资源可获得性如何影响物种内整体植物化学多样性（phytochemical diversity），以及这种影响如何进而作用于植食性损害（herbivore damage），目前尚不清楚。本研究以管花蜂香薄荷（Monarda fistulosa）为对象——该物种可产生多种萜类化合物（terpene compounds）及不同的化学型（chemotypes）（即百里酚型或香芹酚型）——探讨了三个问题：1）来自气候和生产力存在差异、相距遥远的两个大区域的不同种群，其植物化学成分（即总浓度、香农多样性（Shannon diversity）及化学型）存在怎样的差异？2）这些成分如何影响不同植食性物种的侵害？3）不同化学型中较高的植物化学水平会产生怎样的生长代价？研究人员从降水驱动生产力存在差异的两个区域的12个种群中采集种子——其中6个来自蒙大拿州的低生产力环境，6个来自威斯康星州的高生产力环境——并在威斯康星州的共同园圃中种植。我们分析了萜类化合物浓度，量化了植食性动物数量及损害程度，并测定了植物的地上生物量。蒙大拿州的植株表现出较高的萜类化合物浓度但较低的多样性，而威斯康星州的植株则相反，萜类化合物浓度较低但多样性较高。与蒙大拿州的植株相比，威斯康星州的植株受到专一性种子捕食者和食叶性植食动物的损害更严重，尽管专一性蚜虫的丰度较低。总萜类化合物浓度成为植食性损害的主要预测因子，尽管原产地之间及萜类丰富度方面存在一些差异。植食性动物对植物化学特性表现出混合反应：部分植食性动物受到负面影响，而专一性叶瘿虫则表现出正面响应。防御物质产生的代价通过植物生物量与总萜类化合物浓度之间的负相关得以体现（但与化学丰富度或香农多样性无关）。本研究揭示，生产力的区域差异可影响植物化学浓度及多样性的进化，进而影响植物损害程度并产生与生长相关的代价。