Graduate Degree Program in Ecology and Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, Colorado 80523, USA. 2Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, Colorado 80309 USA.
Ecology. 2012 Aug;93(8):1912-21. doi: 10.1890/11-1946.1.
Optimal defense theory posits that plants with limited resources deploy chemical defenses based on the fitness value of different tissues and their probability of attack. However, what constitutes optimal defense depends on the identity of the herbivores involved in the interaction. Generalists, which are not tightly coevolved with their many host plants, are typically deterred by chemical defenses, while coevolved specialists are often attracted to these same chemicals. This imposes an "evolutionary dilemma" in which generalists and specialists exert opposing selection on plant investment in defense, thereby stabilizing defenses at intermediate levels. We used the natural shift in herbivore community composition that typifies many plant invasions to test a novel, combined prediction of optimal defense theory and the evolutionary dilemma model: that the within-plant distribution of defenses reflects both the value of different tissues (i.e., young vs. old leaves) and the relative importance of specialist and generalist herbivores in the community. Using populations of Verbascum thapsus exposed to ambient herbivory in its native range (where specialist and generalist chewing herbivores are prevalent) and its introduced range (where only generalist chewing herbivores are prevalent), we illustrate significant differences in the way iridoid glycosides are distributed among young and old leaves. Importantly, high-quality young leaves are 6.5x more highly defended than old leaves in the introduced range, but only 2x more highly defended in the native range. Additionally, defense levels are tracked by patterns of chewing damage, with damage restricted mostly to low-quality old leaves in the introduced range, but not the native range. Given that whole-plant investment in defense does not differ between ranges, introduced mullein may achieve increased fitness simply by optimizing its within-plant distribution of defense in the absence of certain specialist herbivores.
最优防御理论认为，资源有限的植物会根据不同组织的适合度值及其受攻击的概率来部署化学防御。然而，什么是最优防御取决于参与相互作用的食草动物的身份。非专化性食草动物（与许多宿主植物没有紧密协同进化）通常会被化学防御所阻止，而协同进化的专化性食草动物往往会被这些相同的化学物质所吸引。这就产生了一个“进化困境”，即非专化性食草动物和专化性食草动物对植物防御投资施加了相反的选择，从而使防御稳定在中等水平。我们利用食草动物群落组成的自然变化来检验最优防御理论和进化困境模型的一个新的综合预测：防御在植物体内的分布既反映了不同组织的价值（即幼叶与老叶），也反映了专化性和非专化性食草动物在群落中的相对重要性。我们使用生长在其原生环境中的欧洲婆婆纳种群（其中专化性和非专化性咀嚼食草动物很常见）和引入环境中的种群（其中只有非专化性咀嚼食草动物很常见），说明了生物体内糖苷在幼叶和老叶之间的分布方式存在显著差异。重要的是，在引入环境中，高质量的幼叶比老叶受保护程度高 6.5 倍，但在原生环境中仅高 2 倍。此外，防御水平与咀嚼损伤模式相关，在引入环境中，损伤主要局限于低质量的老叶，但在原生环境中则没有。鉴于植物在整个植株上的防御投资在两个环境中没有差异，引入的婆婆纳可能通过优化其在植物体内的防御分布来提高适应性，而不需要某些专化性食草动物。
