Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, USA.
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA.
Ecology. 2022 Nov;103(11):e3786. doi: 10.1002/ecy.3786. Epub 2022 Jul 25.
Spatiotemporal variation in herbivory is a major driver of intraspecific variation in plant defense. Comparatively little is known, however, about how changes in herbivory regime affect the balance of constitutive and induced resistance, which are often considered alternative defensive strategies. Here, we investigated how nearly a decade of insect herbivore suppression affected constitutive and induced resistance in horsenettle (Solanum carolinense), a widespread herbaceous perennial. We allowed replicated horsenettle populations to respond to the presence or absence of herbivores by applying insecticide to all plants in half of 16 field plots. Horsenettle density rapidly increased in response to insecticide treatment, and this effect persisted for at least 4 years after the cessation of herbivore suppression. We subsequently grew half-sibling families from seeds collected during and shortly after insecticide treatment in a common garden and found strong effects of insect suppression on induced resistance. Feeding trials in field mesocosms with false Colorado potato beetles (Leptinotarsa juncta), a common specialist herbivore, revealed that multiyear herbivore suppression drove rapid attenuation of induced resistance: offspring of plants from insect-suppression plots exhibited a near-complete loss of induced resistance to beetles, whereas those from control plots incurred ~70% less damage after experimental induction. Plants from insect-suppression plots also had ~40% greater constitutive resistance compared with those from control plots, although this difference was not statistically significant. We nonetheless detected a strong trade-off between constitutive and induced resistance across families. In contrast, the constitutive expression of trypsin inhibitors (TI), an important chemical defense trait in horsenettle, was reduced by 20% in the offspring of plants from insect-suppression plots relative to those from control plots. However, TIs were induced to an equal extent whether or not insect herbivores had been historically suppressed. Although several defense and performance traits (prickle density, TI concentration, resistance against false Colorado potato beetles and flea beetles, biomass, and seed mass) varied markedly across families, no traits exhibited significant pairwise correlations. Overall, our results indicate that, whereas the divergent responses of multiple defense traits to insect suppression led to comparatively small changes in overall constitutive resistance, they significantly reduced induced resistance against false Colorado potato beetle.
食草动物的时空变化是植物防御种内变异的主要驱动因素。然而，关于食草动物的变化如何影响组成型和诱导型抗性的平衡，人们知之甚少，而这两种抗性通常被认为是替代的防御策略。在这里，我们研究了近十年的昆虫食草动物抑制对广泛存在的草本多年生植物——刺荨麻（Solanum carolinense）的组成型和诱导型抗性的影响。我们通过在 16 个野外样地中的一半样地上对所有植物施用杀虫剂，允许重复的刺荨麻种群对食草动物的存在或不存在做出反应。在杀虫剂处理后，刺荨麻的密度迅速增加，并且这种效应至少在停止食草动物抑制后持续了 4 年。随后，我们从杀虫剂处理期间和之后不久收集的种子中培育半同胞家系，并在一个共同的花园中进行，发现昆虫抑制对诱导抗性有强烈的影响。在野外中用假褐马铃薯甲虫（Leptinotarsa juncta）进行的饲养试验，一种常见的专食性食草动物，表明多年来的食草动物抑制导致诱导抗性迅速减弱：来自昆虫抑制样地的植物的后代对甲虫几乎完全失去了诱导抗性，而来自对照样地的植物在经过实验诱导后受到的损害减少了约 70%。与对照样地相比，来自昆虫抑制样地的植物的组成型抗性也高出约 40%，尽管这种差异在统计学上并不显著。然而，我们在不同的家系中检测到组成型和诱导型抗性之间存在强烈的权衡。相比之下，在来自昆虫抑制样地的植物的后代中，胰蛋白酶抑制剂（TI）的组成型表达相对于对照样地的植物降低了 20%。然而，无论历史上是否抑制昆虫食草动物，TI 都会被诱导到相同的程度。尽管一些防御和性能特征（刺密度、TI 浓度、对假褐马铃薯甲虫和叶甲的抗性、生物量和种子质量）在不同家系中差异显著，但没有任何特征表现出显著的两两相关性。总的来说，我们的结果表明，尽管多种防御特征对昆虫抑制的不同反应导致整体组成型抗性的变化相对较小，但它们显著降低了对假褐马铃薯甲虫的诱导抗性。
