Chemical Defenses Against Floral Enemies: Costs and Benefits of Toxic Nectar to Nectar Robbing, Pollination, and Plant Fitness

在自然系统中，生物同时面临着与共生菌和拮抗菌的直接和间接相互作用，然而我们对这些竞争压力在塑造表型性状进化中的相对重要性的理解仍然是初级的。例如，开花植物可能面临两难境地，既要吸引传粉者，又要阻止花的敌人，如采蜜者。因为强盗们正在与传粉者争夺同样的资源（例如花蜜），所以植物可能特别难以进化出既能有效对抗拮抗者又能阻止共生者的防御机制。这项研究的目的是确定一种普遍存在但知之甚少的花性状，即有毒花蜜，如何影响与花蜜掠夺者和传粉者的相互作用，以及这些同时的相互作用如何影响这种表型性状的选择。有毒的花蜜，或含有次级化合物的花蜜，是一种广泛存在的特性，它可能赋予对花强盗的抵抗力，但可能会损害传粉者的吸引力。目前，有毒花蜜的成本和收益尚不清楚。除了抗性性状外，植物还可以通过耐受性来对付拮抗剂。抗性和耐受性的概念传统上用于指代食草动物；然而，花蜜劫匪，像食草动物一样，对植物适应性有深远的影响，植物可能会使用抗性和耐受性作为防御机制来对抗劫匪。该研究将通过考察花蜜特性（如花蜜毒性和花蜜生产）作为对花蜜掠夺的抗性和耐受性机制的作用，将抗性和耐受性的概念扩展到更广泛的植物-动物相互作用。这项工作的目的是了解在共生者（传粉者）和拮抗者（花蜜掠夺者）之间相互作用的背景下有毒花蜜的生态作用，并确定抗性和耐受性在多大程度上介导了花蜜掠夺者对植物基因型的影响。这项研究计划将通过实验来控制常青藤（Gelsemium sempervirens）的花蜜毒性，以确定有毒花蜜对昆虫传粉者和昆虫群落的影响，以及对雌雄植物繁殖和后代成功的影响。常青藤是一种多年生藤本植物，其花蜜中含有生物碱。此外，本研究将利用已知花蜜毒性变异的G. sempervirens的掠夺花蜜和授粉基因型来确定掠夺花蜜对植物适应性、抗性和耐受性的遗传变异以及在没有掠夺花蜜的情况下有毒花蜜的成本的直接和间接影响。该研究结合了操作现场实验和观察来解决四个主要问题：1)花蜜毒性是否存在遗传变异？2)有毒花蜜是否通过增加植物对花蜜掠夺的抗性而不减少传粉者的吸引力？3)掠夺花蜜是否直接或间接地降低了植物的适合度，植物基因型对掠夺花蜜的抗性或耐受性是否存在差异？4)在没有抢劫的情况下，有毒的花蜜会有代价吗？这里提出的工作是新颖的，因为它将抗性的成本和收益与一种普遍存在但鲜为人知的花特性-有毒花蜜-在互惠和拮抗花访问者施加的联合选择力量的背景下结合起来。这项工作扩展了现有的概念框架，并提供了对单一花卉特征的多样性的经验见解，从吸引到防御。考虑有机体进化的更广泛背景是我们理解多物种相互作用如何在生态、微观进化和宏观进化尺度上塑造遗传和生物多样性的基础。

ADLER - 0211480In natural systems, organisms face simultaneous direct and indirect interactions with mutualists andantagonists, yet our understanding of the relative importance of these competing pressures inshaping the evolution of phenotypic traits is still rudimentary. For example, flowering plants mayface the dilemma of attracting pollinators while discouraging floral enemies, such as nectarrobbers. Because robbers are competing with pollinators for the same resource (e.g., nectar), it maybe particularly difficult for plants to evolve defensive mechanisms that are effective againstantagonists without also deterring mutualists. The goal of the proposed research is to determinehow a ubiquitous but poorly understood floral trait, toxic nectar, influences interactions with bothnectar robbers and pollinators, and how these simultaneous interactions shape selection on thisphenotypic trait.Toxic nectar, or nectar that contains secondary compounds, is a widespread trait that may conferresistance to floral robbers, but at a potential cost to pollinator attraction. Currently, the costs andbenefits of toxic nectar are unknown. In addition to resistance traits, plants may cope withantagonists via tolerance. The concepts of resistance and tolerance have traditionally been used inreference to herbivores; however, nectar robbers, like herbivores, have profound effects on plantfitness and plants are likely to use resistance and tolerance as defensive mechanisms againstrobbers. The proposed research will extend resistance and tolerance concepts to a wider range ofplant-animal interactions through an examination of the role of nectar traits, such as nectar toxicityand production, as mechanisms of resistance and tolerance to nectar robbing.The aim of this work is to understand the ecological role of toxic nectar within the context ofinteractions between mutualists (pollinators) and antagonists (nectar robbers), and to determine theextent to which resistance and tolerance mediate the impact of nectar robbers on plant genotypes.The research proposed will experimentally manipulate nectar toxicity in Gelsemium sempervirens,a perennial vine with documented alkaloids in its nectar, to determine the impact of toxic nectar onthe community of insect pollinators and robbers as well as on male and female plant reproductionand offspring success. In addition, this study will manipulate nectar robbing and pollination ingenotypes of G. sempervirens with known variability in nectar toxicity to determine the direct andindirect effects of nectar robbing on plant fitness, genetic variation in resistance and tolerance tonectar robbing, and costs of toxic nectar in the absence of nectar robbing. The research combinesmanipulative field experiments with observations to address four main questions: 1) Is theregenetic variation in nectar toxicity? 2) Does toxic nectar benefit plants by increasing resistance tonectar robbing without reducing pollinator attraction? 3) Does nectar robbing reduce plant fitnessdirectly or indirectly, and do plant genotypes vary in their resistance or tolerance of nectar robbing?and 4) Is there a cost of toxic nectar in the absence of robbing?The work proposed here is novel in that it integrates the costs and benefits of resistance associatedwith a ubiquitous but poorly understood floral trait, toxic nectar, in the context of joint forces ofselection exerted by both mutualistic and antagonistic floral visitors. This work extends an existingconceptual framework and provides empirical insight into the diversity of roles a single floral traitcan serve, from attraction to defense. Consideration of the broader context in which organismsevolve is fundamental to our understanding of how multiple-species interactions shape genetic andbiological diversity at ecological, microevolutionary, and macroevolutionary scales.