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

在自然系统中，生物体面临着与互助者和拮抗者的同时直接和间接的相互作用，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，开花植物可能面临这样的两难境地：既要吸引传粉者，又要阻止花卉的天敌，如蜜蛾。由于强盗与传粉者争夺相同的资源(例如花蜜)，植物可能特别难进化出既能有效对抗拮抗者又不能阻止共生体的防御机制。这项拟议研究的目标是确定一种无处不在但知之甚少的花卉性状--有毒花蜜--如何影响与花蜜强盗和传粉者的相互作用，以及这些同时发生的相互作用如何影响这一表型选择。有毒花蜜，或含有次生化合物的花蜜，是一种普遍存在的特征，可能会对花卉窃贼产生抗性，但可能会以吸引传粉者为代价。目前，有毒花蜜的成本和好处尚不清楚。除了抗性特征外，植物还可能通过耐性来应对拮抗者。传统上，抗性和耐受性的概念被用来指草食动物；然而，花蜜窃贼和草食动物一样，对植物的适合性有深远的影响，植物可能利用抗性和耐受作为防御机制。这项拟议的研究将把抗性和耐受性的概念扩展到更广泛的动植物相互作用中，通过研究花蜜特性，如花蜜毒性和产量，作为抵抗和耐受抢蜜的机制。这项工作的目的是了解有毒花蜜在互助者(传粉者)和拮抗者(花蜜窃贼)之间相互作用的生态作用，并确定抗性和耐受性在多大程度上调节抢蜜者对植物基因的影响。拟议的研究将在实验中操纵花蜜毒性，钩吻是一种多年生藤本植物，其花蜜中含有已知的生物碱，确定有毒花蜜对昆虫传粉者和强盗群落以及对雄性和雌性植物繁殖和后代成功的影响。此外，这项研究将操纵已知花蜜毒性变异性的棉花蜜掠夺和授粉独特型，以确定在没有花蜜掠夺的情况下，掠蜜对植物适合度的直接和间接影响，抗性和耐性的遗传变异，以及有毒花蜜的成本。这项研究结合了田间操纵实验和观察，以解决四个主要问题：1)花蜜毒性是否存在遗传变异？2)有毒花蜜是否通过增加对花蜜掠夺的抗性而使植物受益，而不会减少传粉者的吸引？3)窃取花蜜是否直接或间接地降低植物的适合性，以及植物对花蜜掠夺的抗性或耐受性是否存在差异？4)在不抢劫的情况下，有毒花蜜是否有代价？这里提出的工作新颖之处在于，它将抗性的成本和好处与一种普遍存在但知之甚少的花卉特征--有毒花蜜--结合在互惠和对立的花卉访客共同施加的选择力量的背景下进行了整合。这项工作扩展了现有的概念框架，并提供了对单个花卉Trait从吸引到防御所起作用的多样性的经验性见解。考虑更广泛的背景，其中有机体演化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.