Food for thought: The ecological complexity of natural selection on resources in mutualisms

Resources mediate diverse species interactions in communities, including competition, predation, parasitism, and in many cases, mutualisms. In consumer-resource species interactions, the ecological resources in flux are governed by species traits that can evolve, thus shifting the dynamics of resource supply and the dynamics of the interactions they mediate. Hence, resources can be an important mediator of eco-evolutionary feedbacks in species interactions. Understanding such feedbacks requires building a mechanistic understanding of how natural selection operates on the resources that shape both species’ population dynamics. Such a resource-focused perspective has yet to be strongly incorporated in the study of the evolutionary ecology of consumer-resource mutualisms such as plant-pollinator mutualisms mediated by the plant’s production of floral nectar. Furthermore, selection on resources such as floral nectar may vary across space and through time within a single population if the consumer species, such as a pollinator, responds to spatial and temporal variation in resource. In this body of work, I applied a resource-focused perspective to plant-pollinator mutualisms, exploring the ecological drivers of selection, and possible sources of variation in phenotypic selection, on nectar traits. In Chapter one, I built a theoretical framework of hypothesized eco-evolutionary dynamics on nectar evolution in plant-pollinator mutualisms, finding that selection for higher nectar production is strongest when ecological factors such as pollinator behavior and resource availability for nectar production reduce the frequency of plant-pollinator interactions. In the following chapters, I used Amianthium muscaetoxicum, a self-incompatible Appalachian perennial, and its interactions with beetle pollinators as an empirical model for the resource-focused perspective on the evolutionary ecology of plant-pollinator interactions. In Chapter two, I found strong individual-level consistency and high among-individual variation in nectar traits, providing a firm basis for phenotypic selection to act on nectar trait variation. In Chapter three, I measured direct and net selection on nectar traits in the Amianthium population and further found that spatial variation in nectar traits among small plant neighborhoods affected plant seed set, revealing that pollinators responded to local among-individual variation in plant nectar traits in ways that reinforced the direction of individual-scale selection. In Chapter 4, I found that the direction of selection on nectar traits remained largely consistent across high- and low-water environments, despite changes in mean fitness and water-induced plasticity in nectar trait distributions among water environments. My empirical work with A. muscaetoxicum reinforces my theoretical framework of resource evolution in consumer-resource mutualisms: nectar traits can experience strong, consistent directional selection, mediated in part by patterns of pollinator foraging behavior.