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Evolutionary and chemical ecology of Verbascum thapsus reveal potential mechanisms of invasion

Date

2011

Authors

Alba, Christina, author
Hufbauer, Ruth A., advisor
Detling, James K., committee member
Bowers, M. Deane, committee member
Knapp, Alan K., committee member

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Abstract

Biological invasions, which occur when introduced species achieve pest status due to dramatic increases in performance, cause substantial environmental and economic damage. Invasion dynamics are extremely complex, varying in space and time, and as a function of the associations that form between introduced species and the biota present in the communities they invade. For plants, herbivores play a central role in shaping the outcome of introduction events. In particular, when plants are introduced to novel ranges, they often leave behind coevolved specialist herbivores (typically insects) that act to suppress populations in the native range. This can lead to increases in plant performance, for example when introduced plants evolving in communities devoid of enemies reallocate resources from defenses to growth and reproduction. Because of the important biological associations that exist between plants and insect herbivores, as well as the dramatic shifts in these associations that characterize biological invasions, this research places a particular emphasis on the evolutionary and chemical ecology of plant-insect interactions. More broadly, this research quantifies several aspects of the invasion dynamics of the introduced weed Verbascum Thapsus L. (Scrophulariaceae, common mullein). I first present data from a biogeographic comparison in which a survey of more than 50 native (European) and introduced (United States) mullein populations confirms a marked increase in population- and plant-level performance in the introduced range. I also document several ecological differences between ranges, including shifts in the abundance, identity, and degree of damage caused by insect herbivores, as well as differences in the abundance and identity of plant competitors and precipitation availability. A greenhouse experiment revealed that the increased performance observed in the field is maintained when native and introduced plants are grown from seed in a common environment; thus, a component of the performance phenotype is genetically based, or evolved. However, this increase in performance is not associated with an evolved decrease in defense investment as predicted by the evolution of increased competitive ability (EICA) hypothesis. Indeed, despite significant population-level variation in several defenses (trichomes, leaf toughness and iridoid glycosides), there is no evidence for the evolution of range-level differences in defense investment. I further explored how mullein's investment in chemical defense varies in natural populations and in relationship to damage by chewing herbivores. Based on this exploration, I developed new predictions for how changes to defense allocation may result in increased performance. Natural mullein populations exposed to ambient levels of herbivory in the introduced range exhibit significant population- and plant-level variation in iridoid glycosides. In particular, young (highly valuable) leaves are more than 6 better defended than old leaves, and likely because of this incur minimal damage from generalist herbivores. The limited ability of generalists to feed on mullein's well-defended young leaves results in negligible losses of high-quality tissue, suggesting a mechanism for mullein's increased performance in North America. Indeed, the within-plant distribution of iridoid glycosides significantly differs between native and introduced plants exposed to the different insect communities present in each range. Importantly, introduced mullein invests significantly more in the chemical defense of valuable young leaves than does native mullein, which leads to a dramatic reduction in the attack of young leaves in the introduced range relative to the native range. This optimization of within-plant investment in defense reflects the fact that introduced mullein has been released from the evolutionary dilemma posed by simultaneous attack by specialist and generalist herbivores (with specialists often being attracted to the same chemicals used to deter generalists from feeding, resulting in stabilizing selection on defense levels). In summary, this research provides evidence for a dramatic increase in the performance of introduced common mullein that is associated with several ecological differences between ranges as well as potentially adaptive shifts in mullein's chemical defense investment under natural conditions.

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Subject

chemical defense
evolution
invasion
plant-insect interactions

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