Intraspecific phytochemical diversity increases with productivity but has mixed effects on herbivory

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Abstract
Resources play an important role in shaping the evolution of plant defensive strategies. How resource availability influences overall phytochemical diversity within species, and how this in‐turn affects herbivore damage is not well understood. Using Monarda fistulosa, a species that produces diverse terpene compounds and distinct chemotypes (i.e. thymol or carvacrol), we addressed three questions: 1) how do phytochemical components (i.e. total concentration, Shannon diversity, and chemotypes) vary between distinct populations from two large, widely separated regions that differ in climate and productivity? 2) How do these components influence attack by different herbivore species? 3) What are the growth costs of higher phytochemical levels in different chemotypes? Seeds were collected from 12 populations spread across two regions that differ in precipitation‐driven productivity, six from a low‐productivity environment in Montana and six from a high‐productivity environment in Wisconsin, and grown in a common garden in Wisconsin. We analyzed terpene concentrations, quantified the number of herbivores and damage, and measured plant above‐ground biomass. Plants from Montana exhibited higher terpene concentrations but lower diversity, whereas those from Wisconsin displayed lower terpene concentrations but higher diversity. Plants from Wisconsin received more damage from a specialist seed predator and leaf‐chewing herbivores, although abundance of a specialist aphid was lower, compared to plants from Montana. Total terpene concentration emerged as the primary predictor of herbivore damage, although some differences were observed between region of origin and with terpene richness. Herbivores exhibited mixed responses to phytochemistry; some herbivores were negatively affected, while a specialized leaf galler responded positively. Costs of producing defenses were evident by negative correlations between plant biomass and total terpene concentration (but not chemical richness or Shannon diversity). Our study revealed that regional differences in productivity can influence the evolution of phytochemical concentration and diversity, which, in turn, affects plant damage and incurs growth‐related costs.

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