Resistance and susceptibility of milkweed: competition, root herbivory, and plant genetic variation

Beetles in the genus Tetraopes share a long evolutionary history with milkweeds (Asclepias spp.), feeding on roots as larvae and leaves as adults. Despite their extreme specialization on milkweed, Tetraopes require drying grass stems as oviposition sites, even though they do not consume grass. The natural history of the interaction suggests that herbivory may be likely only when milkweeds are in close proximity to grasses. Theory also predicts that two stresses on plants, competition and herbivory, may have non‐additive negative impacts on correlates of fitness. In field experiments conducted over two years, I followed the consequences of grass competition and beetle attack for herbivory, growth, and reproduction of milkweed, and reciprocal effects of milkweed on grass in common gardens. To assess the effect of milkweed traits on beetles, I conducted a quantitative genetic experiment using full‐sibling families of milkweed and measured the effects of putative resistance traits on the abundance of Tetraopes adults. Milkweeds growing next to grass were initially unaffected in growth but suffered 10% greater leaf herbivory by adult Tetraopes than did milkweeds growing alone. This effect was caused by direct attraction of beetles to grass, not by a competitive modification of milkweed's phenotype. In late summer of the first growing season, when Tetraopes naturally oviposits, I experimentally added larvae to milkweed roots with and without grass competition. Within a month, I detected an interaction between competition and herbivory: neither had an individual impact, but jointly they reduced milkweed growth. In spring of the second growing season, when Tetraopes had completed development, I again found strong evidence for a non‐additive effect of competition and herbivory together, severely reducing plant growth compared to their individual effects. Root herbivory induced a plant response that reduced the abundance of leaf‐mining flies by 40%, but only for milkweeds with grass competition. Neither competition nor herbivory affected the production of defensive latex, cardenolides, or carbon, but they interacted to affect leaf nitrogen content. Thus, although trait‐mediated indirect interactions were implicated in the effect of competition and root herbivory on leaf miner abundance, I did not uncover the mechanism. In the final harvest, beetle herbivory reduced reproductive characters (fruit production, fruit mass, aboveground biomass) by 20– 30%, whereas competition had negligible effects. The net interaction effect for grass was competitive, with a 23% reduction in grass biomass caused by milkweed in the absence of herbivory. However, the presence of beetle herbivory on milkweed roots completely alleviated the competitive effect of milkweed on grass. Thus, the associational effect of grass on milkweed resulted in milkweed suffering the non‐additive effects of competition and herbivory, whereas grass enjoyed competitive release by facilitating its neighbor's herbivore. Many traits of milkweed (e.g., growth, reproduction, and several resistance traits) showed variation among 23 full‐sibling families, indicating that competitive ability and resistance may be subject to natural selection. A multiple regression analysis on family means revealed that leaf trichome density and nitrogen content were negatively genetically correlated with abundance of Tetraopes adults, but probability of flowering and plant height were positively associated. Leaf miners were most strongly negatively affected by latex and trichomes. Thus, complex interactions among competition, root herbivory, and plant genetic variation affect the herbivore and plant community and may result in diffuse coevolution between milkweed and its herbivores. I present a general model that predicts the conditions in which plant–plant interactions result in net competition or facilitation.