Multitrophic interactions among species are widespread and may be important for understanding the evolution of plant defenses. In previous research, we have shown that predatory wolf spiders, via their effects on insect herbivores, can alter natural selection on traits of the common monkeyflower, Mimulus guttatus. Here we explore the role of a specific defensive trait of Mimulus guttatus, leaf trichomes. We examine both how predatory spiders affect the evolution of trichomes and how trichome evolution affects multitrophic interactions. We measured selection on trichome density in different ecological contexts in the field. Seedlings from 30 paternal half-sib families were planted into replicate field plots. We removed wolf spider predators and arthropod herbivores from plots in a full factorial design. On each plant we measured trichome density on the fourth true leaf, percent damage from herbivores, plant biomass and fruit production. We then measured selection on trichome density in each plot and compared the pattern of selection between different treatments. In a concurrent field experiment we examined how evolution of trichomes affects ecological interactions. First, we performed three generations of artificial selection on trichome density in the greenhouse, with replicated lines selected for both high and low trichome density. Then, we placed plants from each of these diverged lives into field plots where we manipulated predators and herbivores. Percent damage and plant biomass were measured in each treatment replicate, allowing us to measure the strength of the predator effect. In addition, we measured the abundance of various arthropod herbivores and predatory spiders in each plot throughout the season. Thus, we can determine if plant defense evolution alters either the abundance of interacting species or the strength of ecological interactions. Together these two experiments allow us to simultaneously measure how multitrophic interactions affect selection on trichomes and the ecological consequences of trichome evolution.
We find that predatory spiders alter patterns of natural selection on several traits of Mimulus guttatus, including the density of leaf trichomes. Further, we find that trichome evolution alters the abundance of some herbivore species, while other species are unaffected by trichomes. Trichome evolution did not alter abundance of predatory spiders in our plots. However, the ecological effects of both herbivores and predators differed in magnitude on high trichome plants compared to low trichome plants. These results suggest that as plant defenses evolve in response to multitrophic interactions they in turn will alter the strength of those interactions.