Observational evidence of herbivore-specific associational effects between neighboring conspecifics in natural, dimorphic populations of Datura wrightii.

Associational effects-in which the vulnerability of a plant to herbivores is influenced by its neighbors-have been widely implicated in mediating plant-herbivore interactions. Studies of associational effects typically focus on interspecific interactions or pest-crop dynamics. However, associational effects may also be important for species with intraspecific variation in defensive traits. In this study, we observed hundreds of Datura wrightii-which exhibits dimorphism in its trichome phenotype-from over 30 dimorphic populations across California. Our aim was to determine whether a relationship existed between the trichome phenotype of neighboring conspecifics and the likelihood of being damaged by four species of herbivorous insects. We visited plants at three timepoints to assess how these effects vary both within and between growing seasons. We hypothesized that the pattern of associational effects would provide rare morphs (i.e., focal plants that are a different morph than their neighbors) with an advantage in the form of reduced herbivory, thereby contributing to the negative frequency-dependent selection previously documented in this system. We found the best predictor of herbivory/herbivore presence on focal plants was the phenotype of the focal plant. However, we also found some important neighborhood effects. The total number of plants near a focal individual predicted the likelihood and/or magnitude of herbivory by Tupiochoris notatus, Lema daturaphila, and Manduca sexta. We also found that velvety focal plants with primarily sticky neighbors are more susceptible to infestation by Tupiochoris notatus and Lema daturaphila. This does not align with the hypothesis that associational effects at the near-neighbor scale contribute to a rare-morph advantage in this system. Overall, the results of our study show that the number and trichome-morph composition of neighboring conspecifics impact interactions between D. wrightii and insect herbivores.

Herbivore-mediated negative frequency-dependent selection underlies a trichome dimorphism in nature.

Negative frequency-dependent selection (NFDS) has been shown to maintain polymorphism in a diverse array of traits. The action of NFDS has been confirmed through modeling, experimental approaches, and genetic analyses. In this study, we investigated NFDS in the wild using morph-frequency changes spanning a 20-year period from over 30 dimorphic populations of Datura wrightii. In these populations, plants either possess glandular (sticky) or non-glandular (velvety) trichomes, and the ratio of these morphs varies substantially among populations. Our method provided evidence that NFDS, rather than drift or migration, is the primary force maintaining this dimorphism. Most populations that were initially dimorphic remained dimorphic, and the overall mean and variance in morph frequency did not change over time. Furthermore, morph-frequency differences were not related to geographic distances. Together, these results indicate that neither directional selection, drift, or migration played a substantial role in determining morph frequencies. However, as predicted by negative frequency-dependent selection, we found that the rare morph tended to increase in frequency, leading to a negative relationship between the change in the frequency of the sticky morph and its initial frequency. In addition, we found that morph-frequency change over time was significantly correlated with the damage inflicted by two herbivores: Lema daturaphila and Tupiochoris notatus. The latter is a specialist on the sticky morph and damage by this herbivore was greatest when the sticky morph was common. The reverse was true for L. daturaphila, such that damage increased with the frequency of the velvety morph. These findings suggest that these herbivores contribute to balancing selection on the observed trichome dimorphism.

Predatory lizards perceive plant-derived volatile odorants.

Many lizards are olfactory foragers and prey upon herbivorous arthropods, yet their responses to common herbivore-associated plant volatiles remain unknown. As such, their role in mediating plant indirect defenses also remains largely obscured. In this paper, we use a cotton-swab odor presentation assay to ask whether lizards respond to two arthropod-associated plant-derived volatile compounds: 2-(E)-hexenal and hexanoic acid. We studied the response of two lizard species, Sceloporus virgatusand Aspidoscelis exsanguis, because they differ substantially in their foraging behavior. We found that the actively foraging A. exsanguisresponded strongly to hexanoic acid, whereas the ambush foraging S. virgatus responded to 2-(E)-hexenal-an herbivore-associated plant volatile involved in indirect defense against herbivores. These findings indicate that S. virgatus may contribute to plant indirect defense and that a species' response to specific odorants is linked with foraging mode. Future studies can elucidate how lizards use various compounds to locate prey and how these responses impact plant-herbivore interactions.