Summary: Chemically mediated plant–herbivore interactions contribute to the diversity of terrestrial communities and the diversification of plants and insects. While our understanding of the processes affecting community structure and evolutionary diversification has grown, few studies have investigated how trait variation shapes genetic and species diversity simultaneously in a tropical ecosystem. We investigated secondary metabolite variation among subpopulations of a single plant species, Piper kelleyi (Piperaceae), using high‐performance liquid chromatography (HPLC), to understand associations between plant phytochemistry and host‐specialized caterpillars in the genus Eois (Geometridae: Larentiinae) and associated parasitoid wasps and flies. In addition, we used a genotyping‐by‐sequencing approach to examine the genetic structure of one abundant caterpillar species, Eois encina, in relation to host phytochemical variation. We found substantive concentration differences among three major secondary metabolites, and these differences in chemistry predicted caterpillar and parasitoid community structure among host plant populations. Furthermore, E. encina populations located at high elevations were genetically different from other populations. They fed on plants containing high concentrations of prenylated benzoic acid. Thus, phytochemistry potentially shapes caterpillar and wasp community composition and geographic variation in species interactions, both of which can contribute to diversification of plants and insects.

Phytochemical diversity is comprised of two main dimensions—the average (alpha) within‐plant neighbors or the difference (beta) in the composition of chemicals between plant neighbors. Research, however, has primarily examined the consequences of phytochemical diversity on herbivore performance through a single dimension, even though diversity is multidimensional. Furthermore, the ecological role of phytochemical diversity is not well understood because each of these dimensions exhibits unique biological effects on herbivore performance. Therefore, it has been difficult to tease apart the relative importance of alpha and beta chemical diversities on plant–herbivore interactions. We experimentally manipulated alpha and beta diversities along a chemical gradient to disentangle the relative effects of these dimensions on the performance of a mobile generalist herbivore, Trichoplusia ni (Hübner), using 16 genotypes from the Solanum pennellii introgression lines. First, we found contrasting effects of alpha and beta diversities on herbivore performance. Second, when comparing diversity across and within chemical classes, herbivore performance was reduced when plant neighbors had greater diversity within chemical classes that are biologically inhibiting at higher quantities (i.e., quantitative defenses such as phenolics and acyl sugars). However, herbivore performance was enhanced when plant neighbors had higher levels of chemical classes that are biologically toxic (i.e., qualitative defenses such as alkaloids). Finally, herbivores performed better on plant dicultures compared to monocultures, and performance was positively associated with plant dicultures only when there were high levels of average alpha diversity within plant neighbors. Our results suggest T. ni generalist caterpillars do better when plant neighbors are chemically different because differences provide options for them to choose or to switch between plants to balance chemical uptake. Overall, herbivores interact with a large diversity of plant chemicals at multiple scales, and our results indicate that not all chemical diversity is equal: specific dimensions of phytochemical diversity have unique effects on the dynamics of herbivore performance.

Cultivar mixtures have been studied for decades as a means for pest suppression. The literature, however, shows a large variability in outcomes, suggesting that we are unable to create mixtures that consistently suppress insect pests and attract natural enemies. A key gap in our understanding of how cultivar mixtures influence pest control is that few studies have examined the plant traits or mechanisms by which cultivar diversity affects pests and their interactions with natural enemies. The diversity of plant chemistry in a cultivar mixture is one trait dimension that is likely influential for insect ecology because chemical traits alter how predators and herbivores forage and interact. To understand how plant chemical diversity influences herbivores and their interactions with predators, we fully crossed predator presence or absence with monocultures, bicultures, and tricultures of three chemotypes of tomato that differed in odor diversity (terpenes) or surface chemistry (acyl sugars) in a caged field experiment. We found that the direct effects of plant chemotype diversity on herbivore performance were strongest in bicultures and depended on herbivore sex, and these effects typically acted through growth rather than survival. The effects of chemotype diversity on top‐down pest suppression by natural enemies differed between classes of chemical diversity. Odor diversity (terpenes) interfered with the ability of predators to hunt effectively, whereas diversity in surface chemistry (acyl sugars) did not. Our results suggest that phytochemical diversity can contribute to pest suppression in agroecosystems, but that implementing it will require engineering cultivar mixtures using trait‐based approaches that account for the biology of the pests and natural enemies in the system.

An increasing number of ecological studies have used chemical diversity as a functionally relevant, scalable measure of phytochemical mixtures, demanding more rigorous attention to how chemical diversity is estimated. Most studies have focused on the composition of phytochemical mixtures and have largely ignored structural concerns, which may have greater importance for ecological function. Here, we explore the development of structural complexity and compositional diversity resulting from different biotic and abiotic interactions in Piper kelleyi Tepe (Piperaceae). We also describe how variation in structural complexity and compositional diversity differs between two congeners, P. kelleyi and P. reticulatum. To better interpret these results, we have developed a framework for interpreting these dimensions of chemical diversity in phytochemical mixtures. We used the tropical shrub, P. kelleyi, as a model system to examine interactions between ecological factors and dimensions of phytochemical diversity. We also compared compositional diversity and metabolic complexity in P. kelleyi and P. reticulatum using liquid chromatography and ¹H NMR, respectively, to examine trade‐offs between compositional diversity and structural complexity. A framework is provided to generate meaningful estimates of the structural complexity of phytochemical mixtures as measured by ¹H NMR. Piper is an abundant plant genus that supports diverse insect communities throughout the tropics. Subtle changes in understorey forest light were associated with increases in herbivory that directly increased compositional diversity and indirectly decreased structural complexity in P. kelleyi. This was attributed to the production of oxidation products resulting from herbivory‐driven decomposition of structurally complex defence compounds. This type of complex result would remain undetected using standard chemical ecology approaches and accounts for the detailed molecular changes that are likely to affect species interactions. Synthesis. Our quantitative framework provides a method for considering trade‐offs between structural complexity and compositional diversity and the interpretation of analytical approaches for each. This methodology will provide new theoretical insights and a more sophisticated model for examining the ecology and evolution of chemically mediated interactions.

Deciphering the ecological roles of plant secondary metabolites requires integrative studies that assess both the allocation patterns of compounds and their bioactivity in ecological interactions. Secondary metabolites have been primarily studied in leaves, but many are unique to fruits and can have numerous potential roles in interactions with both mutualists (seed dispersers) and antagonists (pathogens and predators). We described 10 alkenylphenol compounds from the plant species Piper sancti‐felicis (Piperaceae), quantified their patterns of intraplant allocation across tissues and fruit development, and examined their ecological role in fruit interactions. We found that unripe and ripe fruit pulp had the highest concentrations and diversity of alkenylphenols, followed by flowers; leaves and seeds had only a few compounds at detectable concentrations. We observed a nonlinear pattern of alkenylphenol allocation across fruit development, increasing as flowers developed into unripe pulp then decreasing as pulp ripened. This pattern is consistent with the hypothesis that alkenylphenols function to defend fruits from pre‐dispersal antagonists and are allocated based on the contribution of the tissue to the plant’s fitness, but could also be explained by non‐adaptive constraints. To assess the impacts of alkenylphenols in interactions with antagonists and mutualists, we performed fungal bioassays, field observations, and vertebrate feeding experiments. In fungal bioassays, we found that alkenylphenols had a negative effect on the growth of most fungal taxa. In field observations, nocturnal dispersers (bats) removed the majority of infructescences, and diurnal dispersers (birds) removed a larger proportion of unripe infructescences. In feeding experiments, bats exhibited an aversion to alkenylphenols, but birds did not. This observed behavior in bats, combined with our results showing a decrease in alkenylphenols during ripening, suggests that alkenylphenols in fruits represent a trade‐off (defending against pathogens but reducing disperser preference). These results provide insight into the ecological significance of a little studied class of secondary metabolites in seed dispersal and fruit defense. More generally, documenting intraplant spatiotemporal allocation patterns in angiosperms and examining mechanisms behind these patterns with ecological experiments is likely to further our understanding of the evolutionary ecology of plant chemical traits.