Ever since the first plant secondary metabolites (PSMs) were isolated and identified, questions about their ecological functions and diversity have been raised. Recent advances in analytical chemistry and complex data computation, as well as progress in chemical ecology from mechanistic to functional and evolutionary questions, open a new box of hypotheses. Addressing these hypotheses includes the measurement of complex traits, such as chemodiversity, in a context-dependent manner and allows for a deeper understanding of the multifunctionality and functional redundancy of PSMs. Here we review a hypothesis framework that addresses PSM diversity on multiple ecological levels (α, β, and γ chemodiversity), its variation in space and time, and the potential agents of natural selection. We use the concept of chemical information transfer as mediator of antagonistic and mutualistic interaction to interpret functional and microevolutionary studies and create a hypothesis framework for understanding chemodiversity as a factor driving ecological processes.

Highlights d Volatile organic compounds are vehicles of information transfer between plants d Herbivory selects for a plant's abilities to share information with neighbors d Convergence on common volatile signal characterizes information-sharing phenotypes d Plants can serve as a model to understand the evolution of communication

Summary1. Due to geographically variable species interactions, plants may become locally adapted to their sympatric herbivores and pollinators. However, adaptation to the abiotic environment may significantly affect plant interactions with herbivores and pollinators. Local adaptation to the abiotic environment may constrain local adaptation to herbivores and pollinators under contrasting selection pressures, resulting in trade-offs in local adaptation. 2. We studied local adaptation of a perennial herb, Vincetoxicum hirundinaria, in a reciprocal transplant experiment among four populations and measured plant fitness, pollination success and resistance to two specialist herbivores. We also estimated local adaptation of these two herbivores and generalist pollinators to their sympatric plant populations. Local adaptation was compared with within-population genetic variation, genetic and geographical divergence, and with divergence in terms of population size, environmental conditions and plant secondary chemistry. We further compared local adaptation to the environment, to local adaptation to herbivores and pollinators to detect possible trade-offs in local adaptation. 3. The existence and degree of local adaptation varied among the plant populations. Plants from two populations were locally adapted to their sympatric leaf herbivores and plants from two populations were locally adapted to their abiotic environment. Herbivores from one population were locally adapted to their sympatric plant population. Local adaptation of V. hirundinaria to the seed predator increased with increasing among-population divergence in precipitation and temperature. Local adaptation to the seed predator and the environment increased with increasing population genetic variation. Local adaptation of V. hirundinaria in fitness and in herbivore resistance also correlated positively, suggesting lack of trade-offs in local adaptation. 4. Synthesis. These results demonstrate that species interactions can lead to a mosaic of locally adapted plant, herbivore and pollinator populations. In addition to natural enemies, genetic variation, the abiotic environment and mutualistic interactions contribute to the evolution of local adaptation in long-lived plants. These results provide new insights into the patterns and causes of variation in local adaptation and are among the first to demonstrate that conflicting selection pressures within a population do not constrain local adaptation in multiple traits.

The quality and outcome of organismal interactions are not only a function of genotypic composition of the interacting species, but also the surrounding environment. Both the strength and direction of natural selection on interacting populations vary with the community context, which itself is changed by these interactions. Here, we test for the role of interacting evolutionary and ecological processes in plant-herbivore interactions during early community succession in the tall goldenrod, Solidago altissima. We use surveys in a large-scale field experiment with repeated plots representing 6 years of early oldfield succession and reciprocal transplant common garden experiments to test for the relative importance of rapid evolution (genetic) and environmental changes (soil quality) in affecting mean plant resistance and growth phenotypes during community succession. While plant growth varied strongly with soil quality over the first 5 years of agricultural abandonment, plant secondary metabolism, and herbivore resistance varied minimally with the soil environment. Instead, mean composition and abundance of plant secondary compound bouquets differed between S. altissima plants from populations collected in communities in the first ("early") and sixth ("intermediate") years of oldfield succession, which was reflected in the feeding preference of the specialist herbivore, Trirhabda virgata, for early succession lines. Moreover, this preference was most pronounced on poorer quality, early succession soils. Overall, our data demonstrate that plant quality varies for insect herbivores during the course of early succession and this change is a combination of altered genotypic composition of the population and phenotypic plasticity in different soil environments.

Because inbreeding is common in natural populations of plants and their herbivores, herbivore-induced selection on plants, and vice versa, may be significantly modified by inbreeding and inbreeding depression. In a feeding assay with inbred and outbred lines of both the perennial herb, Vincetoxicum hirundinaria, and its specialist herbivore, Abrostola asclepiadis, we discovered that plant inbreeding increased inbreeding depression in herbivore performance in some populations. The effect of inbreeding on plant resistance varied among plant and herbivore populations. The among-population variation is likely to be driven by variation in plant secondary compounds across populations. In addition, inbreeding depression in plant resistance was substantial when herbivores were outbred, but diminished when herbivores were inbred. These findings demonstrate that in plant-herbivore interactions expression of inbreeding depression can depend on the level of inbreeding of the interacting species. Furthermore, our results suggest that when herbivores are inbred, herbivore-induced selection against self-fertilisation in plants may diminish.