Some plant species express an extraordinarily high intraspecific diversity in phytochemicals (= chemodiversity). As discussed for biodiversity, higher chemodiversity may provide better protection against environmental stress, including herbivory. However, little is known about whether the resistance of a plant individual towards herbivores is mostly governed by its own chemodiversity or by associational resistance provided by conspecific neighbours. To investigate the role of chemodiversity in plant-aphid interactions, we used the Asteraceae Tanacetum vulgare, whose individuals differ pronouncedly in the composition of leaf terpenoids, forming distinct chemotypes. Plants were set up in a field consisting of plots containing five individuals of either the same or different chemotypes. Presence of winged aphids, indicating attraction, and abundance of winged and unwinged aphids, indicating fitness, were counted weekly on each plant. During the peak abundance of aphids, leaf samples were taken from all plants for re-analyses of the terpenoid composition and quantification of terpenoid chemodiversity, calculated on an individual plant (Shannon index, Hsind, also considered as α-chemodiversity) and plot level (Hsplot, = β-chemodiversity). Aphid attraction was neither influenced by chemotype nor plot-type. The real-time odour environment may be very complex in this setting, impeding clear preferences. In contrast, the abundance was affected by both chemotype and plot-type. On average, more Uroleucon tanaceti aphids were found on plants of two of the chemotypes growing in homogenous compared to heterogenous plots, supporting the associational resistance hypothesis. For Macrosiphoniella tanacetaria aphids, the probability of presence differed between plot-types on one chemotype. Terpenoid chemodiversity expressed as a gradient revealed negative Hsplot effects on U. tanaceti, but a positive correlation of Hsind with M. tanacetaria abundance. Aphids of M. fuscoviride were not affected by any level of chemodiversity. In conclusion, this study shows that not only the chemotype and chemodiversity of individual plants but also that of conspecific neighbours can influence certain plant-herbivore interactions. These effects are highly specific with regard to the plant chemotype and differ between aphid species and their morphs (winged vs. unwinged). Furthermore, our results highlight the importance of analysing chemodiversity at different levels.

1. Some plant species express an extraordinarily high intraspecific diversity in phytochemicals (= chemodiversity). As discussed for biodiversity, higher chemodiversity may provide better protection against environmental stress, including herbivory. However, little is known about whether the resistance of a plant individual towards herbivores is mostly governed by its own chemodiversity or by associational resistance provided by conspecific neighbours. 2. To investigate the role of chemodiversity in plant-aphid interactions, we used the Asteraceae Tanacetum vulgare, whose individuals differ pronouncedly in the composition of leaf terpenoids, forming distinct chemotypes. Plants were set-up in a field consisting of 60 plots, each containing five individuals of either the same or different chemotypes. Presence of winged aphids, indicating aphid attraction, and abundance of winged and unwinged aphids, indicating fitness, were scored weekly on each plant, focusing on three commonly occurring aphid species specialised on T. vulgare. During the peak abundance of aphids, leaf samples were taken from all plants for re-analyses of the terpenoid composition and quantification of terpenoid chemodiversity, calculated on an individual plant (Shannon index, Hsind) and plot level (Hsplot). 3. Aphid attraction was neither influenced by chemotype nor plot-type. The real-time odour environment may be very complex in this setting, impeding clear preferences. In contrast, the abundance was affected by both chemotype and plot-type. On average, more Uroleucon tanaceti aphids were found on plants of two of the chemotypes growing in homogenous compared to heterogenous plots, supporting the associational resistance hypothesis. For Macrosiphoniella tanacetaria the probability of presence on a plant differed between plot-types on one chemotype. Terpenoid chemodiversity expressed as a gradient revealed negative Hsplot effects on U. tanaceti, but a positive correlation of Hsind with the abundance of M. tanacetaria. Aphids of M. fuscoviride were not affected by any level of chemodiversity. 4. Synthesis. This study shows that not only the chemotype and chemodiversity of individual plants but also that of conspecific neighbours influence plant-herbivore interactions. These effects are highly specific with regard to the plant chemotype, the aphid species as well as its morphs (winged vs. unwinged). Furthermore, our results highlight the importance of analysing chemodiversity at different levels.

Intraspecific plant chemodiversity shapes plant-environment interactions. Within species, chemotypes can be defined according to variation in dominant specialised metabolites belonging to certain classes. Different ecological functions could be assigned to these distinct chemotypes. However, the roles of other metabolic variations and the parental genotype of the chemotypes remain poorly explored. Here, we first compared the capacity of terpenoid profiles and metabolic fingerprints to distinguish five chemotypes of common tansy (Tanacetum vulgare) and depict satellite metabolic differences. Metabolic fingerprints captured higher satellite variation while preserving the ability to define chemotypes. These satellite differences might influence plant performance and interactions with the environment. Next, to characterise the influence of the maternal genotype on chemodiversity, we performed variation partitioning and generalised linear modelling. Our findings revealed that maternal genotype was a higher source of chemical variation than chemotype. Predictive metabolomics unveiled 184 markers predicting maternal genotype with 89% accuracy. These markers included, among others, phenolics, whose functions in plant-environment interactions are well established. Hence, these findings place parental genotype at the forefront of intraspecific chemodiversity. We thus recommend considering this factor when comparing the ecology of various chemotypes. Besides, the combined inclusion of inherited and satellite metabolic variation in computational models may help connecting chemodiversity and evolutionary principles.

Plants produce a great number of phytochemical compounds mediating a variety of different functions. Recently, phytochemical diversity (chemodiversity), a way which to quantify the complex phenotype formed by sets of phytochemicals, has been suggested to be important for function. However, no study has systematically examined the potential (in)direct functional importance of chemodiversity on a general level, partly due to a lack of an agreement on how to quantify this aspect of the plant phenotype. This paper has four aims: 1) We discuss how chemodiversity (deconstructed into components of richness, evenness and disparity) may quantify different aspects of the phenotype that are ecologically relevant. 2) We systematically review the literature on chemodiversity to examine methodological practices, explore ecological patterns of variability in diversity across different levels of biological organization, and investigate the functional role of this diversity in interactions between plants and other organisms. 3) We provide a framework facilitating decisions on which measure of chemodiversity is best used in different contexts. 4) We outline open questions and avenues for future research in this area. A more thorough understanding of phytochemical diversity will increase our knowledge on the functional role phytochemical compounds, and how they shape ecological interactions between plants and their environment.

Intraspecific plant chemodiversity shapes plant-environment interactions. Within species, chemotypes can be defined according to variation in dominant specialised metabolites belonging to certain classes. Different ecological functions could be assigned to these distinct chemotypes. However, the roles of other metabolic variation and the parental origin (or genotype) of the chemotypes remain poorly explored. Here, we first compared the capacity of terpenoid profiles and metabolic fingerprints to distinguish five chemotypes of common tansy (Tanacetum vulgare) and depict metabolic differences. Metabolic fingerprints captured higher variation in metabolites while preserving the ability to define chemotypes. These differences might influence plant performance and interactions with the environment. Next, to characterise the influence of the maternal origin on chemodiversity, we performed variation partitioning and generalised linear modelling. Our findings revealed that maternal origin was a higher source of chemical variation than chemotype. Predictive metabolomics unveiled 184 markers predicting maternal origin with 89% accuracy. These markers included, among others, phenolics, whose functions in plant-environment interactions are well established. Hence, these findings place parental genotype at the forefront of intraspecific chemodiversity. We recommend considering this factor when comparing the ecology of various chemotypes. Additionally, the combined inclusion of inherited variation in main terpenoids and other metabolites in computational models may help connect chemodiversity and evolutionary principles.