Phytochemical diversity drives plant–insect community diversity Lora A. Richardsa,1, Lee A. Dyera, Matthew L. Foristera, Angela M. Smilanicha, Craig D. Dodsonb, Michael D. Leonardb, and Christopher S. Jeffreyb aBiology Department, University of Nevada, Reno, NV 89557; and bChemistry Department, University of Nevada, Reno, NV 89557 Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved July 20, 2015 (received for review March 11, 2015) What are the ecological causes and consequences of variation in that phytochemical diversity is maintained because it increases a phytochemical diversity within and between plant taxa? Despite plant’s likelihood of containing a potent compound or a precursor decades of natural products discovery by organic chemists and to a potent compound that is effective against a particular type of research by chemical ecologists, our understanding of phytochem- natural enemy, cumulatively creating a selective advantage against ically mediated ecological processes in natural communities has a diverse assemblage of natural enemies (2). The screening hy- been restricted to studies of either broad classes of compounds or pothesis also posits that phytochemical diversity provides effective a small number of well-characterized molecules. Until now, no combinations of compounds that work synergistically against a studies have assessed the ecological causes or consequences of particular type of natural enemy (10, 11). The coevolutionary and rigorously quantified phytochemical diversity across taxa in natural screening hypotheses are not mutually exclusive, and both rely on systems. Consequently, hypotheses that attempt to explain varia- assumptions that there are strong correlations between phyto- tion in phytochemical diversity among plants remain largely chemical diversity, plant diversity, and consumer diversity (Table untested. We use spectral data from crude plant extracts to charac- 1). These hypotheses on the causes and consequences of phyto- terize phytochemical diversity in a suite of co-occurring plants in the chemical diversity also predict that mixtures of secondary metab- tropical genus Piper (Piperaceae). In combination with 20 years of data olites within a plant species may differentially impact herbivores focused on Piper-associated insects, we find that phytochemical diver- with different diet breadths (12, 13) and thus structure plant- sity has a direct and positive effect on the diversity of herbivores but specific herbivore assemblages. Specialist herbivores that share a also reduces overall herbivore damage. Elevated chemical diversity is coevolutionary history with plants are often adapted to specific associated with more specialized assemblages of herbivores, and the compounds, and thus phytochemically diverse plants may have cascading positive effect of phytochemistry on herbivore enemies is higher richness and abundance of specialists. Generalist herbi- stronger as herbivore diet breadth narrows. These results are consis- vores that lack adaptations to particular plant taxa may be less tent with traditional hypotheses that predict positive associations be- prevalent on chemically diverse and well-defended plants; on the tween plant chemical diversity, insect herbivore diversity, and trophic other hand, extremely generalized herbivores might be well- specialization. It is clear from these results that high phytochemical adapted to a broad array of defenses and be able to persist on diversity not only enhances the diversity of plant-associated insects plants with high phytochemical diversity. but also contributes to the ecological predominance of specialized These hypotheses that address the origin and maintenance of insect herbivores. phytochemical diversity (2, 14–16) have remained largely un- tested simply because researchers have been unable to rigorously diversity | plant defense | diet breadth | tritrophic | herbivore quantify phytochemical diversity in natural systems (17). Indeed, our understanding of phytochemically mediated ecological pro- he Anthropocene has been characterized by huge losses of cesses in natural communities has been restricted to either broad Tbiodiversity caused by rapid global change, including habitat loss, fragmentation, invasive species, and climate change. Ecol- Significance ogists struggle to understand not only the consequences of diversity loss but also how to quantify ecologically relevant dimensions of diversity, including genetic, taxonomic, and functional diversity. Phytochemical diversity is a key component of functional di- Although it has been difficult to measure, phytochemical diversity versity. Challenges in quantifying phytochemical diversity have (i.e., richness and abundance of plant compounds) is a key axis of limited our understanding of the causes and consequences of functional diversity (1) that affects associated trophic levels and is variation in phytochemical diversity across plant species and likely driving other aspects of biodiversity (2–4). Variation in phy- families. Here we show that phytochemical diversity across ECOLOGY tochemical or metabolic diversity in plants, which is further down- dozens of plant species predicts herbivore diversity, herbivore stream than genomic, transcriptomic, or proteomic diversity (5, 6), specialization, phototoxicity, herbivory, and attack by natural enemies. Our approach and findings provide a framework for potentially reflects variation in response to a diversity of natural future investigations focused on uncovering chemical under- enemies, including specialist and generalist insect herbivores (7, 8). pinnings of trophic interactions at realistic ecological, geo- Furthermore, phytochemistry is one of the most relevant traits to graphic, and taxonomic scales, and have implications for the measure when determining functional roles of plants in natural and conservation of functional and taxonomic diversity. managed communities (9). Considering the importance of phytochemical diversity for Author contributions: L.A.R., L.A.D., and C.S.J. designed research; L.A.R., L.A.D., A.M.S., C.D.D., numerous natural processes, it is not surprising that a broad range and M.D.L. performed research; L.A.R., L.A.D., and C.S.J. analyzed data; and L.A.R., L.A.D., M.L.F., of ecological and evolutionary hypotheses has been proposed to and C.S.J. wrote the paper. explain their role in interactions between plants and herbivores. The authors declare no conflict of interest. From a coevolutionary perspective, the concept of an arms race This article is a PNAS Direct Submission. between plants and herbivores, yielding increasing diversity of plant Data deposition: The data reported in this paper have been deposited in caterpillars.unr. secondary compounds (3), has long been an appealing theoretical edu/lsacatold/Families.htm. framework for evolutionary biologists, and is still a theoretical 1To whom correspondence should be addressed. Email: [email protected]. cornerstone of chemical ecology (Table 1). Additionally, the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. screening hypothesis, which has received less attention, suggests 1073/pnas.1504977112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1504977112 PNAS | September 1, 2015 | vol. 112 | no. 35 | 10973–10978 Downloaded by guest on September 28, 2021 Table 1. Predicted consequences of increased phytochemical diversity based on long-standing general hypotheses or models Predictions from hypotheses linking phytochemical What support is provided by results from the diversity, plants, herbivores, and enemies Relevant path coefficients Piper system? Divergent phytochemistry hypothesis: Higher diversity All path coefficients are relevant. The overall results provide strong support for of chemical defense within a plant community is this general hypothesis, along with clear associated with increased herbivore diversity and mechanisms for increasing herbivore diversity increased specialization in diet breadth (7, 8, 28, 29). via increased specialization. Screening hypothesis: Phytochemical diversity is IA, IB Results from this study are consistent with the maintained by high taxonomic and guild diversity of screening hypothesis, with a strong effect of associated herbivores; increases in phytochemical phytochemical diversity reducing herbivory diversity cause reduced total herbivory (2). and increasing toxicity. Bottom-up cascade: Increases in plant diversity (including IA, IB, IVA, IVB Results provide good support for the bottom-up functional or phytochemical diversity) cause greater hypothesis and that phytochemical diversity diversity at upper trophic levels through direct and (rather than toxicity) increases rates of indirect mechanisms (45). parasitoid success. Hypothesized mode of action: Phytochemical diversity IC, ID, IE Although further support for this hypothesis of phototoxic compounds (associated with downfield will require experimental work, the indirect NMR spectra) reduces the diversity of associated evidence for this hypothesis is clear. herbivores as well as overall herbivory (25, 26, 46, 47). Extreme diet breadth hypothesis: Greater diversity of IIA, IIB, IIC, IID Results provide moderate support for this chemical defense is associated with more restricted hypothesis. Path coefficients were not large diets for specialist herbivores and broader diets for for these specific associations, but local diet generalist herbivores (19, 20). breadth is a complex variable affected