An official website of the United States government
{"Abstract":["Original data and R code to accompany the manuscript: "Interaction diversity explains the maintenance of phytochemical diversity" by Susan R. Whitehead, Ethan Bass, Alexsandra Corrigan, André Kessler, and Katja Poveda Accepted for publication in Ecology Letters<\/p>\n\nAbstract: The production of complex mixtures of secondary metabolites is a ubiquitous feature of plants. Several evolutionary hypotheses seek to explain how phytochemical diversity is maintained, including the synergy hypothesis, the interaction diversity hypothesis, and the screening hypothesis. We experimentally tested predictions derived from these hypotheses by manipulating the richness and structural diversity of phenolic metabolites in the diets of eight plant consumers. Across 3940 total bioassays, there was clear support for the interaction diversity hypothesis over the synergy or screening hypotheses. The number of consumers affected by a particular phenolic composition increased with increasing richness and structural diversity of compounds. Furthermore, the bioactivity of phenolics was consumer-specific. All compounds tested reduced the performance of at least one consumer, but no compounds affected all consumers. These results show how phytochemical diversity may be maintained in nature by a complex selective landscape exerted by diverse communities of plant consumers.<\/p>\n\nhttps://github.com/WhiteheadLabVT/Phytochemical-Diversity-Experiment/releases/tag/v1.0.0<\/p>"]}
more »
« less
Interaction diversity explains the maintenance of phytochemical diversity
Abstract The production of complex mixtures of secondary metabolites is a ubiquitous feature of plants. Several evolutionary hypotheses seek to explain how phytochemical diversity is maintained, including the synergy hypothesis, the interaction diversity hypothesis, and the screening hypothesis. We experimentally tested a set of predictions derived from these hypotheses by manipulating the richness and structural diversity of phenolic metabolites in the diets of eight plant consumers. Across 3940 total bioassays, there was clear support for the interaction diversity hypothesis over the synergy or screening hypotheses. The number of consumers affected by a particular phenolic composition increased with increasing richness and structural diversity of compounds. Furthermore, the bioactivity of phenolics was consumer‐specific. All compounds tested reduced the performance of at least one consumer, but no compounds affected all consumers. These results show how phytochemical diversity may be maintained in nature by a complex selective landscape exerted by diverse communities of plant consumers.
more »
« less
- Award ID(s):
- 1856776
- PAR ID:
- 10452677
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Ecology Letters
- Volume:
- 24
- Issue:
- 6
- ISSN:
- 1461-023X
- Format(s):
- Medium: X Size: p. 1205-1214
- Size(s):
- p. 1205-1214
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract A central goal in ecology is to understand the mechanisms by which biological diversity is maintained. The diversity of plant chemical defences and the strategies by which they are deployed in nature may influence biological diversity. Trees in neotropical forests are subject to relatively high herbivore pressure. Such consistent pressure is thought to select for constitutive, non‐flexible defence‐related phytochemistry with limited capacity for inducible phytochemical responses. However, this has not been explored for volatile organic compounds (VOCs) that have a relatively low ratio of production costs to ecological benefits. To test this, I sampled VOCs emitted from canopy leaves of 10 phylogenetically diverse tree species (3 Magnoliids and 7 Rosids) in the Peruvian Amazon before and after induction with the phytohormone methyl jasmonate (MeJA). There was no phylogenetic signal in induction or magnitude of MeJA‐induced VOC emissions from intact leaves: all trees induced VOC profiles dominated by β‐ocimene, linalool, and α‐farnesene of varying ratios. Moreover, overall inducibility of VOCs from intact leaves was unrelated to phytochemical diversity or richness. In contrast, experimentally wounded leaves showed considerable phylogeny‐based and MeJA‐independent variation the richness and diversity of constitutive wound‐emitted VOCs. Moreover, VOC inducibility from wounded leaves correlated negatively with phytochemical richness and diversity, potentially indicating a tradeoff in constitutive and inducible defence strategies for non‐volatile specialised metabolites but not for inducible VOCs. Importantly, there was no correlation between any chemical profile and either natural herbivory or leaf toughness. The coexistence of multiple phytochemical strategies in a hyper‐diverse forest has broad implications for competitive and multitrophic interactions, and the evolutionary forces that maintain the exceptional plant biodiversity in neotropical forests.more » « less
-
Interactions between plants and leaf herbivores have long been implicated as the major driver of plant secondary metabolite diversity. However, other plant-animal interactions, such as those between fruits and frugivores, may also be involved in phytochemical diversification. Using 12 species of Piper , we conducted untargeted metabolomics and molecular networking with extracts of fruits and leaves. We evaluated organ-specific secondary metabolite composition and compared multiple dimensions of phytochemical diversity across organs, including richness, structural complexity, and variability across samples at multiple scales within and across species. Plant organ identity, species identity, and the interaction between the two all significantly influenced secondary metabolite composition. Leaves and fruit shared a majority of compounds, but fruits contained more unique compounds and had higher total estimated chemical richness. While the relative levels of chemical richness and structural complexity across organs varied substantially across species, fruit diversity exceeded leaf diversity in more species than the reverse. Furthermore, the variance in chemical composition across samples was higher for fruits than leaves. By documenting a broad pattern of high phytochemical diversity in fruits relative to leaves, this study lays groundwork for incorporating fruit into a comprehensive and integrative understanding of the ecological and evolutionary factors shaping secondary metabolite composition at the whole-plant level.more » « less
-
Abstract Species richness in tropical forests is correlated with other dimensions of diversity, including the diversity of plant–herbivore interactions and the phytochemical diversity that influences those interactions. Understanding the complexity of plant chemistry and the importance of phytochemical diversity for plant–insect interactions and overall forest richness has been enhanced significantly by the application of metabolomics to natural systems. The present work used proton nuclear magnetic resonance spectroscopy (1H‐NMR) profiling of crude leaf extracts to study phytochemical similarity and diversity amongPiperplants growing naturally in the Atlantic Rainforest of Brazil. Spectral profile similarity and chemical diversity were quantified to examine the relationship between metrics of phytochemical diversity, specialist and generalist herbivory, and understory plant richness. Herbivory increased with understory species richness, while generalist herbivory increased and specialist herbivory decreased with the diversity ofPiperleaf material available. Specialist herbivory increased when conspecific host plants were more spectroscopically dissimilar. Spectral similarity was lower among individuals of common species, and they were also more spectrally diverse, indicating phytochemical diversity is beneficial to plants. Canopy openness and soil nutrients also influenced chemistry and herbivory. The complex relationships uncovered in this study add information to our growing understanding of the importance of phytochemical diversity for plant–insect interactions and tropical plant species richness.more » « less
-
The tree diversity-productivity relationship is key to effective forest restoration and management; however, it remains unclear what role foliar chemical diversity and interactions between trees and their enemies play in driving this relationship. Trees produce chemical metabolites in their leaves that impact herbivory and pathogen infection. If trees alter the diversity of metabolites they produce when grown in more diverse communities, this could impact interactions with herbivores and pathogens. Ultimately, these tropic interactions with plant enemies, mediated by chemical diversity, could be important drivers of diversity-productivity relationships. Using a large-scale tree diversity experiment, we used a focal tree sampling design from 14 species across a gradient of tree species richness to assess the role of foliar chemicals and trophic interactions in the diversity-productivity relationship. We used untargeted metabolomics to measure foliar phytochemical diversity, monitored tree-enemy interactions, including foliar fungal pathogens, caterpillar communities, and deer browsing, and modelled their relationship to tree growth using path analysis. We unraveled significant evidence for top-down mediation of the diversity-productivity relationship driven primarily by herbivores rather than foliar pathogens, and contrasting effects of foliar chemical diversity on different enemy types. Individual trees growing in more diverse communities had higher phytochemical diversity and higher caterpillar richness, but lower leaf fungal pathogen richness. Leaf phytochemical diversity was positively associated with caterpillar richness and fungal pathogen richness, but negatively associated with browsing by white-tailed deer (Odocoileus virginianus). Path analysis revealed that phytochemical diversity, caterpillar richness, insect damage, and deer damage – but not foliar pathogens – all mediated positive indirect effects of tree richness on tree growth rate. Synthesis: We highlight the significant mediation of diversity-productivity relationships via contrasting effects of phytochemical diversity on plant-enemy interactions. Ultimately, our study underscores the importance of incorporating trophic interactions into biodiversity-ecosystem function studies.more » « less
