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Origin and maintenance of chemical diversity in a species-rich tropical tree lineage


Plant secondary metabolites play important ecological and evolutionary roles, most notably in the deterrence of natural enemies. The classical theory explaining the evolution of plant chemical diversity is that new defences arise through a pairwise co-evolutionary arms race between plants and their specialized natural enemies. However, plant species are bombarded by dozens of different herbivore taxa from disparate phylogenetic lineages that span a wide range of feeding strategies and have distinctive physiological constraints that interact differently with particular plant metabolites. How do plant defence chemicals evolve under such multiple and potentially contrasting selective pressures imposed by diverse herbivore communities? To tackle this question, we exhaustively characterized the chemical diversity and insect herbivore fauna from 31 sympatric species of Amazonian Protieae (Burseraceae) trees. Using a combination of phylogenetic, metabolomic and statistical learning tools, we show that secondary metabolites that were associated with repelling herbivores (1) were more frequent across the Protieae phylogeny and (2) were found in average higher abundance than other compounds. Our findings suggest that generalist herbivores can play an important role in shaping plant chemical diversity and support the hypothesis that chemical diversity can also arise from the cumulative outcome of multiple diffuse interactions.

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Fig. 1: Chemical diversity and investment of 31 Protieae species arranged by their phylogenetic relationships.
Fig. 2: Protieae trees and their associated herbivores.
Fig. 3: Effect of plant secondary chemistry on insect herbivores.
Fig. 4: Association between plant–herbivore interactions and HAM phylogenetic frequency, plant chemical investment and metabolite abundance.

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We thank R. Marquis, M. Metz, N. Whiteman and C. Marshall for comments on the manuscript; G. Takeoka (USDA, Albany), P. Oboyski (Essig Museum), L. Smith (Evolutionary Genetics Laboratory at the University of California, Berkeley) and N. Tsutsui for advice, laboratory space and sample archiving; E. Hendrickson, B. Ho, C. Chong, S. Visvanathan, E. Suh and S. Sharma for help with the laboratory work; and D. Vásquez and C. Villacorta for field assistance. We also thank C. Rivera for help with research permits at the Allpahuayo-Mishana National Reserve. Funding for this project was provided by the NSF DEB (award number 1254214).

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D.S., J.L., P.dV., P.V.A.F. and I.M. contributed to the design, analysis and preparation of the manuscript. I.M., M.V.P. and J.M.A.Z. coordinated the fieldwork and data collection. D.S. and P.V.A.F. wrote the article with contributions from all co-authors.

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Correspondence to Diego Salazar.

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Supplementary Methods, Supplementary Figures 1–11, Supplementary Table 2, Supplementary References

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Supplementary Table 1

Herbivore samples supplementary information. Includes the Essig Museum of Entomology, University of California, Berkeley, Essig Museum and Genbank accession numbers

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Salazar, D., Lokvam, J., Mesones, I. et al. Origin and maintenance of chemical diversity in a species-rich tropical tree lineage. Nat Ecol Evol 2, 983–990 (2018).

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