Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Abstract

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 1.

    Lokvam, J. & Kursar, T. A. Divergence in structure and activity of phenolic defenses in young leaves of two co-occurring Inga species. J. Chem. Ecol. 31, 2563–2580 (2005).

    CAS  Article  Google Scholar 

  2. 2.

    Ehrlich, P. & Raven, P. H. Butterflies and plants: a study in coevolution. Evolution 18, 586–608 (1964).

    Article  Google Scholar 

  3. 3.

    Speed, M. P., Fenton, A., Jones, M. G., Ruxton, G. D. & Brockhurst, M. A. Coevolution can explain defensive secondary metabolite diversity in plants. New Phytol. 208, 1251–1263 (2015).

    Article  Google Scholar 

  4. 4.

    Berenbaum, M. R. Chemical mediation of coevolution: phylogenetic evidence for Apiaceae and associates. Ann. Mo. Bot. Gard. 88, 45–59 (2001).

    Article  Google Scholar 

  5. 5.

    Edger, P. P. et al. The butterfly plant arms-race escalated by gene and genome duplications. Proc. Natl Acad. Sci. USA 112, 8362–8366 (2015).

    CAS  Article  Google Scholar 

  6. 6.

    Alejo-Armijo, A. et al. Antimicrobial and antibiofilm activities of procyanidins extracted from laurel wood against a selection of foodborne microorganisms. Int. J. Food Sci. Technol. 52, 679–686 (2017).

    CAS  Article  Google Scholar 

  7. 7.

    Wise, M. J. & Rausher, M. D. Evolution of resistance to a multiple-herbivore community: genetic correlations, diffuse coevolution, and constraints on the plant’s response to selection. Evolution 67, 1767–1779 (2013).

    Article  Google Scholar 

  8. 8.

    Volf, M. et al. Community structure of insect herbivores is driven by conservatism, escalation and divergence of defensive traits in Ficus. Ecol. Lett. 21, 83–92 (2018).

    Article  Google Scholar 

  9. 9.

    Lankau, R. A. Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol. 175, 176–184 (2007).

    Article  Google Scholar 

  10. 10.

    Volf, M., Hrcek, J., Julkunen-Tiitto, R. & Novotny, V. To each its own: differential response of specialist and generalist herbivores to plant defence in willows. J. Anim. Ecol. 84, 1123–1132 (2015).

    Article  Google Scholar 

  11. 11.

    Janzen, D. H. When is it coevolution? Evolution 34, 611–612 (1980).

    Article  Google Scholar 

  12. 12.

    Iwao, K. & Rausher, M. D. Evolution of plant resistance to multiple herbivores: quantifying diffuse coevolution. Am. Nat. 149, 316–335 (1997).

    Article  Google Scholar 

  13. 13.

    Futuyma, D. J. & Agrawal, A. A. Macroevolution and the biological diversity of plants and herbivores. Proc. Natl Acad. Sci. USA 106, 18054–18061 (2009).

    CAS  Article  Google Scholar 

  14. 14.

    Opitz, S. E. W. & Müller, C. Plant chemistry and insect sequestration. Chemoecology 19, 117–154 (2009).

    CAS  Article  Google Scholar 

  15. 15.

    Reinecke, A. & Hilker, M. in Annual Plant Reviews: Insect–Plant Interactions Vol. 47 (eds Voelckel, C. & Jander, G.) 115–153 (John Wiley & Sons, Chichester, 2014).

  16. 16.

    Johnson, M. T. J., Ives, A. R., Ahern, J. & Salminen, J. P. Macroevolution of plant defenses against herbivores in the evening primroses. New Phytol. 203, 267–279 (2014).

    CAS  Article  Google Scholar 

  17. 17.

    Kursar, T. A. et al. The evolution of antiherbivore defenses and their contribution to species coexistence in the tropical tree genus Inga. Proc. Natl Acad. Sci. USA 106, 18073–18078 (2009).

    CAS  Article  Google Scholar 

  18. 18.

    Richards, L. A. et al. Phytochemical diversity drives plant–insect community diversity. Proc. Natl Acad. Sci. USA 112, 10973–10978 (2015).

    CAS  Article  Google Scholar 

  19. 19.

    Basset, Y. Diversity and abundance of insect herbivores foraging on seedlings in a rainforest in Guyana.Ecol. Entomol. 24, 245–259 (1999).

    Article  Google Scholar 

  20. 20.

    Dyer, L. A. et al. Host specificity of Lepidoptera in tropical and temperate forests. Nature 448, 696–699 (2007).

    CAS  Article  Google Scholar 

  21. 21.

    Novotny, V. et al. Low beta diversity of herbivorous insects in tropical forests. Nature 448, 692–695 (2007).

    CAS  Article  Google Scholar 

  22. 22.

    Jones, C. G. & Lawton, J. H. Plant chemistry and insect species richness of British umbellifers. J. Anim. Ecol. 60, 767–777 (1991).

    Article  Google Scholar 

  23. 23.

    Tibshirani, R. Regression shrinkage and selection via the lasso.J. R. Stat. Soc. B Stat. Methodol. 58, 267–288 (1996).

    Google Scholar 

  24. 24.

    Rasmann, S., Bennett, A., Biere, A., Karley, A. & Guerrieri, E.Root symbionts: powerful drivers of plant above- and belowground indirect defenses. Insect Sci. 24, 947–960 (2017).

    CAS  Article  Google Scholar 

  25. 25.

    Langenheim, J. H. Plant Resins: Chemistry, Evolution, Ecology, and Ethnobotany (Timber Press, Portland, 2003).

    Google Scholar 

  26. 26.

    Andrew, R. L., Peakall, R., Wallis, I. R. & Foley, W. J. Spatial distribution of defense chemicals and markers and the maintenance of chemical variation. Ecology 88, 716–728 (2007).

    Article  Google Scholar 

  27. 27.

    Firn, R. D. & Jones, C. G. in Phytochemical Diversity and Redundancy in Ecological Interactions (eds Romeo, J. T., Saunders, J. A. & Barbosa, P.) 295–312 (Springer, New York, 1996).

  28. 28.

    Coley, P. D., Endara, M.-J. & Kursar, T. A. Consequences of interspecific variation in defenses and herbivore host choice for the ecology and evolution of Inga, a speciose rainforest tree. Oecologia https://doi.org/10.1007/s00442-018-4080-z (2018).

  29. 29.

    Fine, P. V. A., Daly, D. C., Villa, F. G., Mesones, I. & Cameron, K. M. The contribution of edaphic heterogeneity to the evolution and diversity of Burseraceae trees in the western Amazon. Evolution 59, 1464–1478 (2005).

    PubMed  Google Scholar 

  30. 30.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R.DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates.Mol. Mar. Biol. Biotechnol. 3, 294–299 (1994).

    CAS  PubMed  Google Scholar 

  31. 31.

    Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H. & Hallwachs, W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl Acad. Sci. USA 101, 14812–14817 (2004).

    CAS  Article  Google Scholar 

  32. 32.

    Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

    CAS  Article  Google Scholar 

  33. 33.

    Schliep, K. P. phangorn: phylogenetic analysis in R. Bioinformatics 27, 592–593 (2011).

    CAS  Article  Google Scholar 

  34. 34.

    Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003).

    CAS  Article  Google Scholar 

  35. 35.

    Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In 2010 Gateway Computing Environments Workshop (GCE) 1–8 (IEEE, 2010).

  36. 36.

    Miller, M. A., Pfeiffer, W. & Schwartz, T. Extreme digital discovery. In Proc. 2011 TeraGrid Conference 1–8 (ACM, 2011).

  37. 37.

    Salazar, D., Jaramillo, A. & Marquis, R. J. The impact of plant chemical diversity on plant–herbivore interactions at the community level. Oecologia 181, 1199–1208 (2016).

    Article  Google Scholar 

  38. 38.

    Salazar, D., Jaramillo, A. & Marquis, R. J. Chemical similarity and local community assembly in the species rich tropical genus Piper. Ecology 97, 3176–3183 (2016).

    Article  Google Scholar 

  39. 39.

    Lokvam, J. & Fine, P. V. A. An oxidized squalene derivative from Protium subserratum Engl. (Engl.) growing in Peru. Molecules 17, 7451–7457 (2012).

    CAS  Article  Google Scholar 

  40. 40.

    Lokvam, J., Metz, M. R., Takeoka, G. R., Nguyen, L. & Fine, P. V. A. Habitat-specific divergence of procyanidins in Protium subserratum (Burseraceae). Chemoecology 25, 293–302 (2015).

    CAS  Article  Google Scholar 

  41. 41.

    Davies, T. The new automated mass spectrometry deconvolution and identification system (AMDIS). Spectrosc. Eur. 10, 24–27 (1998).

    CAS  Google Scholar 

  42. 42.

    The NIST Mass Spectral Search Program for the NIST/EPA/NIH Mass Spectral Library (National Institute of Standards and Technology, Gaithersburg, 2017).

  43. 43.

    Horai, H. et al. MassBank: a public repository for sharing mass spectral data for life sciences. J. Mass Spectrom. 45, 703–714 (2010).

    CAS  Article  Google Scholar 

  44. 44.

    Stein, S. E. An integrated method for spectrum extraction and compound identification from gas chromatography/mass spectrometry data. J. Am. Soc. Mass Spectrom. 10, 770–781 (1999).

    CAS  Article  Google Scholar 

  45. 45.

    Suzuki, R. & Shimodaira, H. Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540–1542 (2006).

    CAS  Article  Google Scholar 

  46. 46.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2015).

  47. 47.

    Pluskal, T., Castillo, S., Villar-Briones, A. & Orešič, M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11, 395 (2010).

    Article  Google Scholar 

  48. 48.

    Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).

    CAS  Article  Google Scholar 

  49. 49.

    Blomberg, S. P., Garland, T. & Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57, 717–745 (2003).

    Article  Google Scholar 

  50. 50.

    Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).

    Article  Google Scholar 

  51. 51.

    Dray, S. & Dufour, A.-B. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).

    Article  Google Scholar 

  52. 52.

    Friedman, J., Hastie, T. & Tibshirani, R.Regularization paths for generalized linear models via coordinate descent. J. Stat. Softw. 33, 1–22 (2010).

    Article  Google Scholar 

  53. 53.

    Meiners, T. Chemical ecology and evolution of plant–insect interactions: a multitrophic perspective.Curr. Opin. Insect Sci. 8, 22–28 2015).

    Article  Google Scholar 

  54. 54.

    Wäschke, N., Meiners, T. & Rostás, M. in Chemical Ecology of Insect Parasitoids (eds Wajnberg, E. & Colazza, S.) 37–63 (John Wiley & Sons, Chichester, 2013).

  55. 55.

    Erb, M. & Robert, C. A. M. Sequestration of plant secondary metabolites by insect herbivores: molecular mechanisms and ecological consequences. Curr. Opin. Insect Sci. 14, 8–11 (2016).

    Article  Google Scholar 

  56. 56.

    Heckel, D. G. in Annual Plant Reviews: Insect–Plant Interactions Vol. 47 (eds Voelckel, C. & Jander, G.) 77–114 (John Wiley & Sons, Chichester, 2014).

  57. 57.

    Pentzold, S., Zagrobelny, M., Roelsgaard, P. S., Møller, B. L. & Bak, S. The multiple strategies of an insect herbivore to overcome plant cyanogenic glucoside defence. PLoS ONE 9, e91337 (2014).

    Article  Google Scholar 

  58. 58.

    Jones, C. G., Firn, R. D. & Malcolm, S. B. On the evolution of plant secondary chemical diversity [and discussion]. Phil. Trans. R. Soc. Lond. B 333, 273–280 (1991).

    Article  Google Scholar 

Download references

Acknowledgements

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).

Author information

Affiliations

Authors

Contributions

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.

Corresponding author

Correspondence to Diego Salazar.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

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

Reporting Summary

Supplementary Table 1

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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). https://doi.org/10.1038/s41559-018-0552-0

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing