Gut microbes may facilitate insect herbivory of chemically defended plants

Abstract

The majority of insect species consume plants, many of which produce chemical toxins that defend their tissues from attack. How then are herbivorous insects able to develop on a potentially poisonous diet? While numerous studies have focused on the biochemical counter-adaptations to plant toxins rooted in the insect genome, a separate body of research has recently emphasized the role of microbial symbionts, particularly those inhabiting the gut, in plant–insect interactions. Here we outline the “gut microbial facilitation hypothesis,” which proposes that variation among herbivores in their ability to consume chemically defended plants can be due, in part, to variation in their associated microbial communities. More specifically, different microbes may be differentially able to detoxify compounds toxic to the insect, or be differentially resistant to the potential antimicrobial effects of some compounds. Studies directly addressing this hypothesis are relatively few, but microbe–plant allelochemical interactions have been frequently documented from non-insect systems—such as soil and the human gut—and thus illustrate their potential importance for insect herbivory. We discuss the implications of this hypothesis for insect diversification and coevolution with plants; for example, evolutionary transitions to host plant groups with novel allelochemicals could be initiated by heritable changes to the insect microbiome. Furthermore, the ecological implications extend beyond the plant and insect herbivore to higher trophic levels. Although the hidden nature of microbes and plant allelochemicals make their interactions difficult to detect, recent molecular and experimental techniques should enable research on this neglected, but likely important, aspect of insect-plant biology.

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Acknowledgments

We thank Noah Fierer, Stacey Smith, and members of the Bowers lab for their helpful feedback on earlier versions of the manuscript. We also acknowledge insightful comments from two anonymous reviewers that significantly improved this review. T. J. H. is supported by a Graduate Research Fellowship from the National Science Foundation.

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The authors declare that they have no conflict of interest.

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Correspondence to Tobin J. Hammer.

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Highlighted Student Paper: This article is an original contribution to the fields of chemical ecology, entomology, symbiosis, and the study of plant-herbivore coevolution. It is hoped that the ideas, conceptual framework, and methodological directions presented here will further catalyze research in what is potentially fertile ground for new discoveries in insect-plant biology.

Communicated by Corné Pieterse.

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Hammer, T.J., Bowers, M.D. Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179, 1–14 (2015). https://doi.org/10.1007/s00442-015-3327-1

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Keywords

  • Microbiome
  • Secondary metabolites
  • Detoxification
  • Diversification
  • Symbiosis