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An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

  • Plant-Animal interactions - Original Paper
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Abstract

A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.

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Acknowledgments

We are grateful to Jeffrey Conner for providing institutional support and greenhouse space at Michigan State University, Jeffrey Landgraff for help with the RNA extractions, T. Akraiko and C. Wilson for microarray processing, the Arabidopsis Biological Resource Center for supplying seeds for this experiment, and Phyllis Coley, Anurag Agrawal, Juan Bouzat and one anonymous reviewer for constructive comments on previous versions of this manuscript. This work was funded by an NSF grant (DBI 0408406) awarded to MGBB.

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Authors and Affiliations

  1. Department of Biological Sciences, Bowling Green State University, Bowling Green, OH, 43402, USA

    M. Gabriela Bidart-Bouzat

  2. Department of Plant Sciences, University of California, Davis, CA, 95616, USA

    Daniel Kliebenstein

  3. Department of Biological Sciences, Bowling Green State University, 511 Life Sciences Building, Corner of Merry and N College, Bowling Green, OH, 43403, USA

    M. Gabriela Bidart-Bouzat

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  1. M. Gabriela Bidart-Bouzat
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  2. Daniel Kliebenstein
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Correspondence to M. Gabriela Bidart-Bouzat.

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Communicated by Phyllis Coley.

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Bidart-Bouzat, M.G., Kliebenstein, D. An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167, 677–689 (2011). https://doi.org/10.1007/s00442-011-2015-z

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