Host plant iridoid glycosides mediate herbivore interactions with natural enemies
Many insect herbivores are dietary specialists capable of sequestering the secondary metabolites produced by their host plants. These defensive compounds have important but complex implications for tritrophic interactions between plants, herbivores, and natural enemies. The sequestration of host plant secondary metabolites defends herbivores from attack by generalist predators, but may also compromise the immune response, making insect herbivores more vulnerable to parasitism. Here, we investigate the role of plant secondary metabolites in mediating interactions between a specialist herbivore and its natural enemies. The host plants are two Penstemon species, Penstemon glaber and Penstemon virgatus, which are chemically defended by iridoid glycosides (IGs). First, we examined how Penstemon iridoid glycoside content influences the sequestration of IGs by a specialist herbivore, Euphydryas anicia. Then, we performed ant bioassays to assess how host plant species influences larval susceptibility to predators and phenoloxidase assays to assess the immunocompetence and potential vulnerability to parasitoids and pathogens. We found that the concentration of IGs sequestered by E. anicia larvae varied with host plant diet. Larvae reared on P. glaber sequestered more IGs than larvae reared on P. virgatus. Yet, ant predators found larvae unpalatable regardless of host plant diet and were also repelled by sugar solutions containing isolated IGs. However, E. anicia larvae reared on P. glaber showed higher levels of phenoloxidase activity than larvae reared on P. virgatus. Our results suggest that the sequestration of some secondary metabolites can effectively protect herbivores from predation, yet may also increase vulnerability to parasitism via decreased immunocompetence.
KeywordsTritrophic interactions Iridoid glycosides Herbivory Sequestration Lepidoptera
We thank Lauren Bradley, Hadley Hanson, and Abby Thrasher for assistance with laboratory experiments and specimen collection. We gratefully acknowledge Scott Kavanaugh for assistance with the phenoloxidase assays, and Rebecca Safran and Pei-San Tsai for use of their microplate reader. Thanks to Helen McCreery and Michael Breed for the input on rearing ant colonies and Marcus Cohen and the Cruz Lab for use of their high-definition camera during ant experiments. We also thank P. Molgaard (University of Copenhagen) for providing a standard of scutellarioside. This work was supported by grants from the Undergraduate Research Opportunity Program (to MDB), the Department of Ecology and Evolutionary Biology at the University of Colorado, Boulder (to CAK), and the National Science Foundation (DEB 1407053).
Author contribution statement
CAK and MDB conceived and designed the experiments, CAK performed the experiments, conducted the chemical analyses, and analyzed the data, and CAK and MDB wrote the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
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