Plant defense resistance in natural enemies of a specialist insect herbivore

Authors: ZHANG, XI - University Of Bern; VAN DOAN, CONG - University Of Bern; ARCE, CARLA - University Of Bern; HU, LINGFEI - University Of Bern; GRUENIG, SANDRA - University Of Bern; PARISOD, CHRISTIAN - University Of Bern; Hibbard, Bruce; HERVE, MAXIME - University Of Rennes, France; Nielson, Chad; ROBERT, CHRISTELLE - University Of Bern; MACHADO, RICARDO - University Of Bern; ERB, MATHIAS - University Of Bern

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/30/2019
Publication Date: 11/12/2019
Citation: Zhang, X., Van Doan, C., Arce, C.C., Hu, L., Gruenig, S., Parisod, C., Hibbard, B.E., Herve, M.R., Nielson, C.N., Robert, C.A., Machado, R.A., Erb, M. 2019. Plant defense resistance in natural enemies of a specialist insect herbivore. Proceedings of the National Academy of Sciences. 116(46):23174-23181. https://doi.org/10.1073/pnas.1912599116.
DOI: https://doi.org/10.1073/pnas.1912599116

Interpretive Summary: By accumulating plant toxins, herbivores can gain protection against their enemies. Whether herbivore natural enemies can evolve resistance to this form of self-defense is unknown. We show that nematodes from the native range of the western corn rootworm are more resistant to plant toxins accumulated in the rootworm and are more infective towards the rootworm than nematodes from other parts of the world. Exposure of nematodes susceptible to toxins in the western corn rootworm results in the rapid evolution of toxin resistance and infectivity of the nematode to rootworms. Thus, plant defense metabolites can drive the evolution of toxin resistance in herbivore natural enemies. This finding extends the biochemical co-evolutionary arms race between plants and herbivores to the third trophic level and provides a novel target for the improvement of biological control agents.

Technical Abstract: Plants defend themselves against herbivores through the production of toxic and deterrent metabolites. Adapted herbivores can tolerate and sometimes sequester these metabolites, allowing them to feed on defended plants and become toxic to their own enemies. Can herbivore natural enemies overcome sequestered plant defense metabolites to prey on adapted herbivores? To address this question, we studied how entomopathogenic nematodes cope with benzoxazinoid defense metabolites that are produced by grasses and sequestered by a specialist maize herbivore, the western corn rootworm. We find that nematodes from US maize fields in regions in which the western corn rootworm was present over the last 50 y are behaviorally and metabolically resistant to sequestered benzoxazinoids and more infective toward the western corn rootworm than nematodes from other parts of the world. Exposure of a benzoxazinoid-susceptible nematode strain to the western corn rootworm for 5 generations results in higher behavioral and metabolic resistance and benzoxazinoid-dependent infectivity toward the western corn rootworm. Thus, herbivores that are exposed to a plant defense sequestering herbivore can evolve both behavioral and metabolic resistance to plant defense metabolites, and these traits are associated with higher infectivity toward a defense sequestering herbivore. We conclude that plant defense metabolites that are transferred through adapted herbivores may result in the evolution of resistance in herbivore natural enemies. Our study also identifies plant defense resistance as a potential target for the improvement of biological control agents.