Plant defense resistance in natural enemies of a specialist insect herbivore

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 years are
behaviorally and metabolically resistant to sequestered benzoxazinoids and
more infective towards 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 five generations results in higher
behavioral and metabolic resistance and benzoxazinoid-dependent
infectivity towards 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 towards 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.