Jasmonic acid-induced plant defenses delay caterpillar developmental resistance to a baculovirus: Slow-growth, high-mortality hypothesis in plant–insect–pathogen interactions
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Journal of Invertebrate Pathology
Plants damaged by herbivore feeding can induce defensive responses that reduce herbivore growth. The slowgrowth, high-mortality hypothesis postulates that these non-lethal plant defenses prolong the herbivore's period of susceptibility to natural enemies, such as predators and parasitoids. While many juvenile animals increase their disease resistance as they grow, direct tests of the slow-growth, high-mortality hypothesis in the context of plant–herbivore–pathogen interactions are lacking. Caterpillars increase their resistance to lethal baculoviruses as they develop within and across instars, a phenomenon termed developmental resistance. Progression of developmental resistance can occur through age-related increases in systemic immune functioning and/or midgutbased resistance. Here, we examined the slow-growth, high-mortality hypothesis in the context of developmental resistance of caterpillars to baculoviruses. Intra-stadial (within-instar) developmental resistance of the fall armyworm, Spodoptera frugiperda, to an oral inoculum of the baculovirus SfMNPV increased more rapidly with age when larvae were fed on non-induced foliage than foliage that was induced by jasmonic acid (a phytohormone that up-regulates plant anti-herbivore defenses). The degree of developmental resistance observed was attributable to larval weight at the time of virus inoculation. Thus, slower growth on induced plants prolonged the window of larval susceptibility to the baculovirus. Developmental resistance on induced and non-induced plants was absent when budded virus was injected intrahemocoelically bypassing the midgut, suggesting that developmental resistance was gut-based. Addition of fluorescent brightener, which weakens midgut-based resistance mechanisms to oral virus challenge, abolished developmental resistance. These results highlight the impact of plant defenses on herbivore growth rate and consequences for disease risk.
KeywordsAge-related disease resistance; Infection risk; Midgut immunity; Multitrophic interactions; Nucleopolyhedrovirus; Tritrophic interactions
Shikano, Ikkei; McCarthy, Elizabeth; Hayes-Plazolles, Nancy; Slavicek, James M.; Hoover, Kelli. 2018. Jasmonic acid-induced plant defenses delay caterpillar developmental resistance to a baculovirus: Slow-growth, high-mortality hypothesis in plant–insect–pathogen interactions. Journal of Invertebrate Pathology. 158: 16-23. https://doi.org/10.1016/j.jip.2018.09.001.