TY - JOUR
T1 - Jasmonic acid-induced plant defenses delay caterpillar developmental resistance to a baculovirus
T2 - Slow-growth, high-mortality hypothesis in plant–insect–pathogen interactions
AU - Shikano, Ikkei
AU - McCarthy, Elizabeth
AU - Hayes-Plazolles, Nancy
AU - Slavicek, James M.
AU - Hoover, Kelli
N1 - Publisher Copyright:
© 2018 Elsevier Inc.
PY - 2018/10
Y1 - 2018/10
N2 - Plants damaged by herbivore feeding can induce defensive responses that reduce herbivore growth. The slow-growth, 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 midgut-based 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.
AB - Plants damaged by herbivore feeding can induce defensive responses that reduce herbivore growth. The slow-growth, 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 midgut-based 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.
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U2 - 10.1016/j.jip.2018.09.001
DO - 10.1016/j.jip.2018.09.001
M3 - Article
C2 - 30189196
AN - SCOPUS:85052898107
SN - 0022-2011
VL - 158
SP - 16
EP - 23
JO - Journal of invertebrate pathology
JF - Journal of invertebrate pathology
ER -