Host Plant Effects on the Caterpillar Immune Response

Smilanich, Angela M.; Muchoney, Nadya D.

doi:10.1007/978-3-030-86688-4_14

Cited by 11 publications

(13 citation statements)

References 156 publications

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“…In recent years, eco‐immunological research has highlighted the immune response as a critical physiological link between herbivore diet and interactions with natural enemies. Such studies have revealed substantial diet‐mediated variation in herbivore immune function (Singer et al, 2014), with repercussions for resistance against diverse natural enemies (reviewed in Smilanich & Muchoney, 2022). For example, several studies have documented positive effects of dietary protein content on caterpillar immune function, which have been linked to increased survival following bacterial or viral challenge in experimental settings (e.g., Cotter et al, 2019; Lee et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore

Muchoney

Bowers

Carper

et al. 2022

Ecology and Evolution

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Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly, Euphydryas phaeton (Nymphalidae), have recently incorporated an exotic plant, Plantago lanceolata (Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus, Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using either P. lanceolata or a native plant, Chelone glabra (Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies.

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Section: Introductionmentioning

confidence: 99%

Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore

Muchoney

Bowers

Carper

et al. 2022

Ecology and Evolution

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“…An increasing number of studies have focused on the interaction between plant secondary chemistry and herbivore immune responses when explaining the relationship between larval performance on host plants and defence against parasitoids, predators, and pathogens. Nearly all these studies have shown that herbivore immune systems are weakened when they feed on more toxic host plants (Reudler et al, 2011; Smilanich, Dyer, Chambers, et al, 2009; Smilanich & Muchoney, 2022; but see Garvey et al, 2021, Ghosh et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

Plant species with higher chemical defences enhance herbivore cellular immunity with differential effectiveness against two parasitoid species

2023

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1. Insect herbivores simultaneously experience bottom-up effects of plant defensive chemistry and the top-down effects of natural enemies. At the intersection of these effects are herbivore immune systems, herbivore traits that have largely been overlooked in studies of plant-insect interactions. Most previous studies have demonstrated compromised immunity of herbivores that feed on plants with higher defensive chemistry. Many studies have used embedded microfilaments or silica beads as proxies for parasitoid eggs. Yet, parasitoids may evade or suppress host immune responses by injecting venom and calyx fluid, or through modifications of their egg surface structure, necessitating studies that include all three trophic levels to obtain a complete picture of how plant traits may modulate herbivore immunity.2. Here, we examined the effect of host plant species that differ in glucosinolate (antiherbivore compounds produced by plants in the Brassicaceae) concentrations on the immune status of an herbivore and its consequences for two species of parasitoids with different life history traits.3. We found that larvae of the butterfly Pieris rapae that fed on field mustard Brassica rapa, which contain 52-fold higher glucosinolate concentrations than collards B. oleracea, attained lower body weights and experienced prolonged development to adulthood.4. Yet, caterpillars that fed on B. rapa had enhanced cellular immunity, as measured by total and differential haemocyte counts as well as melanization capacity, compared to larvae that fed on B. oleracea. 5. In turn, the likelihood that at least some eggs in clutches of the gregarious endoparasitoid Cotesia glomerata would be encapsulated, leading to a reduction in brood size, were three times greater when their host caterpillars fed on B. rapa compared to B. oleracea.6. Interestingly, eggs of the solitary endoparasitoid Cotesia rubecula were rarely encapsulated irrespective of the host plant on which their host caterpillar fed. | 1493Functional Ecology GHOSH et al. | Study organismsSeeds of collards (Brassica oleracea var. viridis) and field mustard (Brassica rapa subsp. dichotoma) were obtained from the USDA-GRIN seed bank. All plants were grown under greenhouse conditions (26 ± 8°C, 40%-60% RH, and a L:D 16:8 h photoperiod) in 20 cm diameter pots filled with potting soil (Lambert LM-HP) and 5 g of Osmocote fertilizer (N: P: K -1: 1: 1). After 4 weeks, plants with four to six fully expanded leaves were used for all experiments. Adult P. rapae were collected from an organic crucifer farm near Fort Collins, Colorado. Cotesia glomerata cocoons were collected from the same crucifer fields near Fort Collins, and C. rubecula colonies were started from cocoons collected on crucifers on the University of Minnesota campus in St. Paul, Minnesota. Both parasitoid colonies were maintained by parasitizing second instar P. rapae larvae. These colonies were periodically supplemented with fieldcollected parasitoids. Adult parasitoids were maintained in humiditycontrolled incubator (15°C, 50...

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“…An increasing number of studies have focused on the interaction between plant secondary chemistry and herbivore immune responses when explaining the relationship between larval performance on host plants and defense against parasitoids, predators, and pathogens. Nearly all these studies have shown that herbivore immune systems are weakened when they feed on more toxic host plants (Reudler et al 2011;Smilanich et al 2009a;Smilanich & Muchoney 2022; but see Garvey et al 2021, Ghosh et al 2022.…”

Section: Discussionmentioning

confidence: 99%

“…Caterpillar species that sequester plant toxins as well as species where plant toxins accumulate in the hemolymph generally have weak immune systems (e.g., Freitak et al 2003;Smilanich et al 2009;Lampert & Bowers 2015;Tan et al 2019;Smilanich & Muchoney 2022), suggesting that the costs of sequestration trade off with the ability to invest in a robust immune system. Sequestration may reduce the need to invest in costly immune responses.…”

Section: Discussionmentioning

confidence: 99%

“…However, a few studies have found that elevated levels of plant defense chemistry may enhance immune responses (e.g., Garvey et al 2021;Ghosh et al 2022). The majority of eco-immunological studies of plant defense chemistry effects on caterpillar immune responses have been bi-trophic in that immunity has been measured in terms of responses against artificial implants (see review by Smilanich & Muchoney 2022). Our understanding of how these relationships interact with higher trophic levels is largely lacking with rare exception (e.g., Bukovinzsky et al 2009).…”

Section: Introductionmentioning

confidence: 99%

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Host plant chemistry enhances herbivore cellular immunity with differential effectiveness against two parasitoid species

Ghosh

Ode

Ryan³

2022

Preprint

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Insect herbivores must simultaneously balance bottom-up effects of plant defensive chemistry and the top-down effects of natural enemies. At the intersection of these effects are herbivore immune systems, an herbivore trait that has largely been overlooked in studies of plant-insect interactions. Counter to the majority of studies showing that herbivores feeding on plants containing higher levels of toxins are immunocompromised, we demonstrate that Pieris rapae caterpillars feeding on more toxic host plants have enhanced cellular immunity at the cost of reduced growth rates and body size. However, whether enhanced immune systems are effective defense against parasitoids depends on parasitoid identity. Whereas enhanced immunity provided increased protection against the parasitoid Cotesia glomerata, it did not provide protection against C. rubecula that suppressed and evaded the host’s immune system. Our study demonstrates that both herbivore immunity and species identity of trophic participants are crucial in determining the structure of multitrophic interactions.

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Host Plant Effects on the Caterpillar Immune Response

Cited by 11 publications

References 156 publications

Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore

Use of an exotic host plant shifts immunity, chemical defense, and viral burden in wild populations of a specialist insect herbivore

Plant species with higher chemical defences enhance herbivore cellular immunity with differential effectiveness against two parasitoid species

Host plant chemistry enhances herbivore cellular immunity with differential effectiveness against two parasitoid species

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