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1. Top-down effects from parasitoids may mediate plant defence and plant fitness

   https://doi.org/DOI: 10.1111/1365-2435.13617  

   Tan, C.-W. ; Peiffer, Michelle ; Ali, Jared G. ; Luthe, D.S. ; Felton, Gary w. ( October 2020 , Functional ecology)

   null (Ed.)

   1. Plants face many environmental stresses that can impact their survival, development and fitness. Insects are the most diverse, abundant and threatening herbivores in nature. As a consequence, plants produce direct chemical and physical defences to reduce herbivory. They also release volatiles to recruit natural enemies that indirectly protect them from herbivory. The recruitment of parasitic wasps can benefit plant fitness because they ultimately kill their insect hosts. 2. Recently, studies showed that parasitoids can indirectly mediate plant defences by modulating herbivore oral secretions. In addition to the direct benefits of parasitoids in terms of reducing herbivore survival, we tested if the reduction in induced defences by parasitized caterpillars compared to non-parasitized caterpillars may reduce the costs associated with defence expression. 3. We provide evidence that tomato plants treated with saliva from parasitized caterpillars have significantly higher fitness parameters including increased flower numbers (16.3%) and heavier fruit weight (13.5%), compared to plants treated with saliva from non-parasitized caterpillars. Since plants were grown without actual herbivores, the higher values for these fitness parameters were due to lower costs of induced defences and not due to reduced herbivory by parasitized caterpillars. Furthermore, the resulting seed germination time was shorter and the germination rate was higher when the maternal plants were previously exposed to parasitized herbivore treatment compared to control (non-treated) plants. 4. Overall, application of saliva did not result in transgenerational priming of offspring defence responses. However, offspring of parents exposed to caterpillar saliva had lower constitutive levels and higher induced levels of trypsin inhibitor than offspring from unexposed parents. 5. This study shows that the saliva of parasitized caterpillars can modulate plant defences and further demonstrates that the lower induction of plant defences is associated with elevated plant fitness in the absence of herbivore feeding, suggesting that induced plant defences are costly. 

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2. Divergent host plant utilization by adults and offspring is related to intra‐plant variation in chemical defences

   https://doi.org/10.1111/1365-2656.13063  

   Mason, Charles J. ; Long, David C. ; Lindroth, Richard L. ; Hoover, Kelli ; Behmer, ed., Spencer ( July 2019 , Journal of Animal Ecology)

   Adult and juvenile herbivores of the same species can use divergent feeding strategies, and thus may inhabit and consume different parts of the plant. Because the expression of chemical defences often differs between host plant tissues, this variation may result in disparate performance outcomes for adult and juvenile conspecifics that feed on distinct dietary substrates.

   The goal of this study was to evaluate how host range may differ between adults and juveniles in a generalist herbivore. We addressed the impacts of among‐ and within‐plant defence variation using the wood‐feeding Asian longhorned beetle (Anoplophora glabripennis) and three host plants having a range of putative resistance.

   Impacts of host plants on adult and offspring performance were assessed using a series of controlled bioassays. We evaluated adult‐feeding and egg‐laying behaviours in choice and no‐choice experiments using the different hosts, and subsequent offspring establishment. We then evaluated host plant chemical composition related to nutrition and defence.

   Different plants had strong impacts on adult performance, but these patterns did not extend to effects on offspring. Females were capable of developing eggs when providedAcer rubrum, but notPopulus deltoidesorPopulus tomentosa. Females that produced eggs by feeding onA. rubrum,however, deposited eggs into all three plant species. Larvae hatched and consumed tissues in all three hosts. The differences between adult and juvenile utilization ofPopulusspp. were reflected in markedly higher salicinoid phenolic concentrations in bark (>2% dw), while wood had trace quantities.

   Our results demonstrate that plant resistance mechanisms can differentially act upon adult and juvenile life stages of a polyphagous herbivore when there is differential expression of chemical defences among plant tissue types.Anoplophora glabripennishas been a globally successful invader due in part to its broad host range, and our results suggest a mechanism that permits the beetle to exploit marginally resistant plants. This study has implications for how host range differs between insect feeding stages, which is particularly important for invasive, polyphagous species encountering novel food sources.

    

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3. The interactive effects of heat stress, parasitism and host plant quality in a host–parasitoid system

   https://doi.org/10.1111/1365-2435.14498  

   Parker, Anna L. ; Kingsolver, Joel G. ( January 2024 , Functional Ecology)

   Species interactions are expected to change in myriad ways as the frequency and magnitude of extreme temperature events increase with anthropogenic climate change.

   The relationships between endosymbionts, parasites and their hosts are particularly sensitive to thermal stress, which can have cascading effects on other trophic levels.

   We investigate the interactive effects of heat stress and parasitism on a terrestrial tritrophic system consisting of two host plants (one common, high‐quality plant and one novel, low‐quality plant), a caterpillar herbivore and a specialist parasitoid wasp.

   We used a fully factorial experiment to determine the bottom‐up effects of the novel host plant on both the caterpillars' life history traits and the wasps' survival, and the top‐down effects of parasitism and heat shock on caterpillar developmental outcomes and herbivory levels.

   Host plant identity interacted with thermal stress to affect wasp success, with wasps performing better on the low‐quality host plant under constant temperatures but worse under heat‐shock conditions.

   Surprisingly, caterpillars consumed less leaf material from the low‐quality host plant to reach the same final mass across developmental outcomes.

   In parasitized caterpillars, heat shock reduced parasitoid survival and increased both caterpillar final mass and development time on both host plants.

   These findings highlight the importance of studying community‐level responses to climate change from a holistic and integrative perspective and provide insight into potential substantial interactions between thermal stress and diet quality in plant–insect systems.

   Read the freePlain Language Summaryfor this article on the Journal blog.

    

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4. Macroevolutionary patterns in overexpression of tyrosine: An anti‐herbivore defence in a speciose tropical tree genus, Inga (Fabaceae)

   https://doi.org/10.1111/1365-2745.13208  

   Coley, Phyllis D. ; Endara, María‐José ; Ghabash, Gabrielle ; Kidner, Catherine A. ; Nicholls, James A. ; Pennington, R. Toby ; Mills, Anthony G. ; Soule, Abrianna J. ; Lemes, Maristerra R. ; Stone, Graham N. ; et al ( May 2019 , Journal of Ecology)

   Plant secondary metabolites are a key defence against herbivores, and their evolutionary origin is likely from primary metabolites. Yet for this to occur, an intermediate step of overexpression of primary metabolites would need to confer some advantage to the plant. Here, we examine the evolution of overexpression of the essential amino acid, L‐tyrosine and its role as a defence against herbivores.

   We examined overexpression of tyrosine in 97 species ofInga(Fabaceae), a genus of tropical trees, at five sites throughout the Neotropics. We predicted that tyrosine could act as an anti‐herbivore defence because concentrations of 4% tyrosine in artificial diets halved larval growth rates. We also collected insect herbivores to determine if tyrosine and its derivatives influenced host associations.

   Overexpression of tyrosine was only present in a single lineage comprising 21 species, with concentrations ranging from 5% to 20% of the leaf dry weight. Overexpression was pronounced in expanding but not in mature leaves. Despite laboratory studies showing toxicity of L‐tyrosine,Ingaspecies with tyrosine suffered higher levels of herbivory. We therefore hypothesize that overexpression is only favoured in species with less effective secondary metabolites. Some tyrosine‐producing species also contained secondary metabolites that are derived from tyrosine: tyrosine‐gallates, tyramine‐gallates and DOPA‐gallates. Elevated levels of transcripts of prephenate dehydrogenase, an enzyme in the tyrosine biosynthetic pathway that is insensitive to negative feedback from tyrosine, were found only in species that overexpress tyrosine or related gallates. Different lineages of herbivores showed contrasting responses to the overexpression of tyrosine and its derived secondary metabolites in their host plants.

   Synthesis. We propose that overexpression of some primary metabolites can serve as a chemical defence against herbivores, and are most likely to be selected for in species suffering high herbivory due to less effective secondary metabolites. Overexpression may be the first evolutionary step in the transition to the production of more derived secondary metabolites. Presumably, derived compounds would be more effective and less costly than free tyrosine as anti‐herbivore defences.

    

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5. Domesticated tomatoes are more vulnerable to negative plant–soil feedbacks than their wild relatives

   https://doi.org/10.1111/1365-2745.13157  

   Carrillo, Juli ; Ingwell, Laura L. ; Li, Xiaohong ; Kaplan, Ian ; Pineda, ed., Ana ( March 2019 , Journal of Ecology)

   Domesticated plants can differ from their wild counterparts in the strength and outcome of species interactions, both above‐ and belowground. Plant–soil feedbacks influence plant success, and plant‐associated soil microbial communities can influence plant interactions with herbivores and their natural enemies, yet, it remains unclear if domestication has changed these relationships.

   To determine the effects of domestication on plant–soil interactions, we characterized soil microbial communities associated with various cultivars of domesticated tomato and some of its wild relatives. We measured the strength and direction of plant–soil feedbacks for domesticated and wild tomatoes, and the effects of soil on plant resistance to specialist herbivory byManduca sexta, and the attraction of a parasitoid wasp,Cotesia congregata.

   Domesticated tomatoes and their wild relatives had negative plant–soil feedbacks, as conspecifics cultivated soil that negatively impacted performance of subsequent plants (longer germination time, lower biomass) than if they grew in non‐tomato soils. Significant variation existed among domesticated and wild tomato varieties in the strength of these feedbacks, ranging from neutral to strongly negative. For above‐ground plant biomass, tomato wild relatives were unaffected by growing in tomato‐conditioned soil, whereas domesticated tomatoes grew smaller in tomato soil, indicating effects of plant domestication. Overall, increased microbial biomass within the rhizosphere resulted in progressively less‐negative plant–soil feedbacks.

   Plant cultivars had different levels of resistance to herbivory byM. sexta, but this did not depend on plant domestication or soil type. The parasitoidC. congregatawas primarily attracted to herbivore damaged plants, independent of plant domestication status, and for these damaged plants, wasps preferred some cultivars over others, and wild plants grown in tomato soil over wild plants grown in non‐tomato soil.

   Synthesis.These results indicate that crop tomatoes are more likely to show negative plant–soil feedbacks than wild progenitors, which could partially explain their sensitivity to monocultures in agricultural soils. Furthermore, cultivar‐specific variation in the ability to generate soil microbial biomass, independent of domestication status, appears to buffer the negative consequences of sharing the same soil. Last, soil legacies were relatively absent for herbivores, but not for parasitoid wasps, suggesting trophic level specificity in soil feedbacks on plant–insect interactions.

    

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