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

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

   Tan, Ching‐Wen ; Peiffer, Michelle L. ; Ali, Jared G. ; Luthe, Dawn S. ; Felton, Gary W. ; Biere, ed., Arjen ( July 2020 , Functional Ecology)

   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.

   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.

   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.

   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.

   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.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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2. 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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3. 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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4. Chemical defense over decadal scales: Ontogenetic allocation trajectories and consequences for fitness in a foundation tree species

   https://doi.org/10.1111/1365-2435.13425  

   Cope, Olivia L. ; Kruger, Eric L. ; Rubert‐Nason, Kennedy F. ; Lindroth, Richard L. ; Barton, ed., Kasey ( August 2019 , Functional Ecology)

   Expression of herbivore defense traits can change dramatically during the course of plant development. Little is known, however, about the degree of genetic or sexual variation in these ontogenetic defense trajectories or whether the trajectories themselves are adaptive, especially in long‐lived species.

   We used a 13‐year dataset of chemical defense traits, growth and survivorship from a common garden of trembling aspen (Populus tremuloides) genotypes to document long‐term defense trajectories and their relationship to tree fitness during juvenile and early mature stages.

   Overall, concentrations of the two principal classes of aspen defense compounds (salicinoid phenolic glycosides [SPGs] and condensed tannins [CTs]) decreased to differing degrees in foliage of juvenile trees and then remained relatively constant in maturity. Initial values, juvenile rates of change and average mature values all exhibited significant genetic variation for both SPGs and CTs.

   Relationships between defense trajectory parameters and metrics of tree fitness (growth and survivorship) depended on compound type and tree sex. Females with higher‐allocation SPG trajectories (high initial juvenile concentrations, slow juvenile declines, high mature concentrations) grew more slowly relative to females with lower‐allocation trajectories. In males, higher‐allocation SPG trajectories had a lesser effect on growth but were associated with reduced mortality. Juvenile CT trajectories were not correlated with tree fitness, but average CT concentration in maturity was positively related to growth in females.

   These results suggest that ontogenetic defense trajectories are adaptive and subject to natural selection. Genotypic variation and ontogeny shape tree defensive chemistry, both independently and interactively. These patterns of defense expression have the potential to structure trophic interactions and the genetic composition of forests in both space and time.

   A freePlain Language Summarycan be found within the Supporting Information of this article.

    

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5. Herbivory improves the fitness of predatory beetles

   https://doi.org/10.1111/1365-2656.13313  

   Ugine, Todd A. ; Nagra, Avneet ; Grebenok, Robert J. ; Behmer, Spencer T. ; Losey, John E. ; Dussutour, ed., Audrey ( September 2020 , Journal of Animal Ecology)

   While many predatory arthropods consume non‐prey foods from lower trophic levels, little is known about what drives the shift from predator to omnivore. Predatory lady beetles often consume non‐prey foods like plant foliage and pollen. One species,Coccinella septempunctata, eats foliage to redress sterol deficits caused by eating sterol‐deficient prey. Here we explore how omnivory benefits lady beetle fitness.

   We reared seven species of lady beetles—from five genera distributed across the tribe Coccinellini—on pea aphids in the presence or absence of fava bean foliage; pea aphids have very low sterol content. Foliage supplements lengthened the development times of four species and decreased survival to adulthood of two species; it had no effect on adult mass. We mated beetles in a 2 × 2 factorial design (males with or without foliage paired with females with or without foliage). For each species, we observed a profound paternal effect of foliage supplements on fitness. Females mated to foliage‐supplemented males laid more eggs and more viable eggs compared to females mated to non‐supplemented males. Foliage‐supplemented males produced 2.9–4.6 times more sperm compared to non‐supplemented males for the three species we examined.

   We analysed the sterol profile of four beetle species reared on pea aphids—with or without foliage—and compared their sterol profile to field‐collected adults. For two laboratory‐reared species, sterols were not detected in adult male beetles, and overall levels were generally low (total ng of sterol/beetle range: 3–33 ng); the exception beingPropylea quatuordecimpunctatafemales (total ng of sterol/beetle range: 50–157 ng). Laboratory‐reared lady beetle sterol content was not significantly affected by the presence of foliage. Field‐collected beetles had higher levels of sterols compared to laboratory‐reared beetles (2,452–145,348 ng per beetle); cholesterol and sitosterol were the dominant sterols in both field‐collected and laboratory‐reared beetles.

   Our findings indicate that herbivory benefits lady beetle fitness across the Coccinellini, and that this was entirely a paternal effect. Our data provide a rare example of a nutritional constraint impacting fitness in a sex‐specific manner. It also shows, more broadly, how a nutritional constraint can drive predators towards omnivory.

    

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