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  1. Abstract

    Phenotypic variability results from interactions between genotype and environment and is a major driver of ecological and evolutionary interactions. Measuring the relative contributions of genetic variation, the environment, and their interaction to phenotypic variation remains a fundamental goal of evolutionary ecology.

    In this study, we assess the question: How do genetic variation and local environmental conditions interact to influence phenotype within a single population? We explored this question using seed from a single population of common milkweed,Asclepias syriaca, in northern Michigan. We first measured resistance and resistance traits of 14 maternal lines in two common garden experiments (field and greenhouse) to detect genetic variation within the population. We carried out a reciprocal transplant experiment with three of these maternal lines to assess effects of local environment on phenotype. Finally, we compared the phenotypic traits measured in our experiments with the phenotypic traits of the naturally growing maternal genets to be able to compare relative effect of genetic and environmental variation on naturally occurring phenotypic variation. We measured defoliation levels, arthropod abundances, foliar cardenolide concentrations, foliar latex exudation, foliar carbon and nitrogen concentrations, and plant growth.

    We found a striking lack of correlation in trait expression of the maternal lines between the common gardens, or between the common gardens and the naturally growing maternal genets, suggesting that environment plays a larger role in phenotypic trait variation of this population. We found evidence of significant genotype‐by‐environment interactions for all traits except foliar concentrations of nitrogen and cardenolide. Milkweed resistance to chewing herbivores was associated more strongly with the growing environment. We observed no variation in foliar cardenolide concentrations among maternal lines but did observe variation among maternal lines in foliar latex exudation.

    Overall, our data reveal powerful genotype‐by‐environment interactions on the expression of most resistance traits in milkweed.

     
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  2. Abstract

    To understand how comprehensive plant defense phenotypes will respond to global change, we investigated the legacy effects of elevated CO2on the relationships between chemical resistance (constitutive and induced via mechanical damage) and regrowth tolerance in four milkweed species (Asclepias). We quantified potential resistance and tolerance trade‐offs at the physiological level following simulated mowing, which are relevant to milkweed ecology and conservation. We examined the legacy effects of elevated CO2on four hypothesized trade‐offs between the following: (a) plant growth rate and constitutive chemical resistance (foliar cardenolide concentrations), (b) plant growth rate and mechanically induced chemical resistance, (c) constitutive resistance and regrowth tolerance, and (d) regrowth tolerance and mechanically induced resistance. We observed support for one trade‐off between plant regrowth tolerance and mechanically induced resistance traits that was, surprisingly, independent of CO2exposure. Across milkweed species, mechanically induced resistance increased by 28% in those plants previously exposed to elevated CO2.In contrast, constitutive resistance and the diversity of mechanically induced chemical resistance traits declined in response to elevated CO2in two out of four milkweed species. Finally, previous exposure to elevated CO2uncoupled the positive relationship between plant growth rate and regrowth tolerance following damage. Our data highlight the complex and dynamic nature of plant defense phenotypes under environmental change and question the generality of physiologically based defense trade‐offs.

     
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  3. Abstract

    Animals rely on a balance of endogenous and exogenous sources of immunity to mitigate parasite attack. Understanding how environmental context affects that balance is increasingly urgent under rapid environmental change. In herbivores, immunity is determined, in part, by phytochemistry which is plastic in response to environmental conditions. Monarch butterfliesDanaus plexippus, consistently experience infection by a virulent parasiteOphryocystis elektroscirrha, and some medicinal milkweed (Asclepias) species, with high concentrations of toxic steroids (cardenolides), provide a potent source of exogenous immunity.

    We investigated plant‐mediated influences of elevated CO2(eCO2) on endogenous immune responses of monarch larvae to infection byO. elektroscirrha. Recently, transcriptomics have revealed that infection byO. elektroscirrhadoes not alter monarch immune gene regulation in larvae, corroborating that monarchs rely more on exogenous than endogenous immunity. However, monarchs feeding on medicinal milkweed grown under eCO2lose tolerance to the parasite, associated with changes in phytochemistry. Whether changes in milkweed phytochemistry induced by eCO2alter the balance between exogenous and endogenous sources of immunity remains unknown.

    We fed monarchs two species of milkweed;A. curassavica(medicinal) andA. incarnata(non‐medicinal) grown under ambient CO2(aCO2) or eCO2. We then measured endogenous immune responses (phenoloxidase activity, haemocyte concentration and melanization strength), along with foliar chemistry, to assess mechanisms of monarch immunity under future atmospheric conditions.

    The melanization response of late‐instar larvae was reduced on medicinal milkweed in comparison to non‐medicinal milkweed. Moreover, the endogenous immune responses of early‐instar larvae to infection byO. elektroscirrhawere generally lower in larvae reared on foliage from aCO2plants and higher in larvae reared on foliage from eCO2plants. When grown under eCO2, milkweed plants exhibited lower cardenolide concentrations, lower phytochemical diversity and lower nutritional quality (higher C:N ratios). Together, these results suggest that the loss of exogenous immunity from foliage under eCO2results in increased endogenous immune function.

    Animal populations face multiple threats induced by anthropogenic environmental change. Our results suggest that shifts in the balance between exogenous and endogenous sources of immunity to parasite attack may represent an underappreciated consequence of environmental change.

     
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  4. Abstract

    Herbivorous insects have evolved many mechanisms to overcome plant chemical defences, including detoxification and sequestration. Herbivores may also use toxic plants to reduce parasite infection. Plant toxins could directly interfere with parasites or could enhance endogenous immunity. Alternatively, plant toxins could favour down‐regulation of endogenous immunity by providing an alternative (exogenous) defence against parasitism. However, studies on genomewide transcriptomic responses to plant defences and the interplay between plant toxicity and parasite infection remain rare. Monarch butterflies (Danaus plexippus) are specialist herbivores of milkweeds (Asclepiasspp.), which contain toxic cardenolides. Monarchs have adapted to cardenolides through multiple resistance mechanisms and can sequester cardenolides to defend against bird predators. In addition, high‐cardenolide milkweeds confer monarch resistance to a specialist protozoan parasite (Ophryocystis elektroscirrha). We used this system to study the interplay between the effects of plant toxicity and parasite infection on global gene expression. We compared transcriptional profiles between parasite‐infected and uninfected monarch larvae reared on two milkweed species. Our results demonstrate that monarch differentially express several hundred genes when feeding onA. curassavicaandA. incarnata, two species that differ substantially in cardenolide concentrations. These differentially expressed genes include genes within multiple families of canonical insect detoxification genes, suggesting that they play a role in monarch toxin resistance and sequestration. Interestingly, we found little transcriptional response to infection. However, parasite growth was reduced in monarchs reared onA. curassavica, and in these monarchs, several immune genes were down‐regulated, consistent with the hypothesis that medicinal plants can reduce reliance on endogenous immunity.

     
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