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  1. Abstract

    The fundamental tradeoff between carbon gain and water loss has long been predicted as an evolutionary driver of plant strategies across environments. Nonetheless, challenges in measuring carbon gain and water loss in ways that integrate over leaf lifetime have limited our understanding of the variation in and mechanistic bases of this tradeoff. Furthermore, the microevolution of plant traits within species versus the macroevolution of strategies among closely related species may not be the same, and accordingly, the latter must be addressed using comparative phylogenetic analyses.

    Here we introduce the concept of ‘integrated metabolic strategy’ (IMS) to describe the ratio between carbon isotope composition (δ13C) and oxygen isotope composition above source water (Δ18O) of leaf cellulose. IMS is a measure of leaf‐level conditions that integrate several mechanisms contributing to carbon gain (δ13C) and water loss (Δ18O) over leaf lifespan, with larger values reflecting higher metabolic efficiency and hence less of a tradeoff. We tested how IMS evolves among closely related yet ecologically diverse milkweed species, and subsequently addressed phenotypic plasticity in response to water availability in species with divergent IMS.

    Integrated metabolic strategy varied strongly among 20Asclepiasspecies when grown under controlled conditions, and phylogenetic analyses demonstrate species‐specific tradeoffs between carbon gain and water loss. Larger IMS values were associated with species from dry habitats, with larger carboxylation capacity, smaller stomatal conductance and smaller leaves; smaller IMS was associated with wet habitats, smaller carboxylation capacity, larger stomatal conductance and larger leaves. The evolution of IMS was dominated by changes in species’ demand for carbon (δ13C) more so than water conservation (Δ18O). Although some individual physiological traits showed phylogenetic signal, IMS did not.

    In response to experimental decreases in soil moisture, three species maintained similar IMS across levels of water availability because of proportional increases inδ13C and Δ18O (or little change in either), while one species increased IMS due to disproportional changes inδ13C relative to Δ18O.

    Synthesis.IMS is a broadly applicable mechanistic tool; IMS variation among and within species may shed light on unresolved questions relating to the evolution and ecology of plant ecophysiological strategies.

     
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  2. Abstract

    Ecological interactions range from purely specialized to extremely generalized in nature. Recent research has showed very high levels of specialization in the cyanolichens involvingPeltigera(mycobionts) and theirNostocphotosynthetic partners (cyanobionts). Yet, little is known about the mechanisms contributing to the establishment and maintenance of such high specialization levels.

    Here, we characterized interactions betweenPeltigeraandNostocpartners at a global scale, using more than one thousand thalli. We used tools from network theory, community phylogenetics and biogeographical history reconstruction to evaluate how these symbiotic interactions may have evolved.

    After splitting the interaction matrix into modules of preferentially interacting partners, we evaluated how module membership might have evolved along the mycobionts’ phylogeny. We also teased apart the contributions of geographical overlap vs phylogeny in driving interaction establishment betweenPeltigeraandNostoctaxa.

    Module affiliation rarely evolves through the splitting of large ancestral modules. Instead, new modules appear to emerge independently, which is often associated with a fungal speciation event. We also found strong phylogenetic signal in these interactions, which suggests that partner switching is constrained by conserved traits. Therefore, it seems that a high rate of fungal diversification following a switch to a new cyanobiont can lead to the formation of large modules, with cyanobionts associating with multiple closely retatedPeltigeraspecies.

    Finally, when restricting our analyses toPeltigerasister species, the latter differed more through partner acquisition/loss than replacement (i.e., switching). This pattern vanishes as we look at sister species that have diverged longer ago. This suggests that fungal speciation may be accompanied by a stepwise process of (a) novel partner acquisition and (b) loss of the ancestral partner. This could explain the maintenance of high specialization levels in this symbiotic system where the transmission of the cyanobiont to the next generation is assumed to be predominantly horizontal.

    Synthesis.Overall, our study suggests that oscillation between generalization and ancestral partner loss may maintain high specialization within the lichen genusPeltigera, and that partner selection is not only driven by partners’ geographical overlap, but also by their phylogenetically conserved traits.

     
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  3. Abstract

    Forest structure and diversity can regulate tree vulnerability to damage by insects and pathogens. Past work suggests that trees with diverse neighbours should experience less leaf herbivory and less damage from specialist herbivores and diseases, and that the effect of neighbourhood diversity should be strongest at small spatial scales.

    In an early stage temperate tree diversity experiment, we monitored damage from leaf removing herbivores, specialist (gallers and leaf miners) herbivores, and two specialist fungal diseases (maple leaf anthracnose and cedar apple gall rust) over 3 years. The experimental design included treatments that varied independently in phylogenetic and functional diversity and we made our analyses across four spatial scales (1–16 m2).

    Neighborhood diversity simultaneously increased leaf removal for some species, decreased it for others, and had no effect on yet others. Height apparency—the difference between a focal plant’s height and its neighbours’—was the best single predictor of leaf removal across species and spatial scales, but the strength and direction of its effect were also species‐specific.

    Specialist pathogens and fungal foliar diseases showed signs of associational resistance and susceptibility. Oaks (Quercusspp.) were more resistant to leaf miners and maples were more resistant to anthracnose when surrounded by diverse neighbours (associational resistance). In contrast, birches (Betula papyrifera) were more susceptible to leaf miners and eastern red cedars (Juniperus virginiana) were more susceptible to cedar apple gall rust (Gymnosporangium juniperi‐virginianae) infection in diverse environments (associational susceptibility).

    Herbivore and pathogen damage was better predicted by community structure and diversity at small spatial scales (1 and 4 m2) than large scales (9 and 16 m2), suggesting a characteristic spatial scale for these biodiversity‐ecosystem functioning effects.

    Synthesis.Humans control forest diversity through selective harvesting and planting in natural stands and plantations. Our experimental demonstration of the role of local community structure and diversity in suppressing some forms of pest and pathogen damage to trees suggests that forest management can be most effective when diversity is considered at small spatial scales and the underlying biology of particular pests, pathogens, and hosts is taken into account. Pictured here: the “galls” formed by cedar apple gall rust (Gymnosporangium juniperae‐virginiae) on eastern red cedar (Juniperus virginiana) in early spring release wind‐dispersed teleospores. Junipers showed associational susceptibility: greater susceptibility to gall rust with more diverse neighbours.

     
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  4. Abstract

    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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