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All organisms experience fundamental conflicts between divergent metabolic processes. In plants, a pivotal conflict occurs between allocation to growth, which accelerates resource acquisition, and to defense, which protects existing tissue against herbivory. Trade-offs between growth and defense traits are not universally observed, and a central prediction of plant evolutionary ecology is that context-dependence of these trade-offs contributes to the maintenance of intraspecific variation in defense [Züst and Agrawal,Annu. Rev. Plant Biol., 68, 513–534 (2017)]. This prediction has rarely been tested, however, and the evolutionary consequences of growth–defense trade-offs in different environments are poorly understood, especially in long-lived species [Cipolliniet al.,Annual Plant Reviews(Wiley, 2014), pp. 263–307]. Here we show that intraspecific trait trade-offs, even when fixed across divergent environments, interact with competition to drive natural selection of tree genotypes corresponding to their growth–defense phenotypes. Our results show that a functional trait trade-off, when coupled with environmental variation, causes real-time divergence in the genetic architecture of tree populations in an experimental setting. Specifically, competitive selection for faster growth resulted in dominance by fast-growing tree genotypes that were poorly defended against natural enemies. This outcome is a signature example of eco-evolutionary dynamics: Competitive interactions affected microevolutionary trajectories on a timescale relevant to subsequent ecological interactions [Brunneret al.,Funct. Ecol.33, 7–12 (2019)]. Eco-evolutionary drivers of tree growth and defense are thus critical to stand-level trait variation, which structures communities and ecosystems over expansive spatiotemporal scales.

 

Although genetic diversity within stands of trees is known to have community-level consequences, whether such effects are present at an even finer genetic scale is unknown. We examined the hypothesis that genetic variability (heterozygosity) within an individual plant would affect its dependent community, which adds a new dimension to the importance of genetic diversity. Our study contrasted foliar arthropod community diversity and microsatellite marker-derived measures of genetic diversity of cottonwood (Populus fremontii) trees that had been felled by beavers (Castor canadensis) and were resprouting, relative to adjacent standing, unfelled trees. Three patterns emerged: 1. Productivity (specific leaf area), phytochemical defenses (salicortin), and arthropod community richness, abundance, and diversity were positively correlated with the heterozygosity of individual felled trees, but not with that of unfelled trees; 2. These relationships were not explained by population substructure, genetic relatedness of the trees, or hybridization; 3. The underlying mechanism appears to be that beaver herbivory stimulates increased productivity (i.e., 2× increase from the most homozygous to the most heterozygous tree) that is the greatest in more heterozygous trees. Salicortin defenses in twigs were also expressed at higher concentrations in more heterozygous trees (i.e., 3× increase from the most homozygous to the most heterozygous tree), which suggests that this compound may dissuade further herbivory by beavers, as has been found for other mammalian herbivores. We suggest that high stress to trees as a consequence of felling reveals a heterozygosity–productivity linkage, which in turn is attractive to arthropods. Although experiments are required to demonstrate causality, these results link the genetic diversity of individual trees to community diversity, supporting the hypothesis that interactions among foundation species (beavers and trees) have community-level effects, and underscores the importance of genetic diversity for biodiversity, conservation, and restoration. 

The North American beaver (Castor canadensis Kuhl) and cottonwoods (Populus spp.) are foundation species, the interactions of which define a much larger community and affect a threatened riparian habitat type. Few studies have tested the effect of these interactions on plant chemistry and a diverse arthropod community. We experimentally examined the impact of beaver foraging on riparian communities by first investigating beaver food preferences for one cottonwood species, Fremont cottonwood (P. fremontii S. Watson), compared to other locally available woody species. We next examined the impact of beaver foraging on twig chemistry and arthropod communities in paired samples of felled and unfelled cottonwood species in northern Arizona (P. fremontii) and southwestern Colorado (narrowleaf cottonwood, P. angustifolia James, and Eastern cottonwood, P. deltoides W. Bartram ex Marshall). Four major patterns emerged: (1) In a cafeteria experiment, beavers chose P. fremontii six times more often than other woody native and exotic species. (2) With two cottonwood species, we found that the nitrogen and salicortin concentrations were up to 45% greater and lignin concentration 14% lower in the juvenile resprout growth of felled trees than the juvenile growth on unfelled trees (six of seven analyses were significant for P. fremontii and four of six were significant for P. angustifolia). (3) With two cottonwood species, arthropod community composition on juvenile branches differed significantly between felled and unfelled trees, with up to 38% greater species richness, 114% greater relative abundance and 1282% greater species diversity on felled trees (six of seven analyses with P. fremontii and four of six analyses with P. angustifolia were significant). The above findings indicate that the highest arthropod diversity is achieved in the heterogenous stands of mixed felled and unfelled trees than in stands of cottonwoods, where beavers are not present. These results also indicate that beaver herbivory changes the chemical composition in 10 out of 13 chemical traits in the juvenile growth of two of the three cottonwood species to potentially allow better defense against future beaver herbivory. (4) With P. deltoides, only one of five analyses in chemistry was significant, and none of the four arthropod community analyses were significant, suggesting that this species and its arthropod community responds differently to beaver. Potential reasons for these differences are unknown. Overall, our findings suggest that in addition to their impact on riparian vegetation, other mammals, birds, and aquatic organisms, beavers also may define the arthropod communities of two of three foundation tree species in these riparian ecosystems. 

Plant resource allocation patterns often reveal tradeoffs that favor growth (G) over defense (D), or vice versa. Ecologists most often explain G–D tradeoffs through principles of economic optimality, in which negative trait correlations are attributed to the reconciliation of fitness costs. Recently, researchers in molecular biology have developed ‘big data’ resources including multi‐omic (e.g. transcriptomic, proteomic and metabolomic) studies that describe the cellular processes controlling gene expression in model species. In this synthesis, we bridge ecological theory with discoveries in multi‐omics biology to better understand how selection has shaped the mechanisms of G–D tradeoffs. Multi‐omic studies reveal strategically coordinated patterns in resource allocation that are enabled by phytohormone crosstalk and transcriptional signal cascades. Coordinated resource allocation justifies the framework of optimality theory, while providing mechanistic insight into the feedbacks and control hubs that calibrate G–D tradeoff commitments. We use the existing literature to describe the coordinated resource allocation hypothesis (CoRAH) that accounts for balanced cellular controls during the expression of G–D tradeoffs, while sustaining stored resource pools to buffer the impacts of future stresses. The integrative mechanisms of the CoRAH unify the supply‐ and demand‐side perspectives of previous G–D tradeoff theories.

 

Condensed tannins (CTs) are proanthocyanidin heteropolymers that are widely distributed among plants. Their biochemical properties are determined by molecular structure (e.g. polymer size, hydroxylation, stereochemistry). InPopulus, genetically and environmentally‐determined CT concentrations have been related to ecological effects, while the potential role of CT molecular structure has received little attention.

Evaluate CT polymerisation, major constituent monomers, stereochemistry and overall content inPopulus tremuloidesfoliage using ultra‐high‐performance liquid chromatography with photodiode array and mass spectrometry (UPLC‐PDA‐(−)esi‐MS) detection following thiolytic depolymerisation of the CTs.

CTs were extracted from dried foliage of sixP. tremuloidesgenotypes into methanol and thiolytically depolymerised into constituent monomers. Calibration standards were prepared by thiolysis of CT mixtures isolated fromP. tremuloidesfoliage on Sephadex LH‐20, followed by preparative high‐performance liquid chromatography (HPLC).

Populus tremuloidesCTs contained predominantly repeating subunits of three putative stereoisomers each of catechin and gallocatechin. Linear calibrations for standards of these subunits and their thioethers (purities 44–87%, UPLC‐(−)esi‐MS) were generally stable over the course of 10 months. CT polymer size, hydroxylation, stereochemistry and concentrations differed among genotypes.

This thiolysis‐UPLC‐PDA‐(−)esiMS method was optimised for analysis of CT polymer size, hydroxylation, stereochemistry, and total concentration inPopulusfoliage. It revealed significant variation in each of these properties amongP. tremuloidesgenotypes, and will facilitate evaluation of how environmental factors affect CT molecular structures.

 

The ability to tolerate neighboring plants (i.e. degree of competitive response) is a key determinant of plant success in high‐competition environments. Plant genotypes adjust their functional trait expression under high levels of competition, which may help explain intra‐specific variation in competitive response. However, the relationships between traits and competitive response are not well understood, especially in trees. In this study, we investigated among‐genotype associations between tree trait plasticity and competitive response.

We manipulated competition intensity in experimental stands of trembling aspen (Populus tremuloides) to address the covariance between competition‐induced changes in functional trait expression and aspects of competitive ability at the genotype level.

Genotypic variation in the direction and magnitude of functional trait responses, especially those of crown foliar mass, phytochemistry, and leaf physiology, was associated with genotypic variation in competitive response. Traits exhibited distinct plastic responses to competition, with varying degrees of genotypic variation and covariance with other trait responses.

The combination of genotypic diversity and covariance among functional traits led to tree responses to competition that were coordinated among traits yet variable among genotypes. Such relationships between tree traits and competitive success have the potential to shape stand‐level trait distributions over space and time.

 

Climate change is threatening the persistence of many tree species via independent and interactive effects on abiotic and biotic conditions. In addition, changes in temperature, precipitation, and insect attacks can alter the traits of these trees, disrupting communities and ecosystems. For foundation species such asPopulus, phytochemical traits are key mechanisms linking trees with their environment and are likely jointly determined by interactive effects of genetic divergence and variable environments throughout their geographic range. Using reciprocal Fremont cottonwood (Populus fremontii) common gardens along a steep climatic gradient, we explored how environment (garden climate and simulated herbivore damage) and genetics (tree provenance and genotype) affect both foliar chemical traits and the plasticity of these traits. We found that (1) Constitutive and plastic chemical responses to changes in garden climate and damage varied among defense compounds, structural compounds, and leaf nitrogen. (2) For both defense and structural compounds, plastic responses to different garden climates depended on the climate in which a population or genotype originated. Specifically, trees originating from cool provenances showed higher defense plasticity in response to climate changes than trees from warmer provenances. (3) Trees from cool provenances growing in cool garden conditions expressed the lowest constitutive defense levels but the strongest induced (plastic) defenses in response to damage. (4) The combination of hot garden conditions and simulated herbivory switched the strategy used by these genotypes, increasing constitutive defenses but erasing the capacity for induction after damage. Because Fremont cottonwood chemistry plays a major role in shaping riparian communities and ecosystems, the effects of changes in phytochemical traits can be wide reaching. As the southwestern US is confronted with warming temperatures and insect outbreaks, these results improve our capacity to predict ecosystem consequences of climate change and inform selection of tree genotypes for conservation and restoration purposes.

 

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.