Limits of thermal and hydrological tolerance in a foundation tree species (Populus fremontii) in the desert southwestern United States.

Populus fremontii is among the most dominant, and ecologically important riparian tree species in the western United States and can thrive in hyper-arid riparian corridors. Yet, P. fremontii forests have rapidly declined over the last decade, particularly in places where temperatures sometimes exceed 50°C. We evaluated high temperature tolerance of leaf metabolism, leaf thermoregulation, and leaf hydraulic function in eight P. fremontii populations spanning a 5.3°C mean annual temperature gradient in a well-watered common garden, and at source locations throughout the lower Colorado River Basin. Two major results emerged. First, despite having an exceptionally high Tcrit (the temperature at which Photosystem II is disrupted) relative to other tree taxa, recent heat waves exceeded Tcrit , requiring evaporative leaf cooling to maintain leaf-to-air thermal safety margins. Second, in midsummer, genotypes from the warmest locations maintained lower midday leaf temperatures, a higher midday stomatal conductance, and maintained turgor pressure at lower water potentials than genotypes from more temperate locations. Taken together, results suggest that under well-watered conditions, P. fremontii can regulate leaf temperature below Tcrit along the warm edge of its distribution. Nevertheless, reduced Colorado River flows threaten to lower water tables below levels needed for evaporative cooling during episodic heat waves.

Provenance, genotype, and flooding influence growth and resource acquisition characteristics in a clonal, riparian shrub.

PREMISE: Riparian plants can exhibit intraspecific phenotypic variability across the landscape related to temperature and flooding gradients. Phenotypes that vary across a climate gradient are often partly genetically determined and may differ in their response to inundation. Changes to inundation patterns across a climate gradient could thus result in site-specific inundation responses. Phenotypic variability is more often studied in riparian trees, yet riparian shrubs are key elements of riparian systems and may differ from trees in phenotypic variability and environmental responses. METHODS: We tested whether individuals of a clonal, riparian shrub, Pluchea sericea, collected from provenances spanning a temperature gradient differed in their phenotypes and responses to inundation and to what degree any differences were related to genotype. Plants were subjected to different inundation depths and a subset genotyped. Variables related to growth and resource acquisition were measured and analyzed using hierarchical, multivariate Bayesian linear regressions. RESULTS: Individuals from different provenances differed in their phenotypes, but not in their response to inundation. Phenotypes were not related to provenance temperature but were partially governed by genotype. Growth was more strongly influenced by inundation, while resource acquisition was more strongly controlled by genotype. CONCLUSIONS: Growth and resource acquisition responses in a clonal, riparian shrub are affected by changes to inundation and plant demographics in unique ways. Shrubs appear to differ from trees in their responses to environmental change. Understanding environmental effects on shrubs separately from those of trees will be a key part of evaluating impacts of environmental change on riparian ecosystems.

Evidence of climate-driven selection on tree traits and trait plasticity across the climatic range of a riparian foundation species.

Selection on quantitative traits by heterogeneous climatic conditions can lead to substantial trait variation across a species range. In the context of rapidly changing environments, however, it is equally important to understand selection on trait plasticity. To evaluate the role of selection in driving divergences in traits and their associated plasticities within a widespread species, we compared molecular and quantitative trait variation in Populus fremontii (Fremont cottonwood), a foundation riparian distributed throughout Arizona. Using SNP data and genotypes from 16 populations reciprocally planted in three common gardens, we first performed QST -FST analyses to detect selection on traits and trait plasticity. We then explored the environmental drivers of selection using trait-climate and plasticity-climate regressions. Three major findings emerged: (1) There was significant genetic variation in traits expressed in each of the common gardens and in the phenotypic plasticity of traits across gardens, both of which were heritable. (2) Based on QST -FST comparisons, there was evidence of selection in all traits measured; however, this result varied from no effect in one garden to highly significant in another, indicating that detection of past selection is environmentally dependent. We also found strong evidence of divergent selection on plasticity across environments for two traits. (3) Traits and/or their plasticity were often correlated with population source climate (R2 up to .77 and .66, respectively). These results suggest that steep climate gradients across the Southwest have played a major role in shaping the evolution of divergent phenotypic responses in populations and genotypes now experiencing climate change.

Genetic divergence along a climate gradient shapes chemical plasticity of a foundation tree species to both changing climate and herbivore damage.

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 as Populus, 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.

Simulating selection and evolution at the community level using common garden data.

A key issue in evolutionary biology is whether selection acting at levels higher than the individual can cause evolutionary change. If it can, then conceptual and empirical studies must consider how selection operates at multiple levels of biological organization. Here, we test the hypothesis that estimates of broad-sense community heritability, H C 2 , can be used to predict the evolutionary response by community-level phenotypes when community-level selection is imposed. Using an approach informed by classic quantitative genetics, we made three predictions. First, when we imposed community-level selection, we expected a significant change in the average phenotype of arthropod communities associated with individual tree genotypes [we imposed selection by favoring high and low NMDS (nonmetric multidimensional scaling) scores that reflected differences in arthropod species richness, abundance and composition]. Second, we expected H C 2 to predict the magnitude of the community-level response. Third, we expected no significant change in average NMDS scores with community-level selection imposed at random. We tested these hypotheses using three years of common garden data for 102 species comprising the arthropod communities, associated with nine clonally replicated Populus angustifolia genotypes. Each of our predictions were met. We conclude that estimates of H C 2 account for the resemblance among communities sharing common ancestry, the persistence of community composition over time, and the outcome of selection when it occurs at the community level. Our results provide a means for exploring how this process leads to large-scale community evolutionary change, and they identify the circumstances in which selection may routinely act at the community level.

Tradeoffs between leaf cooling and hydraulic safety in a dominant arid land riparian tree species.

Leaf carbon gain optimization in hot environments requires balancing leaf thermoregulation with avoiding excessive water loss via transpiration and hydraulic failure. The tradeoffs between leaf thermoregulation and transpirational water loss can determine the ecological consequences of heat waves that are increasing in frequency and intensity. We evaluated leaf thermoregulation strategies in warm- (>40°C maximum summer temperature) and cool-adapted (<40°C maximum summer temperature) genotypes of the foundation tree species, Populus fremontii, using a common garden near the mid-elevational point of its distribution. We measured leaf temperatures and assessed three modes of leaf thermoregulation: leaf morphology, midday canopy stomatal conductance and stomatal sensitivity to vapour pressure deficit. Data were used to parameterize a leaf energy balance model to estimate contrasts in midday leaf temperature in warm- and cool-adapted genotypes. Warm-adapted genotypes had 39% smaller leaves and 38% higher midday stomatal conductance, reflecting a 3.8°C cooler mean leaf temperature than cool-adapted genotypes. Leaf temperatures modelled over the warmest months were on average 1.1°C cooler in warm- relative to cool-adapted genotypes. Results show that plants adapted to warm environments are predisposed to tightly regulate leaf temperatures during heat waves, potentially at an increased risk of hydraulic failure.

North American tree migration paced by climate in the West, lagging in the East.

Tree fecundity and recruitment have not yet been quantified at scales needed to anticipate biogeographic shifts in response to climate change. By separating their responses, this study shows coherence across species and communities, offering the strongest support to date that migration is in progress with regional limitations on rates. The southeastern continent emerges as a fecundity hotspot, but it is situated south of population centers where high seed production could contribute to poleward population spread. By contrast, seedling success is highest in the West and North, serving to partially offset limited seed production near poleward frontiers. The evidence of fecundity and recruitment control on tree migration can inform conservation planning for the expected long-term disequilibrium between climate and forest distribution.

Tree genotypes affect rock lichens and understory plants: examples of trophic-independent interactions.

Genetic variation in foundation tree species can strongly influence communities of trophic-dependent organisms, such as herbivorous insects, pollinators, and mycorrhizal fungi. However, the extent and manner in which this variation results in unexpected interactions that reach trophic-independent organisms remains poorly understood, even though these interactions are essential to understanding complex ecosystems. In pinyon-juniper woodland at Sunset Crater (Arizona, USA), we studied pinyon (Pinus edulis) that were either resistant or susceptible to stem-boring moths (Dioryctria albovittella). Moth herbivory alters the architecture of susceptible trees, thereby modifying the microhabitat beneath their crowns. We tested the hypothesis that this interaction between herbivore and tree genotype extends to affect trophic-independent communities of saxicolous (i.e., growing on rocks) lichens and bryophytes and vascular plants beneath their crowns. Under 30 pairs of moth-resistant and moth-susceptible trees, we estimated percent cover of lichens, bryophytes, and vascular plants. We also quantified the cover of leaf litter and rocks as well as light availability. Four major findings emerged. (1) Compared to moth-resistant trees, which exhibited monopodial architecture, the microhabitat under the shrub-like susceptible trees was 60% darker and had 21% more litter resulting in 68% less rock exposure. (2) Susceptible trees had 56% and 87% less cover, 42% and 80% less richness, and 38% and 92% less diversity of saxicolous and plant communities, respectively, compared to resistant trees. (3) Both saxicolous and plant species accumulated at a slower rate beneath susceptible trees, suggesting an environment that might inhibit colonization and/or growth. (4) Both saxicolous and plant communities were negatively affected by the habitat provided by susceptible trees. The results suggest that herbivory of moth-susceptible trees generated litter at high enough rates to reduce rock substrate availability, thereby suppressing the saxicolous communities. However, our results did not provide a causal pathway explaining the suppression of vascular plants. Nonetheless, the cascading effects of genetic variation in pinyon appear to extend beyond trophic-dependent moths to include trophic-independent saxicolous and vascular plant communities that are affected by specific tree-herbivore interactions that modify the local environment. We suggest that such genetically based interactions are common in nature and contribute to the evolution of complex communities.

Plastic responses to hot temperatures homogenize riparian leaf litter, speed decomposition, and reduce detritivores.

Efforts to maintain the function of critical ecosystems under climate change often begin with foundation species. In the southwestern United States, cottonwood trees support diverse communities in riparian ecosystems that are threatened by rising temperatures. Genetic variation within cottonwoods shapes communities and ecosystems, but these effects may be modified by phenotypic plasticity, where genotype traits change in response to environmental conditions. Here, we investigated plasticity in Fremont cottonwood (Populus fremontii) leaf litter traits as well as the consequences of plasticity for riparian ecosystems. We used three common gardens each planted with genotypes from six genetically divergent populations spanning a 12°C temperature gradient, and a decomposition experiment in a common stream environment. We found that leaf litter area, specific leaf area, and carbon to nitrogen ratio (C:N) were determined by interactions between genetics and growing environment, as was the subsequent rate of litter decomposition. Most of the genetic variation in leaf litter traits appeared among rather than within source populations with distinct climate histories. Source populations from hotter climates generally produced litter that decomposed more quickly, but plasticity varied the magnitude of this effect. We also found that hotter growing conditions reduced the variation in litter traits produced across genotypes, homogenizing the litter inputs to riparian ecosystems. All genotypes in the hottest garden produced comparatively small leaves that decomposed quickly and supported lower abundances of aquatic invertebrates, whereas the same genotypes in the coldest garden produced litter with distinct morphologies and decomposition rates. Our results suggest that plastic responses to climate stress may constrict the expression of genetic variation in predictable ways that impact communities and ecosystems. Understanding these interactions between genetic and environmental variation is critical to our ability to plan for the role of foundation species when managing and restoring riparian ecosystems in a warming world.

Genetic data improves niche model discrimination and alters the direction and magnitude of climate change forecasts.

Ecological niche models (ENMs) have classically operated under the simplifying assumptions that there are no barriers to gene flow, species are genetically homogeneous (i.e., no population-specific local adaptation), and all individuals share the same niche. Yet, these assumptions are violated for most broadly distributed species. Here, we incorporate genetic data from the widespread riparian tree species narrowleaf cottonwood (Populus angustifolia) to examine whether including intraspecific genetic variation can alter model performance and predictions of climate change impacts. We found that (1) P. angustifolia is differentiated into six genetic groups across its range from México to Canada and (2) different populations occupy distinct climate niches representing unique ecotypes. Comparing model discriminatory power, (3) all genetically informed ecological niche models (gENMs) outperformed the standard species-level ENM (3-14% increase in AUC; 1-23% increase in pROC). Furthermore, (4) gENMs predicted large differences among ecotypes in both the direction and magnitude of responses to climate change and (5) revealed evidence of niche divergence, particularly for the Eastern Rocky Mountain ecotype. (6) Models also predicted progressively increasing fragmentation and decreasing overlap between ecotypes. Contact zones are often hotspots of diversity that are critical for supporting species' capacity to respond to present and future climate change, thus predicted reductions in connectivity among ecotypes is of conservation concern. We further examined the generality of our findings by comparing our model developed for a higher elevation Rocky Mountain species with a related desert riparian cottonwood, P. fremontii. Together our results suggest that incorporating intraspecific genetic information can improve model performance by addressing this important source of variance. gENMs bring an evolutionary perspective to niche modeling and provide a truly "adaptive management" approach to support conservation genetic management of species facing global change.

Local adaptation and rapid evolution of aphids in response to genetic interactions with their cottonwood hosts.

Several studies have demonstrated the ecological consequences of genetic variation within a single plant species. For example, these studies show that individual plant genotypes support unique composition of the plants' associated arthropod community. By contrast, fewer studies have explored how plant genetic variation may influence evolutionary dynamics in the plant's associated species. Here, we examine how aphids respond evolutionarily to genetic variation in their host plant. We conducted two experiments to examine local adaptation and rapid evolution of the free-feeding aphid Chaitophorus populicola across genetic variants of its host plant, Populus angustifolia. To test for local adaptation, we collected tree cuttings and aphid colonies from three sites along an elevation/climate gradient and conducted a reciprocal transplant experiment. In general, home aphids (aphids transplanted onto trees from the same site) produced 1.7-3.4 times as many offspring as foreign aphids (aphids transplanted onto trees from different sites). To test for rapid evolution, we used 4 clonally replicated aphid genotypes and transplanted each onto 5 clonally replicated P. angustifolia genotypes. Each tree genotype started with the same aphid genotype composition. After 21 days (~two aphid generations), aphid genotype composition changed (i.e., aphids evolved) and some tree genotypes supported unique evolutionary trajectories of aphids. These results suggest that plant evolution in response to human perturbation, such as climate change and invasive species, will also result in evolutionary responses in strongly interacting species that could cascade to affect whole communities.

Adaptive capacity in the foundation tree species Populus fremontii: implications for resilience to climate change and non-native species invasion in the American Southwest.

Populus fremontii (Fremont cottonwood) is recognized as one of the most important foundation tree species in the southwestern USA and northern Mexico because of its ability to structure communities across multiple trophic levels, drive ecosystem processes and influence biodiversity via genetic-based functional trait variation. However, the areal extent of P. fremontii cover has declined dramatically over the last century due to the effects of surface water diversions, non-native species invasions and more recently climate change. Consequently, P. fremontii gallery forests are considered amongst the most threatened forest types in North America. In this paper, we unify four conceptual areas of genes to ecosystems research related to P. fremontii's capacity to survive or even thrive under current and future environmental conditions: (i) hydraulic function related to canopy thermal regulation during heat waves; (ii) mycorrhizal mutualists in relation to resiliency to climate change and invasion by the non-native tree/shrub, Tamarix; (iii) phenotypic plasticity as a mechanism for coping with rapid changes in climate; and (iv) hybridization between P. fremontii and other closely related Populus species where enhanced vigour of hybrids may preserve the foundational capacity of Populus in the face of environmental change. We also discuss opportunities to scale these conceptual areas from genes to the ecosystem level via remote sensing. We anticipate that the exploration of these conceptual areas of research will facilitate solutions to climate change with a foundation species that is recognized as being critically important for biodiversity conservation and could serve as a model for adaptive management of arid regions in the southwestern USA and around the world.

Legacy effects of tree mortality mediated by ectomycorrhizal fungal communities.

Successive droughts have resulted in extensive tree mortality in the southwestern United States. Recovery of these areas is dependent on the survival and recruitment of young trees. For trees that rely on ectomycorrhizal fungi (EMF) for survival and growth, changes in soil fungal communities following tree mortality could negatively affect seedling establishment. We used tree-focused and stand-scale measurements to examine the impact of pinyon pine mortality on the performance of surviving juvenile trees and the potential for mutualism limitation of seedling establishment via altered EMF communities. Mature pinyon mortality did not affect the survival of juvenile pinyons, but increased their growth. At both tree and stand scales, high pinyon mortality had no effect on the abundance of EMF inocula, but led to altered EMF community composition including increased abundance of Geopora and reduced abundance of Tuber. Seedling biomass was strongly positively associated with Tuber abundance, suggesting that reductions in this genus with pinyon mortality could have negative consequences for establishing seedlings. These findings suggest that whereas mature pinyon mortality led to competitive release for established juvenile pinyons, changes in EMF community composition with mortality could limit successful seedling establishment and growth in high-mortality sites.

Long-Term Studies Reveal Differential Responses to Climate Change for Trees Under Soil- or Herbivore-Related Stress.

Worldwide, trees are confronting increased temperature and aridity, exacerbating susceptibility to herbivory. Long-term studies comparing patterns of plant performance through drought can help identify variation among and within populations in vulnerability to climate change and herbivory. We use long-term monitoring data to examine our overarching hypothesis that the negative impacts of poor soil and herbivore susceptibility would be compounded by severe drought. We studied pinyon pine, Pinus edulis, a widespread southwestern tree species that has suffered extensive climate-change related mortality. We analyzed data on mortality, growth, male reproduction, and herbivory collected for 14-32 years in three areas with distinct soil-types. We used standardized precipitation-evapotranspiration index (SPEI) as a climate proxy that summarizes the impacts of drought due to precipitation and temperature variation on semi-arid forests. Several key findings emerged: (1) Plant performance measurements did not support our hypothesis that trees growing in stressful, coarse-textured soils would suffer more than trees growing in finer-textured soils. Stem growth at the area with coarse, young cinder soils (area one) responded only weakly to drought, while stem growth on more developed soils with sedimentary (area two) and volcanic (area three) substrates, was strongly negatively affected by drought. Male reproduction declined less with drought at area one and more at areas two and three. Overall mortality was 30% on coarse cinder soils (area one) and averaged 55% on finer soil types (areas two and three). (2) Although moth herbivore susceptible trees were hypothesized to suffer more with drought than moth resistant trees, the opposite occurred. Annual stem growth was negatively affected by drought for moth resistant trees, but much less strongly for moth susceptible trees. (3) In contrast to our hypothesis, moths declined with drought. Overall, chronically water-stressed and herbivore-susceptible trees had smaller declines in performance relative to less-stressed trees during drought years. These long-term findings support the idea that stressed trees might be more resistant to drought since they may have adapted or acclimated to resist drought-related mortality.

Heritable Phytohormone Profiles of Poplar Genotypes Vary in Resistance to a Galling Aphid.

Insect galls are highly specialized structures arising from atypical development of plant tissue induced by insects. Galls provide the insect enhanced nutrition and protection against natural enemies and environmental stresses. Galls are essentially plant organs formed by an intimate biochemical interaction between the gall-inducing insect and its host plant. Because galls are plant organs, their development is likely to be governed by phytohormones involved in normal organogenesis. We characterized concentrations of both growth and defensive phytohormones in ungalled control leaves and galls induced by the aphid Pemphigus betae on narrowleaf cottonwood Populus angustifolia that differ genotypically in resistance to this insect. We found that susceptible trees differed from resistant trees in constitutive concentrations of both growth and defense phytohormones. Susceptible trees were characterized by significantly higher constitutive cytokinin concentrations in leaves, significantly greater ability of aphids to elicit cytokinin increases, and significantly lower constitutive defense phytohormone concentrations than observed in resistant trees. Phytohormone concentrations in both constitutive and induced responses in galled leaves exhibited high broad-sense heritability that, respectively, ranged from 0.39 to 0.93 and from 0.28 to 0.66, suggesting that selection can act upon these traits and that they might vary across the landscape. Increased cytokinin concentrations may facilitate forming strong photosynthate sinks in the galls, a requirement for galling insect success. By characterizing for the first time the changes in 15 phytohormones belonging to five different classes, this study offers a better overview of the signaling alteration occurring in galls that has likely been important for their ecology and evolution. Copyright © 2019 The Author(s). This is an open-access article distributed under the CC BY-NC-ND 4.0 International license .

Genotypic variation in phenological plasticity: Reciprocal common gardens reveal adaptive responses to warmer springs but not to fall frost.

Species faced with rapidly shifting environments must be able to move, adapt, or acclimate in order to survive. One mechanism to meet this challenge is phenotypic plasticity: altering phenotype in response to environmental change. Here, we investigated the magnitude, direction, and consequences of changes in two key phenology traits (fall bud set and spring bud flush) in a widespread riparian tree species, Populus fremontii. Using replicated genotypes from 16 populations from throughout the species' thermal range, and reciprocal common gardens at hot, warm, and cool sites, we identified four major findings: (a) There are significant genetic (G), environmental (E), and GxE components of variation for both traits across three common gardens; (b) The magnitude of phenotypic plasticity is correlated with provenance climate, where trees from hotter, southern populations exhibited up to four times greater plasticity compared to the northern, frost-adapted populations; (c) Phenological mismatches are correlated with higher mortality as the transfer distances between provenance and garden increase; and (d) The relationship between plasticity and survival depends not only on the magnitude and direction of environmental transfer, but also on the type of environmental stress (i.e., heat or freezing), and how particular traits have evolved in response to that stress. Trees transferred to warmer climates generally showed small to moderate shifts in an adaptive direction, a hopeful result for climate change. Trees experiencing cooler climates exhibited large, non-adaptive changes, suggesting smaller transfer distances for assisted migration. This study is especially important as it deconstructs trait responses to environmental cues that are rapidly changing (e.g., temperature and spring onset) and those that are fixed (photoperiod), and that vary across the species' range. Understanding the magnitude and adaptive nature of phenotypic plasticity of multiple traits responding to multiple environmental cues is key to guiding restoration management decisions as climate continues to change.

Linking tree genetics and stream consumers: isotopic tracers elucidate controls on carbon and nitrogen assimilation.

Leaf litter provides an important nutrient subsidy to headwater streams, but little is known about how tree genetics influence energy pathways from litter to higher trophic levels. Despite the charge to quantify carbon (C) and nitrogen (N) pathways from decomposing litter, the relationship between litter decomposition and aquatic consumers remains unresolved. We measured litter preference (attachments to litter), C and N assimilation rates, and growth rates of a shredding caddisfly (Hesperophylax magnus, Limnephilidae) in response to leaf litter of different chemical and physical phenotypes using Populus cross types (P. fremontii, P. angustifolia, and F1 hybrids) and genotypes within P. angustifolia. We combined laboratory mesocosm studies using litter from a common garden with a field study using doubly labeled litter (13 C and 15 N) grown in a greenhouse and incubated in Oak Creek, Arizona, USA. We found that, in the lab, shredders initially chose relatively labile (low lignin and condensed tannin concentrations, rapidly decomposing) cross type litter, but preference changed within 4 d to relatively recalcitrant (high lignin and condensed tannin concentrations, slowly decomposing) litter types. Additionally, in the lab, shredder growth rates were higher on relatively recalcitrant compared to labile cross type litter. Over the course of a three-week field experiment, shredders also assimilated more C and N from relatively recalcitrant compared to labile cross type litter. Finally, among P. angustifolia genotypes, N assimilation by shredders was positively related to litter lignin and C:N, but negatively related to condensed tannins and decomposition rate. C assimilation was likewise positively related to litter C:N, and also to litter %N. C assimilation was not associated with condensed tannins or lignin. Collectively, these findings suggest that relatively recalcitrant litter of Populus cross types provides more nutritional benefit, in terms of N fluxes and growth, than labile litter, but among P. angustifolia genotypes the specific trait of litter recalcitrance (lignin or tannins) determines effects on C or N assimilation. As shredders provide nutrients and energy to higher trophic levels, the influence of these genetically based plant decomposition pathways on shredder preference and performance may affect community and food web structure.

Large effect quantitative trait loci for salicinoid phenolic glycosides in Populus: Implications for gene discovery.

Genomic studies have been used to identify genes underlying many important plant secondary metabolic pathways. However, genes for salicinoid phenolic glycosides (SPGs)-ecologically important compounds with significant commercial, cultural, and medicinal applications-remain largely undescribed. We used a linkage map derived from a full-sib population of hybrid cottonwoods (Populus spp.) to search for quantitative trait loci (QTL) for the SPGs salicortin and HCH-salicortin. SSR markers and primer sequences were used to anchor the map to the V3.0 P. trichocarpa genome. We discovered 21 QTL for the two traits, including a major QTL for HCH-salicortin (R2 = .52) that colocated with a QTL for salicortin on chr12. Using the V3.0 Populus genome sequence, we identified 2,983 annotated genes and 1,480 genes of unknown function within our QTL intervals. We note ten candidate genes of interest, including a BAHD-type acyltransferase that has been potentially linked to Populus SPGs. Our results complement other recent studies in Populus with implications for gene discovery and the evolution of defensive chemistry in a model genus. To our knowledge, this is the first study to use a full-sib mapping population to identify QTL intervals and gene lists associated with SPGs.

Genetic-Based Susceptibility of a Foundation Tree to Herbivory Interacts With Climate to Influence Arthropod Community Composition, Diversity, and Resilience.

Understanding how genetic-based traits of plants interact with climate to affect associated communities will help improve predictions of climate change impacts on biodiversity. However, few community-level studies have addressed such interactions. Pinyon pine (Pinus edulis) in the southwestern U.S. shows genetic-based resistance and susceptibility to pinyon needle scale (Matsucoccus acalyptus). We sought to determine if susceptibility to scale herbivory influenced the diversity and composition of the extended community of 250+ arthropod species, and if this influence would be consistent across consecutive years, an extreme drought year followed by a moderate drought year. Because scale insects alter the architecture of susceptible trees, it is difficult to separate the direct influences of susceptibility on arthropod communities from the indirect influences of scale-altered tree architecture. To separate these influences, scales were experimentally excluded from susceptible trees for 15 years creating susceptible trees with the architecture of resistant trees, hereafter referred to as scale-excluded trees. Five patterns emerged. (1) In both years, arthropod abundance was 3-4X lower on susceptible trees compared to resistant and scale-excluded trees. (2) Species accumulation curves show that alpha and gamma diversity were 2-3X lower on susceptible trees compared to resistant and scale-excluded trees. (3) Reaction norms of arthropod richness and abundance on individual tree genotypes across years showed genotypic variation in the community response to changes in climate. (4) The genetic-based influence of susceptibility on arthropod community composition is climate dependent. During extreme drought, community composition on scale-excluded trees resembled susceptible trees indicating composition was strongly influenced by tree genetics independent of tree architecture. However, under moderate drought, community composition on scale-excluded trees resembled resistant trees indicating traits associated with tree architecture became more important. (5) One year after extreme drought, the arthropod community rebounded sharply. However, there was a much greater rebound in richness and abundance on resistant compared to susceptible trees suggesting that reduced resiliency in the arthropod community is associated with susceptibility. These results argue that individual genetic-based plant-herbivore interactions can directly and indirectly impact community-level diversity, which is modulated by climate. Understanding such interactions is important for assessing the impacts of climate change on biodiversity.

Tree genetics defines fungal partner communities that may confer drought tolerance.

Plant genetic variation and soil microorganisms are individually known to influence plant responses to climate change, but the interactive effects of these two factors are largely unknown. Using long-term observational studies in the field and common garden and greenhouse experiments of a foundation tree species (Pinus edulis) and its mutualistic ectomycorrhizal fungal (EMF) associates, we show that EMF community composition is under strong plant genetic control. Seedlings acquire the EMF community of their seed source trees (drought tolerant vs. drought intolerant), even when exposed to inoculum from the alternate tree type. Drought-tolerant trees had 25% higher growth and a third the mortality of drought-intolerant trees over the course of 10 y of drought in the wild, traits that were also observed in their seedlings in a common garden. Inoculation experiments show that EMF communities are critical to drought tolerance. Drought-tolerant and drought-intolerant seedlings grew similarly when provided sterile EMF inoculum, but drought-tolerant seedlings grew 25% larger than drought-intolerant seedlings under dry conditions when each seedling type developed its distinct EMF community. This demonstration that particular combinations of plant genotype and mutualistic EMF communities improve the survival and growth of trees with drought is especially important, given the vulnerability of forests around the world to the warming and drying conditions predicted for the future.