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Climate means and variability are shifting rapidly, leading to mismatches between climate and locally adapted plant traits. Phenotypic plasticity, the ability of a plant to respond to environmental conditions within a lifetime, may provide a buffer for plants to persist under increasing temperature and water stress. We used two reciprocal common gardens across a steep temperature gradient to investigate plasticity in six populations of Fremont cottonwood, an important foundation tree species in arid riparian ecosystems. We investigated two components of leaf hydraulic architecture: leaf venation and stomatal morphology, both of which regulate leaf water potential and photosynthesis. These traits will likely affect plant performance under climate stressors, but it is unclear whether they are controlled by genetic or environmental factors, and whether they respond to the environment in parallel or independent directions. We found that: 1) Populations had divergent responses to a hotter growing environment, increasing or decreasing vein density. 2) Populations showed surprisingly independent responses of venation vs. stomatal traits. 3) As a result of these different responses, plasticity in hydraulic architecture traits was not predictable from historic climate conditions at population source locations, and often varied substantially within populations. 4) Hydraulic architecture was clearly linked to growth, with higher vein and stomatal density predicting greater tree growth in the hottest growing environment. However, higher plasticity in these traits did not increase average growth across multiple environments. Thus, P. fremontii populations and genotypes vary in their capacity to adjust their leaf hydraulic architecture and support growth in contrasting environments, but that this plasticity is not clearly predictable or beneficial. Identifying genotypes suitable for future conditions will depend on the relative importance of multiple traits, and on both evolutionary and ecological responses to changing temperature and water availability. 

IntroductionClimate change has increased the need for forest restoration, but low planting success and limited availability of planting materials hamper these efforts. Invasive plants and their soil legacies can further reduce restoration success. Thus, strategies that optimize restoration are crucial. Assisted migration and inoculation with native microbial symbiont communities have great potential to increase restoration success. However, assisted migrants can still show reduced survival compared to local provenances depending on transfer distance. Inoculation with mycorrhizal fungi, effective if well-matched to plants and site conditions, can have neutral to negative results with poor pairings. Few studies have examined the interaction between these two strategies in realistic field environments where native plants experience the combined effects of soil legacies left by invasive plants and the drought conditions that result from a warming, drying climate. MethodsWe planted two ecotypes (local climate and warmer climate) ofPopulus fremontii(Fremont cottonwoods), in soils with and without legacies of invasion byTamarixspp. (tamarisk), and with and without addition of native mycorrhizal fungi and other soil biota from the warmer climate. ResultsFour main results emerged. 1) First year survival in soil legacies left behind after tamarisk invasion and removal was less than one tenth of survival in soil without a tamarisk legacy. 2) Actively restoring soil communities after tamarisk removal tripled first year cottonwood survival for both ecotypes, but only improved survival of the warmer, assisted migrant ecotype trees in year two. 3) Actively restoring soil communities in areas without a tamarisk history reduced first year survival for both ecotypes, but improved survival of the warmer, assisted migrant ecotype trees in year two. 4) By the second year, inoculated assisted migrants survived at five times the rate of inoculated trees from the local ecotype. DiscussionResults emphasize the detrimental effects of soil legacies left after tamarisk invasion and removal, the efficacy of assisted migration and restoring soil communities alongside plants, and the need to thoughtfully optimize pairings between plants, fungi, and site conditions. 

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 0.77 and 0.66, 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. 

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 nitrogen. 2) For both defense and structural compounds, plastic responses to garden climate depended on the climate in which a population or genotype evolved. Specifically, trees originating from cool provenances showed higher defense plasticity in response to climate changes than trees from hotter provenances. 3) Trees from cool provenances growing in cool conditions expressed the lowest constitutive defense levels but the strongest induced (plastic) defenses. 4) The combination of hot growing conditions and simulated herbivory switched the strategy used by these genotypes, increasing constitutive defenses but erasing the capacity for induction. Because Fremont cottonwood chemistry plays a major role in shaping riparian communities and ecosystems in the southwestern US, 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. 

Efforts to maintain the function of critical ecosystems under climate change often begin with foundation species. In the southwestern US, 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 12oC 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. 

Abstract 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. 

Abstract 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. 

Mycorrhizal restoration benefits are widely acknowledged, yet factors underpinning this success remain unclear. To illuminate when natural regeneration might be sufficient, we investigated the degree mycorrhizal fungi would colonizePopulus fremontii(Fremont cottonwood) 2 years after the restoration of a riparian corridor, in the presence of an adjacent source. We compared colonization levels across plant populations and ecotypes, and from trees in the planted area to those in natural source populations. Four findings contribute to the theory and application of host–symbiont interactions. (1) Median ectomycorrhizal colonization of trees in the planted area was less than one‐tenth of that within natural source populations (p < 0.05), suggesting that even with adjacent intact habitat, sluggish regeneration would make proactive mycorrhizal restoration beneficial. (2) Within the planted area, median ectomycorrhizal and arbuscule colonization of trees sourced from greater distances were less than one‐third of that for trees sourced locally (p < 0.05), suggesting translocation poses barriers to symbioses. (3) Changes in colonization did not align with plant ecotypes, suggesting that geographic scales of selection for plants and fungi differ. (4) Slight increases in median mycorrhizal colonization (from 0% to 5%) were strongly correlated with increased survival for the plant provenance with lowest survival (r² = 46% andr_s = 48%,p < 0.05), suggesting mycorrhizae are particularly beneficial when plants are under stress (including translocation‐induced stress). This study is novel in demonstrating that mycorrhizal regeneration is slow even in the presence of adjacent intact habitat, and that when colonization could seem negligible, it may still have biological significance. 

Abstract 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.