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Despite an increased focus on multiscale relationships and interdisciplinary integration, few macroecological studies consider the contribution of genetic-based processes to landscape-scale patterns. We test the hypothesis that tree genetics, climate, and geography jointly drive continental-scale patterns of community structure, using genome-wide SNP data from a broadly distributed foundation tree species (Populus fremontii S. Watson) and two dependent communities (leaf-modifying arthropods and fungal endophytes) spanning southwestern North America. Four key findings emerged: (1) Tree genetic structure was a significant predictor for both communities; however, the strength of influence was both scale- and community-dependent. (2) Tree genetics was the primary driver for endophytes, explaining 17% of variation in continental-scale community structure, whereas (3) climate was the strongest predictor of arthropod structure (24%). (4) Power to detect tree genotype—community phenotype associations changed with scale of genetic organization, increasing from individuals to populations to ecotypes, emphasizing the need to consider nonstationarity (i.e., changes in the effects of factors on ecological processes across scales) when inferring macrosystem properties. Our findings highlight the role of foundation tree species as drivers of macroscale community structure and provide macrosystems ecology with a theoretical framework for linking fine- and intermediate-scale genetic processes to landscape-scale patterns. Management of the genetic diversity harbored within foundation species is a critical consideration for conserving and sustaining regional biodiversity. 

Evolution has been viewed as occurring primarily through selection among individuals. We present a framework based on multilevel selection for evaluating evolutionary change from individuals to communities, with supporting empirical evidence. Essential to this evaluation is the role that interspecific indirect genetic effects play in shaping community organization, in generating variation among community phenotypes, and in creating community heritability. If communities vary in phenotype, and those phenotypes are heritable and subject to selection at multiple levels, then a community view of evolution must be merged with mainstream evolutionary theory. Rapid environmental change during the Anthropocene will require a better understanding of these evolutionary processes, especially selection acting at the community level, which has the potential to eliminate whole communities while favoring others. 

Populus fremontiiis 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. fremontiiforests 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 eightP. fremontiipopulations 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 highT_crit(the temperature at which Photosystem II is disrupted) relative to other tree taxa, recent heat waves exceededT_crit, 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. fremontiican regulate leaf temperature belowT_critalong 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.

 

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 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. 

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.