Natural soil microbiome variation affects spring foliar phenology with consequences for plant productivity and climate-driven range shifts.

Identifying the potential for natural soil microbial communities to predictably affect complex plant traits is an important frontier in climate change research. Plant phenology varies with environmental and genetic factors, but few studies have examined whether the soil microbiome interacts with plant population differentiation to affect phenology and ecosystem function. We compared soil microbial variation in a widespread tree species (Populus angustifolia) with different soil inoculum treatments in a common garden environment to test how the soil microbiome affects spring foliar phenology and subsequent biomass growth. We hypothesized and show that soil bacterial and fungal communities vary with tree conditioning from different populations and elevations, that this soil community variation influences patterns of foliar phenology and plant growth across populations and elevation gradients, and that transferring lower elevation plant genotypes to higher elevation soil communities delayed foliar phenology, thereby shortening the growing season and reducing annual biomass production. Our findings show the importance of plant-soil interactions that help shape the timing of tree foliar phenology and productivity. These geographic patterns in plant population × microbiome interactions also broaden our understanding of how soil communities impact plant phenotypic variation across key climate change gradients, with consequences for ecosystem functioning.

Climate-driven reduction of genetic variation in plant phenology alters soil communities and nutrient pools.

We examined the hypothesis that climate-driven evolution of plant traits will influence associated soil microbiomes and ecosystem function across the landscape. Using a foundation tree species, Populus angustifolia, observational and common garden approaches, and a base population genetic collection that spans 17 river systems in the western United States, from AZ to MT, we show that (a) as mean annual temperature (MAT) increases, genetic and phenotypic variation for bud break phenology decline; (b) soil microbiomes, soil nitrogen (N), and soil carbon (C) vary in response to MAT and conditioning by trees; and (c) with losses of genetic variation due to warming, population-level regulation of community and ecosystem functions strengthen. These results demonstrate a relationship between the potential evolutionary response of populations and subsequent shifts in ecosystem function along a large temperature gradient.

Genetics-based interactions of foundation species affect community diversity, stability and network structure.

We examined the hypothesis that genetics-based interactions between strongly interacting foundation species, the tree Populus angustifolia and the aphid Pemphigus betae, affect arthropod community diversity, stability and species interaction networks of which little is known. In a 2-year experimental manipulation of the tree and its aphid herbivore four major findings emerged: (i) the interactions of these two species determined the composition of an arthropod community of 139 species; (ii) both tree genotype and aphid presence significantly predicted community diversity; (iii) the presence of aphids on genetically susceptible trees increased the stability of arthropod communities across years; and (iv) the experimental removal of aphids affected community network structure (network degree, modularity and tree genotype contribution to modularity). These findings demonstrate that the interactions of foundation species are genetically based, which in turn significantly contributes to community diversity, stability and species interaction networks. These experiments provide an important step in understanding the evolution of Darwin's 'entangled bank', a metaphor that characterizes the complexity and interconnectedness of communities in the wild.

Phylogeny is a powerful tool for predicting plant biomass responses to nitrogen enrichment.

Increasing rates of anthropogenic nitrogen (N) enrichment to soils often lead to the dominance of nitrophilic plant species and reduce plant diversity in natural ecosystems. Yet, we lack a framework to predict which species will be winners or losers in soil N enrichment scenarios, a framework that current literature suggests should integrate plant phylogeny, functional tradeoffs, and nutrient co-limitation. Using a controlled fertilization experiment, we quantified biomass responses to N enrichment for 23 forest tree species within the genus Eucalyptus that are native to Tasmania, Australia. Based on previous work with these species' responses to global change factors and theory on the evolution of plant resource-use strategies, we hypothesized that (1) growth responses to N enrichment are phylogenetically structured, (2) species with more resource-acquisitive functional traits have greater growth responses to N enrichment, and (3) phosphorus (P) limits growth responses to N enrichment differentially across species, wherein P enrichment increases growth responses to N enrichment more in some species than others. We built a hierarchical Bayesian model estimating effects of functional traits (specific leaf area, specific stem density, and specific root length) and P fertilization on species' biomass responses to N, which we then compared between lineages to determine whether phylogeny explains variation in responses to N. In concordance with literature on N limitation, a majority of species responded strongly and positively to N enrichment. Mean responses ranged three-fold, from 6.21 (E. pulchella) to 16.87 (E. delegatensis) percent increases in biomass per g N·m-2 ·yr-1 added. We identified a strong difference in responses to N between two phylogenetic lineages in the Eucalyptus subgenus Symphyomyrtus, suggesting that shared ancestry explains variation in N limitation. However, our model indicated that after controlling for phylogenetic non-independence, eucalypt responses to N were not associated with functional traits (although post-hoc analyses show a phylogenetic pattern in specific root length similar to that of responses to N), nor were responses differentially limited by P. Overall, our model results suggest that phylogeny is a powerful predictor of winners and losers in anthropogenic N enrichment scenarios in Tasmanian eucalypts, which may have implications for other species.

Phylogeny Explains Variation in The Root Chemistry of Eucalyptus Species.

Plants are dependent on their root systems for survival, and thus are defended from belowground enemies by a range of strategies, including plant secondary metabolites (PSMs). These compounds vary among species, and an understanding of this variation may provide generality in predicting the susceptibility of forest trees to belowground enemies and the quality of their organic matter input to soil. Here, we investigated phylogenetic patterns in the root chemistry of species within the genus Eucalyptus. Given the known diversity of PSMs in eucalypt foliage, we hypothesized that (i) the range and concentrations of PSMs and carbohydrates in roots vary among Eucalyptus species, and (ii) that phylogenetic relationships explain a significant component of this variation. To test for interspecific variation in root chemistry and the influence of tree phylogeny, we grew 24 Eucalyptus species representing two subgenera (Eucalyptus and Symphyomyrtus) in a common garden for two years. Fine root samples were collected from each species and analyzed for total phenolics, condensed tannins, carbohydrates, terpenes, and formylated phloroglucinol compounds. Compounds displaying significant interspecific variation were mapped onto a molecular phylogeny and tested for phylogenetic signal. Although all targeted groups of compounds were present, we found that phenolics dominated root defenses and that all phenolic traits displayed significant interspecific variation. Further, these compounds displayed a significant phylogenetic signal. Overall, our results suggest that within these representatives of genus Eucalyptus, more closely related species have more similar root chemistry, which may influence their susceptibility to belowground enemies and soil organic matter accrual.

Rapid evolution and range expansion of an invasive plant are driven by provenance-environment interactions.

To improve our ability to prevent and manage biological invasions, we must understand their ecological and evolutionary drivers. We are often able to explain invasions after they happen, but our predictive ability is limited. Here, we show that range expansions of introduced Pinus taeda result from an interaction between genetic provenance and climate and that temperature and precipitation clines predict the invasive performance of particular provenances. Furthermore, we show that genotypes can occupy climate niche spaces different from those observed in their native ranges and, at least in our case, that admixture is not a main driver of invasion. Genotypes respond to climate in distinct ways, and these interactions affect the ability of populations to expand their ranges. While rapid evolution in introduced ranges is a mechanism at later stages of the invasion process, the introduction of adapted genotypes is a key driver of naturalisation of populations of introduced species.

An evolutionary case for plant rarity: Eucalyptus as a model system.

Species rarity is a common phenomenon across global ecosystems that is becoming increasingly more common under climate change. Although species rarity is often considered to be a stochastic response to environmental and ecological constraints, we examined the hypothesis that plant rarity is a consequence of natural selection acting on performance traits that affect a species range size, habitat specificity, and population aggregation; three primary descriptors of rarity. Using a common garden of 25 species of Tasmanian Eucalyptus, we find that the rarest species have 70% lower biomass than common species. Although rare species demonstrate lower biomass, rare species allocated proportionally more biomass aboveground than common species. There is also a negative phylogenetic autocorrelation underlying the biomass of rare and common species, indicating that traits associated with rarity have diverged within subgenera as a result of environmental factors to reach different associated optima. In support of our hypothesis, we found significant positive relationships between species biomass, range size and habitat specificity, but not population aggregation. These results demonstrate repeated convergent evolution of the trait-based determinants of rarity across the phylogeny in Tasmanian eucalypts. Furthermore, the phylogenetically driven patterns in biomass and biomass allocation seen in rare species may be representative of a larger plant strategy, not yet considered, but offering a mechanism as to how rare species continue to persist despite inherent constraints of small, specialized ranges and populations. These results suggest that if rarity can evolve and is related to plant traits such as biomass, rather than a random outcome of environmental constraints, we may need to revise conservation efforts in these and other rare species to reconsider the abiotic and biotic factors that underlie the distributions of rare plant species.

Evolution of rarity and phylogeny determine above- and belowground biomass in plant-plant interactions.

Rare species are often considered inferior competitors due to occupancy of small ranges, specific habitats, and small local populations. However, the phylogenetic relatedness and rarity level (level 1-7 and common) of interacting species in plant-plant interactions are not often considered when predicting the response of rare plants in a biotic context. We used a common garden of 25 species of Tasmanian Eucalyptus, to differentiate non-additive patterns in the biomass of rare versus common species when grown in mixtures varying in phylogenetic relatedness and rarity. We demonstrate that rare species maintain progressively positive non-additive responses in biomass when interacting with phylogenetically intermediate, less rare and common species. This trend is not reflected in common species that out-performed in monocultures compared to mixtures. These results offer predictability as to how rare species' productivity will respond within various plant-plant interactions. However, species-specific interactions, such as those involving E. globulus, yielded a 97% increase in biomass compared to other species-specific interaction outcomes. These results are important because they suggest that plant rarity may also be shaped by biotic interactions, in addition to the known environmental and population factors normally used to describe rarity. Rare species may utilize potentially facilitative interactions with phylogenetically intermediate and common species to escape the effects of limiting similarity. Biotically mediated increases in rare plant biomass may have subsequent effects on the competitive ability and geographic occurrence of rare species, allowing rare species to persist at low abundance across plant communities. Through the consideration of species rarity and evolutionary history, we can more accurately predict plant-plant interaction dynamics to preserve unique ecosystem functions and fundamentally challenge what it means to be "rare".

Above- and belowground fungal biodiversity of Populus trees on a continental scale.

Understanding drivers of terrestrial fungal communities over large scales is an important challenge for predicting the fate of ecosystems under climate change and providing critical ecological context for bioengineering plant-microbe interactions in model systems. We conducted an extensive molecular and microscopy field study across the contiguous United States measuring natural variation in the Populus fungal microbiome among tree species, plant niche compartments and key symbionts. Our results show clear biodiversity hotspots and regional endemism of Populus-associated fungal communities explained by a combination of climate, soil and geographic factors. Modelling climate change impacts showed a deterioration of Populus mycorrhizal associations and an increase in potentially pathogenic foliar endophyte diversity and prevalence. Geographic differences among these symbiont groups in their sensitivity to environmental change are likely to influence broader forest health and ecosystem function. This dataset provides an above- and belowground atlas of Populus fungal biodiversity at a continental scale.

Welcome to the neighbourhood: interspecific genotype by genotype interactions in Solidago influence above- and belowground biomass and associated communities.

Intra- and interspecific plant-plant interactions are fundamental to patterns of community assembly and to the mixture effects observed in biodiversity studies. Although much research has been conducted at the species level, very little is understood about how genetic variation within and among interacting species may drive these processes. Using clones of both Solidago altissima and Solidago gigantea, we found that genotypic variation in a plant's neighbours affected both above- and belowground plant traits, and that genotype by genotype interactions between neighbouring plants impacted associated pollinator communities. The traits for which focal plant genotypic variation explained the most variation varied by plant species, whereas neighbour genotypic variation explained the most variation in coarse root biomass. Our results provide new insight into genotypic and species diversity effects in plant-neighbour interactions, the extended consequences of diversity effects, and the potential for evolution in response to competitive or to facilitative plant-neighbour interactions.

Genetic components to belowground carbon fluxes in a riparian forest ecosystem: a common garden approach.

Soil carbon dioxide (CO(2)) efflux is a major component of terrestrial carbon (C) cycles; yet, the demonstration of covariation between overstory tree genetic-based traits and soil C flux remains a major frontier in understanding biological controls over soil C. Here, we used a common garden with two native tree species, Populus fremontii and P. angustifolia, and their naturally occurring hybrids to test the predictability of belowground C fluxes on the basis of taxonomic identity and genetic marker composition of replicated clones of individual genotypes. Three patterns emerged: soil CO(2) efflux and ratios of belowground flux to aboveground productivity differ by as much as 50-150% as a result of differences in clone identity and cross type; on the basis of Mantel tests of molecular marker matrices, we found that c. 30% of this variation was genetically based, in which genetically similar trees support more similar soil CO(2) efflux under their canopies than do genetically dissimilar trees; and the patterns detected in an experimental garden match observations in the wild, and seem to be unrelated to measured abiotic factors. Our findings suggest that the genetic makeup of the plants growing on soil has a significant influence on the release of C from soils to the atmosphere.

Aphid and ladybird beetle abundance depend on the interaction of spatial effects and genotypic diversity.

Intraspecific variation and genotypic diversity of host-plants can affect the structure of associated arthropod communities and the dynamics of populations. Similarly, neighboring plants can also affect interactions between host-plants and their associated arthropods. However, most studies on the effects of host-plant genotypes have largely ignored the potential effects of neighboring host-plants on arthropod communities. In this study, we used a common garden experiment to ask how spatial effects of neighboring patches, along with genotype identity and genotypic diversity in tall goldenrod (Solidago altissima), affect the abundances of a common goldenrod herbivore (Uroleucon nigrotuberculatum) and their dominant predator (Harmonia axyridis, a ladybird beetle). Aphid abundance varied 80-fold among genotypes, while ladybird beetle abundance was not affected by genotype identity. Additionally, there were strong effects of neighboring plots: aphid abundance in a focal plot was positively correlated to aphid abundance in nearby plots, suggesting strong spatial patterning in the abundance of aphids. Neither aphid nor ladybird beetle abundance was affected by genotypic diversity. However, focal plot genotypic diversity mediated the strength of the neighborhood effect (i.e., strong effects for genotype polyculture focal plots and weak effects for genotype monoculture focal plots). Our results show that aphids were directly influenced by host-plant genotype identity while ladybird beetles responded mainly to prey abundance, and suggest that genotypic diversity can influence the effects of spatial processes on the plant-herbivore interactions.

Stacked distribution models predict climate-driven loss of variation in leaf phenology at continental scales.

Climate change is having profound effects on species distributions and is likely altering the distribution of genetic variation across landscapes. Maintaining population genetic diversity is essential for the survival of species facing rapid environmental change, and variation loss will further ecological and evolutionary change. We used trait values of spring foliar leaf-out phenology of 400 genotypes from three geographically isolated populations of Populus angustifolia grown under common conditions, in concert with stacked species distribution modeling, to ask: (a) How will climate change alter phenological variation across the P. angustifolia species-range, and within populations; and (b) will the distribution of phenological variation among and within populations converge (become more similar) in future climatic conditions? Models predicted a net loss of phenological variation in future climate scenarios on 20-25% of the landscape across the species' range, with the trailing edge population losing variation on as much as 47% of the landscape. Our models also predicted that population's phenological trait distributions will become more similar over time. This stacked distribution model approach allows for the identification of areas expected to experience the greatest loss of genetically based functional trait variation and areas that may be priorities to conserve as future genetic climate refugia.

Aggregate population-level models informed by genetics predict more suitable habitat than traditional species-level model across the range of a widespread riparian tree.

Identifying and predicting how species ranges will shift in response to climate change is paramount for conservation and restoration. Ecological niche models are the most common method used to estimate potential distributions of species; however, they traditionally omit knowledge of intraspecific variation that can allow populations to respond uniquely to change. Here, we aim to test how population X environment relationships influence predicted suitable geographic distributions by comparing aggregated population-level models with species-level model predictions of suitable habitat within population ranges and across the species' range. We also test the effect of two variable selection methods on these predictions-both addressing the possibility of local adaptation: Models were built with (a) a common set, and number, of predictors and, (b) a unique combination and number of predictors specific to each group's training extent. Our study addresses the overarching hypothesis that populations have unique environmental niches, and specifically that (1) species-level models predict more suitable habitat within the ranges of genetic populations than individual models built from those groups, particularly when compared models are built with the same set of environmental predictors; and (2) aggregated genetic population models predict more suitable habitat across the species' range than the species-level model, an = d this difference will increase when models are trained with individualized predictors. We found the species models predicted more habitat within population ranges for two of three genetic groups regardless of variable selection, and that aggregated population models predicted more habitat than species' models, but that individualized predictors increased this difference. Our study emphasizes the extent to which changes to model predictions depend on the inclusion of genetic information and on the type and selection of predictors. Results from these modeling decisions can have broad implications for predicting population-level ecological and evolutionary responses to climate change.

Soil biota drive expression of genetic variation and development of population-specific feedbacks in an invasive plant.

Invasive plant species alter soils in ways that may affect the success of subsequent generations, creating plant-soil feedbacks. Ailanthus altissima is an invasive tree introduced two centuries ago to North America. We hypothesized that geographically distinct populations of A. altissima have established feedbacks specific to their local environment, due to soil communities cultivated by A. altissima. We collected seeds and soils from three populations in the eastern United States, and in the greenhouse reciprocally planted all families in all collected soils as well as in a control mixed soil, and in soils that had been irradiated for sterilization. There were positive plant-soil feedbacks for two populations in the live field-collected soils, but strong negative feedbacks for the third population. There were no population-level performance differences or feedbacks in the sterilized population locale soils, supporting a soil biotic basis for feedbacks and for the expression of genetic differentiation in A. altissima. If populations of Ailanthus altissima vary in the extent to which they benefit from and promote these plant-soil biota feedbacks, the interaction between invader and invaded community may be more important in determining the course of invasion than are the characteristics of either alone.

Climate-driven divergence in plant-microbiome interactions generates range-wide variation in bud break phenology.

Soil microbiomes are rapidly becoming known as an important driver of plant phenotypic variation and may mediate plant responses to environmental factors. However, integrating spatial scales relevant to climate change with plant intraspecific genetic variation and soil microbial ecology is difficult, making studies of broad inference rare. Here we hypothesize and show: 1) the degree to which tree genotypes condition their soil microbiomes varies by population across the geographic distribution of a widespread riparian tree, Populus angustifolia; 2) geographic dissimilarity in soil microbiomes among populations is influenced by both abiotic and biotic environmental variation; and 3) soil microbiomes that vary in response to abiotic and biotic factors can change plant foliar phenology. We show soil microbiomes respond to intraspecific variation at the tree genotype and population level, and geographic variation in soil characteristics and climate. Using a fully reciprocal plant population by soil location feedback experiment, we identified a climate-based soil microbiome effect that advanced and delayed bud break phenology by approximately 10 days. These results demonstrate a landscape-level feedback between tree populations and associated soil microbial communities and suggest soil microbes may play important roles in mediating and buffering bud break phenology with climate warming, with whole ecosystem implications.

A genetic basis to community repeatability and stability.

Recent studies have shown that genetically based traits of plants can structure associated arthropod and microbial communities, but whether the effects are consistent and repeatable across years is unknown. If communities are both heritable (i.e., related individuals tend to support similar communities) and repeatable (i.e., the same patterns observed over multiple years), then plant genetics may also affect community properties previously thought to be emergent, such as "stability." Using replicated clones of narrowleaf cottonwood (Populus angustifolia) and examining an arthropod community of 103 species, we found that (1) individual tree genotypes supported significantly different arthropod communities, which exhibited broad-sense heritability; (2) these findings were highly repeatable over three consecutive years (repeatability = 0.91) indicating that community responses to individual tree genotypes are consistent from year to year; (3) differences among tree genotypes in community stability (i.e., changes in community composition over multiple years) exhibited broad-sense heritability (H(C)2 = 0.32). In combination, these findings suggest that an emergent property such as stability can be genetically based and thus subject to natural selection.

Plant genetic variation drives geographic differences in atmosphere-plant-ecosystem feedbacks.

The objective of this study was to understand how genetic variation in a riparian species, Populus angustifolia, affects mass and energy exchange between the land and atmosphere across ~1,700 km of latitude of the western United States. To examine the potential for large-scale land-atmosphere feedbacks in hydrologic processes driven by geographic differences in plant population traits, we use a physical hydrology model, paired field, and greenhouse observations of plant traits, and stable isotope compositions of soil, stem, and leaf water of P. angustifolia populations. Populations show patterns of local adaptation in traits related to landscape hydrologic functioning-a 47% difference in stomatal density in greenhouse conditions and a 74% difference in stomatal ratio in the field. Trait and stable isotope differences reveal that populations use water differently which is related to historical landscape hydrologic functioning (evapotranspiration and streamflow). Overall, results suggest that populations from landscapes with different hydrologic histories will differ in their ability to maintain favorable water balance with changing atmospheric demands for water, with ecosystem consequences.

Intraspecific trait variation across elevation predicts a widespread tree species' climate niche and range limits.

Global change is widely altering environmental conditions which makes accurately predicting species range limits across natural landscapes critical for conservation and management decisions. If climate pressures along elevation gradients influence the distribution of phenotypic and genetic variation of plant functional traits, then such trait variation may be informative of the selective mechanisms and adaptations that help define climatic niche limits. Using extensive field surveys along 16 elevation transects and a large common garden experiment, we tested whether functional trait variation could predict the climatic niche of a widespread tree species (Populus angustifolia) with a double quantile regression approach. We show that intraspecific variation in plant size, growth, and leaf morphology corresponds with the species' total climate range and certain climatic limits related to temperature and moisture extremes. Moreover, we find evidence of genetic clines and phenotypic plasticity at environmental boundaries, which we use to create geographic predictions of trait variation and maximum values due to climatic constraints across the western US. Overall, our findings show the utility of double quantile regressions for connecting species distributions and climate gradients through trait-based mechanisms. We highlight how new approaches like ours that incorporate genetic variation in functional traits and their response to climate gradients will lead to a better understanding of plant distributions as well as identifying populations anticipated to be maladapted to future environments.

A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences.

Knowledge of the manner in which genetic variation within a tree species affects associated communities and ecosystem processes across its entire range is important for understanding how geographic mosaics of genetic interactions might develop and support different communities. While numerous studies have investigated the community and ecosystem consequences of genetic variation at the hybrid cross type or genotype level within a species, none has investigated the community-level effects of intraspecific genetic variation across the geographic range of a widespread species. This is the scale at which geographic mosaics of coevolution are hypothesized to exist. Studies at this level are particularly important for foundation tree species, which typically support numerous microbial, fungal, plant, and animal communities. We studied genetic variation across eight geographical races of the forest tree Eucalyptus globulus representing its natural distribution across southeastern Australia. The study was conducted in a 15-year-old common garden trial based on families derived from single-tree open-pollinated seed collections from the wild. Neutral molecular genetic variation within E. globulus was also assessed and compared with genetic divergence in the phenotypic and community traits. Three major findings emerged. First, we found significant genetically based, hierarchical variation in associated communities corresponding to geographical races of E. globulus and families within races. Second, divergence in foliar communities at the racial level was associated with genetically based divergence in specific leaf morphological and chemical traits that have known defensive functions. Third, significant positive correlations between canopy community dissimilarity and both neutral molecular genetic and leaf quantitative genetic dissimilarity at the race level supported a genetic similarity rule. Our results argue that genetic variation within foundation tree species has the potential to be a significant driver of the geographical mosaics of variation typical of forest communities, which could have important ecological and evolutionary implications.