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.

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.

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.

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.

Environmental variation shapes genetic variation in Bouteloua gracilis: Implications for restoration management of natural populations and cultivated varieties in the southwestern United States.

With the increasing frequency of large-scale restoration efforts, the need to understand the adaptive genetic structure of natural plant populations and their relation to heavily utilized cultivars is critical. Bouteloua gracilis (blue grama) is a wind-dispersed, perennial grass consisting of several cytotypes (2n = 2×-6×) with a widespread distribution in western North America. The species is locally dominant and used regularly in restoration treatments. Using amplified fragment length polymorphism (AFLP) and cpDNA analyses, we assessed the genetic variability and adaptive genetic structure of blue grama within and among 44 sampling sites that are representative of the species' environmental and habitat diversity in the southwestern United States. Five cultivars were also included to investigate genetic diversity and differentiation in natural versus cultivated populations. Three main findings resulted from this study: (a) Ninety-four polymorphic AFLP markers distinguished two population clusters defined largely by samples on and off the Colorado Plateau; (b) substructure of samples on the Colorado Plateau was indicated by genetic divergence between boundary and interior regions, and was supported by cytotype distribution and cpDNA analysis; and (c) six AFLP markers were identified as "outliers," consistent with being under selection. These loci were significantly correlated to mean annual temperature, mean annual precipitation, precipitation of driest quarter, and precipitation of wettest quarter in natural populations, but not in cultivated samples. Marker × environment relationships were found to be largely influenced by cytotype and cultivar development. Our results demonstrate that blue grama is genetically variable, and exhibits genetic structure, which is shaped, in part, by environmental variability across the Colorado Plateau. Information from our study can be used to guide the selection of seed source populations for commercial development and long-term conservation management of B. gracilis, which could include genetic assessments of diversity and the adaptive potential of both natural and cultivated populations for wildland restoration.

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.

Genetic analyses of Astragalus sect. Humillimi (Fabaceae) resolve taxonomy and enable effective conservation.

PREMISE OF THE STUDY: Astragalus sect. Humillimi is distributed across the southwestern United States and contains two endangered taxa, A. cremnophylax var. cremnophylax and A. humillimus. The former was originally described from the South Rim of the Grand Canyon. Analysis of individuals discovered on the North Rim of the Grand Canyon yielded some evidence that the population represented a distinct species. To enable effective conservation, we clarify the group's taxonomy and characterize the genetic diversity of A. cremnophylax and A. humillimus. METHODS: We used AFLPs to genotype most species in sect. Humillimi, focusing on the two endangered forms. We examined patterns of genetic diversity using complementary analytical approaches. KEY RESULTS: Our results demonstrate that North Rim populations group with A. c. var. cremnophylax. We found low levels of genetic diversity at certain localities and strong differentiation among populations. Astragalus humillimus, which has suffered recent and severe population declines, exhibits weak differentiation among and low diversity within populations. CONCLUSIONS: Our results clarify the taxonomy of sect. Humillimi and define the boundaries of A. c. var. cremnophylax, which is shown to inhabit both rims of the Grand Canyon. This clarification, and detailed analysis of genetic variation within both endangered taxa, may advance ongoing efforts to conserve these taxa. Our results suggest that range-wide genetic analysis of A. humillimus may inform recovery strategies for this taxon.

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.

Conserving threatened riparian ecosystems in the American West: Precipitation gradients and river networks drive genetic connectivity and diversity in a foundation riparian tree (Populus angustifolia).

Gene flow is an evolutionary process that supports genetic connectivity and contributes to the capacity of species to adapt to environmental change. Yet, for most species, little is known about the specific environmental factors that influence genetic connectivity, or their effects on genetic diversity and differentiation. We used a landscape genetic approach to understand how geography and climate influence genetic connectivity in a foundation riparian tree (Populus angustifolia), and their relationships with specieswide patterns of genetic diversity and differentiation. Using multivariate restricted optimization in a reciprocal causal modelling framework, we quantified the relative contributions of riparian network connectivity, terrestrial upland resistance and climate gradients on genetic connectivity. We found that (i) all riparian corridors, regardless of river order, equally facilitated connectivity, while terrestrial uplands provided 2.5× more resistance to gene flow than riparian corridors. (ii) Cumulative differences in precipitation seasonality and precipitation of the warmest quarter were the primary climatic factors driving genetic differentiation; furthermore, maximum climate resistance was 45× greater than riparian resistance. (iii) Genetic diversity was positively correlated with connectivity (R2  = 0.3744, p = .0019), illustrating the utility of resistance models for identifying landscape conditions that can support a species' ability to adapt to environmental change. From these results, we present a map highlighting key genetic connectivity corridors across P. angustifolia's range that if disrupted could have long-term ecological and evolutionary consequences. Our findings provide recommendations for conservation and restoration management of threatened riparian ecosystems throughout the western USA and the high biodiversity they support.

Arthropod communities on hybrid and parental cottonwoods are phylogenetically structured by tree type: Implications for conservation of biodiversity in plant hybrid zones.

Although hybridization in plants has been recognized as an important pathway in plant speciation, it may also affect the ecology and evolution of associated communities. Cottonwood species (Populus angustifolia and P. fremontii) and their naturally occurring hybrids are known to support different plant, animal, and microbial communities, but no studies have examined community structure within the context of phylogenetic history. Using a community composed of 199 arthropod species, we tested for differences in arthropod phylogenetic patterns within and among hybrid and parental tree types in a common garden. Three major patterns emerged. (1) Phylogenetic diversity (PD) was significantly different between arthropod communities on hybrids and Fremont cottonwood when pooled by tree type. (2) Mean phylogenetic distance (MPD) and net relatedness index (NRI) indicated that communities on hybrid trees were significantly more phylogenetically overdispersed than communities on either parental tree type. (3) Community distance (Dpw) indicated that communities on hybrids were significantly different than parental species. Our results show that arthropod communities on parental and hybrid cottonwoods exhibit significantly different patterns of phylogenetic structure. This suggests that arthropod community assembly is driven, in part, by plant-arthropod interactions at the level of cottonwood tree type. We discuss potential hypotheses to explain the effect of plant genetic dissimilarity on arthropod phylogenetic community structure, including the role of competition and environmental filtering. Our findings suggest that cottonwood species and their hybrids function as evolutionarily significant units (ESUs) that affect the assembly and composition of associated arthropod communities and deserve high priority for conservation.

Genetically informed ecological niche models improve climate change predictions.

We examined the hypothesis that ecological niche models (ENMs) more accurately predict species distributions when they incorporate information on population genetic structure, and concomitantly, local adaptation. Local adaptation is common in species that span a range of environmental gradients (e.g., soils and climate). Moreover, common garden studies have demonstrated a covariance between neutral markers and functional traits associated with a species' ability to adapt to environmental change. We therefore predicted that genetically distinct populations would respond differently to climate change, resulting in predicted distributions with little overlap. To test whether genetic information improves our ability to predict a species' niche space, we created genetically informed ecological niche models (gENMs) using Populus fremontii (Salicaceae), a widespread tree species in which prior common garden experiments demonstrate strong evidence for local adaptation. Four major findings emerged: (i) gENMs predicted population occurrences with up to 12-fold greater accuracy than models without genetic information; (ii) tests of niche similarity revealed that three ecotypes, identified on the basis of neutral genetic markers and locally adapted populations, are associated with differences in climate; (iii) our forecasts indicate that ongoing climate change will likely shift these ecotypes further apart in geographic space, resulting in greater niche divergence; (iv) ecotypes that currently exhibit the largest geographic distribution and niche breadth appear to be buffered the most from climate change. As diverse agents of selection shape genetic variability and structure within species, we argue that gENMs will lead to more accurate predictions of species distributions under climate change.

Bud phenology and growth are subject to divergent selection across a latitudinal gradient in Populus angustifolia and impact adaptation across the distributional range and associated arthropods.

Temperate forest tree species that span large geographical areas and climatic gradients often have high levels of genetic variation. Such species are ideal for testing how neutral demographic factors and climate-driven selection structure genetic variation within species, and how this genetic variation can affect ecological communities. Here, we quantified genetic variation in vegetative phenology and growth traits in narrowleaf cottonwood, Populus angustifolia, using three common gardens planted with genotypes originating from source populations spanning the species' range along the Rocky Mountains of North America (ca. 1700 km). We present three main findings. First, we found strong evidence of divergent selection (Q ST > F ST) on fall phenology (bud set) with adaptive consequences for frost avoidance. We also found evidence for selection on bud flush duration, tree height, and basal diameter, resulting in population differentiation. Second, we found strong associations with climate variables that were strongly correlated with latitude of origin. More strongly differentiated traits also showed stronger climate correlations, which emphasizes the role that climate has played in divergent selection throughout the range. We found population × garden interaction effects; for some traits, this accounted for more of the variance than either factor alone. Tree height was influenced by the difference in climate of the source and garden locations and declined with increasing transfer distance. Third, growth traits were correlated with dependent arthropod community diversity metrics. Synthesis. Overall, we conclude that climate has influenced genetic variation and structure in phenology and growth traits and leads to local adaptation in P. angustifolia, which can then impact dependent arthropod species. Importantly, relocation of genotypes far northward or southward often resulted in poor growth, likely due to a phenological mismatch with photoperiod, the proximate cue for fall growth cessation. Genotypes moved too far southward suffer from early growth cessation, whereas those moved too far northward are prone to fall frost and winter dieback. In the face of current and forecasted climate change, habitat restoration, forestry, and tree breeding efforts should utilize these findings to better match latitudinal and climatic source environments with management locations for optimal future outcomes.

Genetic variation in NIN1 and C/VIF1 genes is significantly associated with Populus angustifolia resistance to a galling herbivore, Pemphigus betae.

The identification of genes associated with ecologically important traits provides information on the potential genetic mechanisms underlying the responses of an organism to its natural environment. In this study, we investigated the genetic basis of host plant resistance to the gall-inducing aphid, Pemphigus betae, in a natural population of 154 narrowleaf cottonwoods (Populus angustifolia). We surveyed genetic variation in two genes putatively involved in sink-source relations and a phenology gene that co-located in a previously identified quantitative trait locus for resistance to galling. Using a candidate gene approach, three major findings emerged. First, natural variation in tree resistance to galling was repeatable. Sampling of the same tree genotypes 20 years after the initial survey in 1986 show that 80% of the variation in resistance was due to genetic differences among individuals. Second, we identified significant associations at the single nucleotide polymorphism and haplotype levels between the plant neutral invertase gene NIN1 and tree resistance. Invertases are a class of sucrose hydrolyzing enzymes and play an important role in plant responses to biotic stress, including the establishment of nutrient sinks. These associations with NIN1 were driven by a single nucleotide polymorphism (NIN1_664) located in the second intron of the gene and in an orthologous sequence to two known regulatory elements. Third, haplotypes from an inhibitor of invertase (C/VIF1) were significantly associated with tree resistance. The identification of genetic variation in these two genes provides a starting point to understand the possible genetic mechanisms that contribute to tree resistance to gall formation. We also build on previous work demonstrating that genetic differences in sink-source relationships of the host influence the ability of P. betae to manipulate the flow of nutrients and induce a nutrient sink.

Landscape genetic connectivity in a riparian foundation tree is jointly driven by climatic gradients and river networks.

Fremont cottonwood (Populus fremonti) is a foundation riparian tree species that drives community structure and ecosystem processes in southwestern U.S. ecosystems. Despite its ecological importance, little is known about the ecological and environmental processes that shape its genetic diversity, structure, and landscape connectivity. Here, we combined molecular analyses of 82 populations including 1312 individual trees dispersed over the species' geographical distribution. We reduced the data set to 40 populations and 743 individuals to eliminate admixture with a sibling species, and used multivariate restricted optimization and reciprocal causal modeling to evaluate the effects of river network connectivity and climatic gradients on gene flow. Our results confirmed the following: First, gene flow of Fremont cottonwood is jointly controlled by the connectivity of the river network and gradients of seasonal precipitation. Second, gene flow is facilitated by mid-sized to large rivers, and is resisted by small streams and terrestrial uplands, with resistance to gene flow decreasing with river size. Third, genetic differentiation increases with cumulative differences in winter and spring precipitation. Our results suggest that ongoing fragmentation of riparian habitats will lead to a loss of landscape-level genetic connectivity, leading to increased inbreeding and the concomitant loss of genetic diversity in a foundation species. These genetic effects will cascade to a much larger community of organisms, some of which are threatened and endangered.

Climate relicts and their associated communities as natural ecology and evolution laboratories.

Climate relicts, marginal populations that have become isolated via climate-driven range shifts, preserve ecological and evolutionary histories that can span millennia. Studies point to climate relicts as 'natural laboratories' for investigating how long-term environmental change impacts species and populations. However, we propose that such research should be expanded to reveal how climate change affects 'interacting' species in ways that reshape community composition and evolution. Biotic interactions and their community and ecosystem effects are often genetically based and driven by associations with foundation species. We discuss evolution in climate relicts within the context of the emerging fields of community and ecosystem genetics, exploring the idea that foundation relicts are also natural community and ecosystem laboratories and windows to future landscapes.

Pollinator-mediated gene flow fosters genetic variability in a narrow alpine endemic, Abronia alpina (Nyctaginaceae).

PREMISE OF THE STUDY: For rare and endemic plants that exist in small, isolated habitats, natural selection is expected to favor self-compatibility, which can result in low genetic diversity due to inbreeding and genetic drift. Using Abronia alpina, a rare alpine endemic of the California Floristic Province, we demonstrate that there are exceptions to these predictions. METHODS: We present the results of both a pollination experiment and a genetic study using AFLPs (amplified fragment length polymorphisms). Using controlled hand-pollination and pollinator observations, we examined the breeding system, pollination ecology, and mechanism for self-incompatibility in A. alpina. KEY RESULTS: Abronia alpina exhibits an allogamous mating system with probable self-incompatibility resulting from limited growth of pollen tubes originating from self-pollination. Only xenogamous crosses and open-pollinated controls produced seed, and only xenogamous crosses produced pollen tubes that reached the ovary. The molecular study shows that A. alpina has substantial genetic diversity for a rare, endemic species, evidenced by the high percentage of polymorphic loci and average expected heterozygosity. Gene flow among subpopulations, as inferred from AFLP markers, appears to be substantial, although the Kern River is an important physical barrier. CONCLUSIONS: Our results indicate that A. alpina is dependent on insects for both seed production and the maintenance of genetic diversity. This finding suggests that pollinators may be crucial to the long-term adaptive potential of rare, endemic plants and that conservation of rare endemics is, in part, dependent on community-level interactions such as plant-pollinator mutualisms.