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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 (R 2 = .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.

We examined the hypothesis that ecologically important phytochemical traits differ predictably among various developmental zones of trees (i.e., mature and juvenile zones of individual trees and juvenile ramets that sprout from roots) and that the slope of this phytochemical gradient represents a "developmental trajectory." We focused on Populus fremontii (Fremont cottonwood), P. angustifolia (narrowleaf cottonwood), and their natural hybrids. Two major patterns emerged. First, within narrowleaf and hybrids, concentrations of important phytochemicals (condensed tannins and phenolic glycosides) differ greatly and predictably between developmental zones. Second, developmental trajectories differ greatly among these cottonwood species and their hybrids: Fremont exhibits a flat trajectory, narrowleaf a steep trajectory, and hybrids an intermediate trajectory, suggesting an additive genetic component and an ontogenetic basis to this phytochemical variation. Because diverse herbivorous species respond to the phytochemistry of their host plants, we predict that the developmental trajectories of plants play a major role in mediating ecological interactions and structuring communities, and that biodiversity in a stand of trees is determined by both interplant genetic diversity and intraplant ontogenetic diversity.

We tested the hypothesis that leaf modifying arthropod communities are correlated with cottonwood host plant genetic variation from local to regional scales. Although recent studies found that host plant genetic composition can structure local dependent herbivore communities, the abiotic environment is a stronger factor than the genetic effect at increasingly larger spatial scales. In contrast to these studies we found that dependent arthropod community structure is correlated with both the cross type composition of cottonwoods and individual genotypes within local rivers up to the regional scale of 720 000 km 2 (Four Corner States region in the southwestern USA). Across this geographical extent comprising two naturally hybridizing cottonwood systems, the arthropod community follows a simple genetic similarity rule: genetically similar trees support more similar arthropod communities than trees that are genetically dissimilar. This relationship can be quantified with or without genetic data in Populus .

We define a genetic similarity rule that predicts how genetic variation in a dominant plant affects the structure of an arthropod community. This rule applies to hybridizing cottonwood species where plant genetic variation determines plant–animal interactions and structures a dependent community of leaf-modifying arthropods. Because the associated arthropod community is expected to respond to important plant traits, we also tested whether plant chemical composition is one potential intermediate link between plant genes and arthropod community composition. Two lines of evidence support our genetic similarity rule. First, in a common garden experiment we found that trees with similar genetic compositions had similar chemical compositions and similar arthropod compositions. Second, in a wild population, we found a similar relationship between genetic similarity in cottonwoods and the dependent arthropod community. Field data demonstrate that the relationship between genes and arthropods was also significant when the hybrids were analysed alone, i.e. the pattern is not dependent upon the inclusion of both parental species. Because plant–animal interactions and natural hybridization are common to diverse plant taxa, we suggest that a genetic similarity rule is potentially applicable, and may be extended, to other systems and ecological processes. For example, plants with similar genetic compositions may exhibit similar litter decomposition rates. A corollary to this genetic similarity rule predicts that in systems with low plant genetic variability, the environment will be a stronger factor structuring the dependent community. Our findings argue that the genetic composition of a dominant plant can structure higher order ecological processes, thus placing community and ecosystem ecology within a genetic and evolutionary framework. A genetic similarity rule also has important conservation implications because the loss of genetic diversity in one species, especially dominant or keystone species that define many communities, may cascade to negatively affect the rest of the dependent community.

We argue that the genetic diversity of a dominant plant is important to the associated dependent community because dependent species such as herbivores are restricted to a subset of genotypes in the host-plant population. For plants that function as habitat, we predicted that greater genetic diversity in the plant population would be associated with greater diversity in the dependent arthropod community. Using naturally hybridizing cottonwoods (Populus spp.) in western North America as a model system, we tested the general hypothesis that arthropod alpha (within cross-type richness) and beta (among cross-type composition) diversities are correlated with cottonwood cross types from local to regional scales. In common garden experiments and field surveys, leaf-modifying arthropod richness was significantly greater on either the F 1 (1.54 times) or backcross (1.46 times) hybrid cross types than on the pure broadleaf cross type (P. deltoides Marshall or P. fremontii Watson). Composition was significantly different among three cross types of cottonwoods at all scales. Within a river system, cottonwood hybrid zones had 1.49 times greater richness than the broadleaf zone, and community composition was significantly different between each parental zone and the hybrid zone, demonstrating a hierarchical concentration of diversity. Overall, the habitats with the highest cottonwood cross-type diversity also had the highest arthropod diversity. These data show that the genetics of habitat is an important conservation concept and should be a component of conservation theory.

To test the hypothesis that genes have extended phenotypes on the community, we quantified how genetic differences among cottonwoods affect the diversity, abundance, and composition of the dependent arthropod com- munity. Over two years, five major patterns were observed in both field and common-garden studies that focused on two species of cottonwoods and their naturally occurring F1 and backcross hybrids (collectively referred to as four different cross types). We did not find overall significant differences in arthropod species richness or abundance among cottonwood cross types. We found significant differences in arthropod community composition among all cross types except backcross and narrowleaf cottonwoods. Thus, even though we found similar richness among cross types, the species that composed the community were significantly different. Using vector analysis, we found that the shift in arthropod community composition was correlated with percent Fremont alleles in the host plant, which suggests that the arthropod community responds to the underlying genetic differences among trees. We found 13 arthropod species representing different trophic levels that were significant indicators of the four different cross types. Even though arthropod communities changed in species composition from one year to the next, the overall patterns of community differences remained remarkably stable, suggesting that the genetic differences among cross types exert a strong organizing influence on the arthropod community. Together, these results support the extended phenotype concept. Few studies have observationally and experimentally shown that entire arthropod communities can be structured by genetic differences in their host plants. These findings contribute to the developing field of community genetics and suggest a strategy for conserving arthropod diversity by promoting genetic diversity in their host plants.

Ecological genetics is increasingly recognized as critical to understanding interactions among organisms and ecosystem processes. Using a common garden with pure and hybrid cottonwood trees of known genotype, two years of field surveys, and a cafeteria feeding experiment, we link introgression of Fremont genetic markers, condensed tannins (a genetically based plant trait), and foraging by beavers. These data support two major arguments. First, hybridization is an important mechanism for the transmission of ecologically functional traits. Second, links between a genetically based plant trait in a dominant riparian-forest tree species and the foraging behavior of beavers, an ecosystem engineer, emphasize that genetically based plant traits can directly and indirectly link population, community, and ecosystem processes.

We present evidence that the heritable genetic variation within individual species, especially dominant and keystone species, has community and ecosystem conse- quences. These consequences represent extended phenotypes, i.e., the effects of genes at levels higher than the population. Using diverse examples from microbes to vertebrates, we demonstrate that the extended phenotype can be traced from the individuals possessing the trait, to the community, and to ecosystem processes such as leaf litter decomposition and N mineralization. In our development of a community genetics perspective, we focus on intraspecific genetic variation because the extended phenotypes of these genes can be passed from one generation to the next, which provides a mechanism for heritability. In support of this view, common-garden experiments using synthetic crosses of a dominant tree show that their progeny tend to support arthropod communities that resemble those of their parents. We also argue that the combined interactions of extended phenotypes con- tribute to the among-community variance in the traits of individuals within communities. The genetic factors underlying this among-community variance in trait expression, partic- ularly those involving genetic interactions among species, constitute community heritability. These findings have diverse implications. (1) They provide a genetic framework for un- derstanding community structure and ecosystem processes. The effects of extended phe- notypes at these higher levels need not be diffuse; they may be direct or may act in relatively few steps, which enhances our ability to detect and predict their effects. (2) From a con- servation perspective, we introduce the concept of the minimum viable interacting popu- lation (MVIP), which represents the size of a population needed to maintain genetic diversity at levels required by other interacting species in the community. (3) Genotype 3 environ- ment interactions in dominant and keystone species can shift extended phenotypes to have unexpected consequences at community and ecosystem levels, an issue that is especially important as it relates to global change. (4) Documenting community heritability justifies a community genetics perspective and is an essential first step in demonstrating community evolution. (5) Community genetics requires and promotes an integrative approach, from genes to ecosystems, that is necessary for the marriage of ecology and genetics. Few studies span from genes to ecosystems, but such integration is probably essential for understanding the natural world.

Hybrids have long been recognized as a potential pathway for gene flow between species that can have important consequences for evolution and conservation biology. However, few studies have demonstrated that genes from one species can introgress or invade another species over a broad geographic area. Using 35 genetically mapped restriction fragment length polymorphism (RFLP) markers of two species of cottonwoods (Populus fremontii x P. angustifolia) and their hybrids (n = 550 trees), we showed that the majority of the genome is prohibited from introgressing from one species into the other. However, this barrier was not absolute; Fremont cpDNA and mtDNA were found throughout the geographic range of narrowleaf cottonwood, and 20% of the nuclear markers of Fremont cottonwood introgressed varying distances (some over 100 km) into the recipient species' range. Rates of nuclear introgression were variable, but two nuclear markers introgressed as fast as the haploid, cytoplasmically inherited chloroplast and mitochondrial markers. Our genome-wide analysis provides evidence for positive, negative, and neutral effects of introgression. For example, we predict that DNA fragments that introgress through several generations of backcrossing will be small, because small fragments are less likely to contain deleterious genes. These results argue that recombination will be important, that introgression can be very selective, and that evolutionary forces within the hybrid population to effectively "filter" gene flow between species. A strong filter may make introgression adaptive, prevent genetic assimilation, lead to relaxed isolating mechanisms, and contribute to the stability of hybrid zones. Thus, rather than hybridization being a negative factor as is commonly argued, natural hybridization between native species may provide important genetic variation that impacts both ecological and evolutionary processes. Finally, we propose two hypotheses that contrast the likelihood of contemporary versus ancient introgression in this system.

We examined the potential of a common herbivore to indirectly influence other diverse community members by providing habitat. Larvae of the leafroller Anacampsis niveopulvella commonly construct shelters by rolling leaves of cottonwood trees. These leaf rolls are later colonized by other arthropods. We first documented 4 times greater species richness and 7 times greater abundance on cottonwood shoots that contained a rolled leaf compared to adjacent shoots without leaf rolls. Second, with both removal and addition experiments, we showed that leaf rolls are responsible for these differences in arthropod assemblages. Leaf roll removal caused a 5-fold decline in richness and a 7-fold decline in abundance; leaf roll addition resulted in a 2.5-fold increase in richness and a 6-fold increase in abundance. Third, to determine whether rolled leaves are colonized for food or for shelter, we compared colonization of natural and artificial leaf rolls. Both richness and abundance were approximately 2-fold greater in artificial leaf rolls, indicating that leaf rolls are colonized primarily for shelter. Fourth, in a natural hybrid zone we found that leafroller densities were 2-fold greater on backcross hybrids than on F1 hybrids. These differences are likely associated with genetically-based differences in leaf morphology and/or leaf chemistry. Ultimately, plant genotype affects positive indirect interactions that have the potential to affect community structure. This study and others demonstrate that shelter builders (i.e., leafrollers and gall formers) enhance biodiversity, while free-feeders are more likely to negatively affect biodiversity.

Plant hybrid zones are dynamic centers of ecological and evolutionary processes for plants and their associated communities. Studies in the wild and in gardens with synthetic crosses showed that hybrid eucalypts supported the greatest species richness and abundances of insect and fungal taxa. In an updated review of 152 case studies of taxa associated with diverse hybridizing systems, there were 43 (28%) cases of hybrids being more susceptible than their parent species, 7 (5%) resistant, 35 (23%) additive, 35 (23%) dominant, and 32 (21%) showed no response to hybridization. Thus, most taxa respond to hybrids in ways that result in equal or greater abundance, and hybrids tend to accumulate the taxa of their parent species. These studies suggest that genetic-based plant traits affect the distribution of many species and that the variation in hybrids can be used as tools to examine the genetic components of community structure and biodiversity. Several patterns have emerged thus far. (1) Genetic variation between classes of hybrids (e.g., F1’s vs. backcrosses) may equal or even exceed that found between species. (2) As a reflection of this genetic variation, herbivores are more likely to differentiate between hybrid classes than they are to differentiate between pure plant species. (3) The communities associated with different hybrid classes can differ from one another as well as from their parental species. (4) Generalist and specialist herbivores predictably vary in their responses to hybrids. (5) Plant hybrid zones may represent essential habitat for some arthropod species. (6) Even nesting birds respond to hybridizing plants. (7) Including multiple trophic levels and taxa from microbes to vertebrates, susceptible hybrid genotypes support greater biodiversity than resistant genotypes. (8) The effects of hybridization on common or keystone species can either positively or negatively affect biodiversity. The indirect impacts of hybridization on biodiversity may exceed the direct impacts and may result in “apparent” herbivore resistance or susceptibility at the community level. (9) Although hybrids are often maligned, exotic or problem hybrids generally result from human disturbances, whereas native hybrids are part of natural ecosystems and should be conserved. Three predictions are made: (1) Intermediate genetic differences between the parental species will result in the greatest genetic variation in the hybrid zone, which in turn will have a positive effect on biodiversity. (2) Bidirectional introgression enhances species richness on hybrids, whereas F1 sterility and unidirectional introgression limit the accumulation of species on hybrids. (3) Although susceptible hybrids are likely to support the greatest biodiversity, the impacts of hybridization on keystone species will be crucial in determining the overall effect.

We documented an indirect interaction between beavers (Castor canadensis) and leaf beetles (Chrysomela confluens), mediated by changing plant chemistry of their cottonwood hosts (Populus fremontii 3 P. angustifolia). Resprout growth arising from the stumps and roots of beaver-cut trees contained twice the level of defensive chemicals as normal juvenile growth. However, rather than being repelled by these defenses, leaf beetles were attracted to resprout growth, resulting in a strong positive association between beavers and beetles. Why? Cottonwoods contain phenolic glycosides, chemicals that are defensive against mammalian herbivores, but are sequestered and used by the beetles for their own defense. Experiments showed that beetles fed resprout growth were better defended against their predators than those fed nonresprout growth. There also may have been a nutritional benefit, because the conversion of the plant's defense, salicin and other phenolic glycosides, to salicylaldehyde releases glucose. Also, resprout growth contained more total nitrogen than did nonresprout growth. Transfer experiments showed that, in apparent response to these increased nutritional benefits, beetles fed resprout growth developed faster and weighed more at maturity. Although indirect interactions are much less studied than direct interactions, our work suggests that the indirect interactions resulting from beaver cutting of cottonwoods have important consequences for other organisms and could represent an important component of community structure. The habitat mosaics created by beaver herbivory increase arthropod biodiversity and may benefit other organisms such as birds and mammals. Furthermore, by stimulating the production of resprout growth, beavers may play an important role in the regeneration of a habitat type that is rapidly vanishing in the West.

For the purposes of energy forests, we argue that biological pest control should be interpreted as any method of using natural organisms or their products for the regulation of herbivores, below the economic threshold. The organisms include the energy forest crop species and natural enemies of pest herbivores. In natural vegetation, potentially harmful arthropod herbivores are normally regulated at low populations through a combination of bottom-up forces in food webs including edaphic factors and plant factors, and top-down effects from carnivores. Bottom-up effects tend to be strong, impacting both herbivores and carnivores in the food web, forcing the consideration of three-trophic-level systems as the minimal unit of study. Examples are provided of three-trophic-level interactions, including some on willows and poplars. Bottom-up effects may be particularly strong in juvenile Salicaceae, which are used in energy forest production, because plants are growing vigorously, and many herbivores respond positively. Some major pests on willows and poplars appear to have weak top-down regulation, and they may be influenced most by bottom-up effects such as plant resistance through genetic variation, ontogenetic aging and physiological aging. Balancing the bottom-up and top-down forces in energy forests may be difficult in short-rotation crops, but harvesting may prove to be important as a control during pest outbreaks damaging to yield. However, we suggest that many aspects of energy forests are conducive to pest control, which are enumerated, and emphasize the need for further research on native three-trophic-level systems, economic thresholds, cultural methods and crop species and genotype selection.

Using surveys of natural populations, experimental crosses, and common garden trials, we tested the hypothesis that hybrid cottonwoods (Populus fremontii × P. angustifolia) from the Weber River in northern Utah would produce as many viable offspring as their parental species. We found that both F(1) generations and backcross generations can be just as fit as the parent taxa. First, F(1) hybrids produced as many viable seed as P. angustifolia (but less than P. fremontii), and backcross genotypes produced as many viable seeds as both parent taxa. Second, hybrids produced nearly two times as many ramets from root sprouts as P. angustifolia and four times as many ramets as P. fremontii. Third, the high mortality of germinated seedlings of all tree types (i.e., >90%) and very low mortality of asexually derived ramets provide hybrids with equal sexual reproduction and enhanced asexual reproduction, especially since backcross hybrids exhibit transgressive segregation in ramet production. Our findings suggest that the introgression of P. fremontii seed traits into the hybrid genome is responsible for their equivalent performance (at least to one parent) in sexual reproduction, while the contributions of asexual traits from P. angustifola results in hybrids having equal or greater fitness.

We examined the impact of pocket gopher disturbances on the dynamics of a shortgrass prairie community. Through their burrowing activity, pocket gophers (Thomomys bottae) cast up mounds of soil which both kill existing vegetation and create sites for colonization by competitively-inferior plant species. Three major patterns emerge from these disturbances: First, we show that 10 of the most common herbaceous perennial dicots benefit from pocket gopher disturbance; that is, a greater proportion of seedlings are found in the open space created by pocket gopher disturbance than would be expected based on the availability of disturbed habitat. Additionally, these seedlings exhibited higher growth rates than adjacent seedlings of the same species growing in undisturbed habitat. Second, we tested two predictions of the Intermediate Disturbance Hypothesis and found that species diversity was greatest for plots characterized by disturbances of intermediate age. However, we did not detect significant differences in diversity between plots characterized by intermediate and high levels of disturbance, indicating that many species are adapted to or at least tolerant of high levels of disturbance. Third, we noted that the abundance of grasses decreased with increasing disturbance, while the abundance of dicots increased with increasing disturbance.

With the emerging field of community genetics, it is important to quantify the key mechanisms that link genetics and community structure. We studied cottonwoods in common gardens and in natural stands and examined the potential for plant chemistry to be a primary mechanism linking plant genetics and arthropod communities. If plant chemistry drives the relationship between plant genetics and arthropod community structure, then several predictions followed. We would find (i) the strongest correlation between plant genetic composition and chemical composition; (ii) an intermediate correlation between plant chemical composition and arthropod community composition; and (iii) the weakest relationship between plant genetic composition and arthropod community composition. Our results supported our first prediction: plant genetics and chemistry had the strongest correlation in the common garden and the wild. Our results largely supported our second prediction, but varied across space, seasonally, and according to arthropod feeding group. Plant chemistry played a larger role in structuring common garden arthropod communities relative to wild communities, free-living arthropods relative to leaf and stem modifiers, and early-season relative to late-season arthropods. Our results did not support our last prediction, as host plant genetics was at least as tightly linked to arthropod community structure as plant chemistry, if not more so. Our results demonstrate the consistency of the relationship between plant genetics and biodiversity. Additionally, plant chemistry can be an important mechanism by which plant genetics affects arthropod community composition, but other genetic-based factors are likely involved that remain to be measured.

Cottonwoods are foundation riparian species, and hybridization among species is known to produce ecological effects at levels higher than the population, including effects on dependent species, communities and ecosystems. Because these patterns result from increased genetic variation in key cottonwood traits, novel applications of genetic tools (for example, QTL mapping) could be used to place broad-scale ecological research into a genomic perspective. In addition, linkage maps have been produced for numerous species within the genus, and, coupled with the recent publication of the Populus genome sequence, these maps present a unique opportunity for genome comparisons in a model system. Here, we conducted linkage analyses in order to (1) create a platform for QTL and candidate gene studies of ecologically important traits, (2) create a framework for chromosomal-scale perspectives of introgression in a natural population, and (3) enhance genome-wide comparisons using two previously unmapped species. We produced 246 backcross mapping (BC(1)) progeny by crossing a naturally occurring F(1) hybrid (Populus fremontii x P. angustifolia) to a pure P. angustifolia from the same population. Linkage analysis resulted in a dense linkage map of 541 AFLP and 111 SSR markers distributed across 19 linkage groups. These results compared favorably with other Populus linkage studies, and addition of SSR loci from the poplar genome project provided coarse alignment with the genome sequence. Preliminary applications of the data suggest that our map represents a useful framework for applying genomic research to ecological questions in a well-studied system, and has enhanced genome-wide comparisons in a model tree.

To test the hypothesis that genes have extended phenotypes on the community, we quantified how genetic differences among cottonwoods affect the diversity, abundance, and composition of the dependent arthropod community. Over two years, five major patterns were observed in both field and common-garden studies that focused on two species of cottonwoods and their naturally occurring F1 and backcross hybrids (collectively referred to as four different cross types). We did not find overall significant differences in arthropod species richness or abundance among cottonwood cross types. We found significant differences in arthropod community composition among all cross types except backcross and narrowleaf cottonwoods. Thus, even though we found similar richness among cross types, the species that composed the community were significantly different. Using vector analysis, we found that the shift in arthropod community composition was correlated with percent Fremont alleles in the host plant, which suggests that the arthropod community responds to the underlying genetic differences among trees. We found 13 arthropod species representing different trophic levels that were significant indicators of the four different cross types. Even though arthropod communities changed in species composition from one year to the next, the overall patterns of community differences remained remarkably stable, suggesting that the genetic differences among cross types exert a strong organizing influence on the arthropod community. Together, these results support the extended phenotype concept. Few studies have observationally and experimentally shown that entire arthropod communities can be structured by genetic differences in their host plants. These findings contribute to the developing field of community genetics and suggest a strategy for conserving arthropod diversity by promoting genetic diversity in their host plants.

Genetic variation in dominant species can affect plant and ecosystem functions in natural systems through multiple pathways. Our study focuses on how genetic variation in a dominant riparian tree (Populus fremontii, P. angustifolia and their natural F1 and backcross hybrids) affects whole-tree water use, and its potential ecosystem implications. Three major patterns were found. First, in a 12-year-old common garden with trees of known genetic makeup, hybrids had elevated daily integrated leaf-specific transpiration (E tl ; P=0.013) and average canopy conductance (G c ; P=0.037), with both E tl and G c ~30% higher in hybrid cross types than parental types. Second, δ13C values of leaves from these same trees were significantly more negative in hybrids (P=0.004), and backcross hybrids had significantly more negative values than all other F1 hybrid and parental types (P

We present three lines of evidence which each suggest that intraspecific competition has significantly influenced the spacing patterns of Formica altipetens colonies. First, nearest-neighbor analysis of nest spacing patterns detected significant uniformity in six of eight plots. Second, there was a signifcant increase in the distance separating nearest neighbors as ant nest diameters increased. Third, ant nest density predicted substantial variation in the colony dispersion index, indicating the existence of a dispersion continuum at our study site.