Stuart C. Wooley

From Genes to Ecosystems : The Genetic Basis of Condensed Tannins and Their Role in Nutrient Regulation in a Populus Model System

Research that connects ecosystem processes to genetic mechanisms has recently gained significant ground, yet actual studies that span the levels of organization from genes to ecosystems are extraordinarily rare. Utilizing foundation species from the genus Populus, in which the role of condensed tannins (CT) has been investigated aboveground, belowground, and in adjacent streams, we examine the diverse mechanisms for the expression of CT and the ecological consequences of CT for forests and streams. The wealth of data from this genus highlights the importance of form and function of CT in large-scale and long-term ecosystem processes and demonstrates the following four patterns: (1) plant-specific concentration of CT varies as much as fourfold among species and individual genotypes; (2) large within-plant variation in CT occurs due to ontogenetic stages (that is, juvenile and mature), tissue types (that is, leaves versus twigs) and phenotypic plasticity in response to the environment; (3) CT have little consistent effect on plant–herbivore interactions, excepting organisms utilizing woody tissues (that is, fungal endophytes and beaver), however; (4) CT in plants consistently slow rates of leaf litter decomposition (aquatic and terrestrial), alter the composition of heterotrophic soil communities (and some aquatic communities) and reduce nutrient availability in terrestrial ecosystems. Taken together, these data suggest that CT may play an underappreciated adaptive role in regulating nutrient dynamics in ecosystems. These results also demonstrate that a holistic perspective from genes-to-ecosystems is a powerful approach for elucidating complex ecological interactions and their evolutionary implications.

Within-species variation in foliar chemistry influences leaf-litter decomposition in a Utah river

Abstract Leaf-litter inputs provide substrate and energy to stream systems. These contributions vary based on species-specific differences in litter quality, but little is known about how differences in litter quality within a species can affect ecosystem processes. Genetic variation within tree species, such as oaks and cottonwoods, affects ecosystem processes including decomposition and nutrient cycling in forest ecosystems and has the potential to do the same in streams. We collected litter from 5 genotypes of each of 4 different cottonwood cross types (Populus fremontii, Populus angustifolia, and natural F1 and backcross hybrids), grown in a common garden, and measured their decomposition rates using litter bags in the Weber River, Utah. The proportion of 35 species-specific P. fremontii restriction-fragment length polymorphism markers in the genotype explained 46% and genetically controlled phytochemical mechanisms (e.g., % soluble condensed tannin in litter) explained >72% of the variation in leaf-litter decomposition rate, respectively. Understanding how natural genetic variation in plants can affect ecosystem processes will provide baseline information with which to address the loss of genetic variation (through habitat fragmentation and global change) and altered genetic variation through hybridization with cultivars and transgenic manipulations in the wild.

Plant genetics predicts intra-annual variation in phytochemistry and arthropod community structure

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.

Aspen Decline, Aspen Chemistry, and Elk Herbivory: Are They Linked?

and has high aesthetic appeal in autumn. However, the amount and quality of aspen cover in the West has been declining for many years. For example, aspen cover in the Dixie and Fishlake National forests in Utah has decreased by more than 60% from historic levels, and in the Uinta National Forest aspen cover has been reduced by nearly 40%

Forest gene diversity is correlated with the composition and function of soil microbial communities

The growing field of community and ecosystem genetics indicates that plant genotype and genotypic variation are important for structuring communities and ecosystem processes. Little is known, however, regarding the effects of stand gene diversity on soil communities and processes under field conditions. Utilizing natural genetic variation occurring in Populus spp. hybrid zones, we tested the hypothesis that stand gene diversity structures soil microbial communities and influences soil nutrient pools. We found significant unimodal patterns relating gene diversity to soil microbial community composition, microbial exoenzyme activity of a carbon-acquiring enzyme, and availability of soil nitrogen. Multivariate analyses indicate that this pattern is due to the correlation between gene diversity, plant secondary chemistry, and the composition of the microbial community that impacts the availability of soil nitrogen. Together, these data from a natural system indicate that stand gene diversity may affect soil microbial communities and soil processes in ways similar to species diversity (i.e., unimodal patterns). Our results further demonstrate that the effects of plant genetic diversity on other organisms may be mediated by plant functional trait variation.

Aspen Decline, Aspen Chemistry, and Elk Herbivory: Are They Linked?: Aspen chemical ecology can inform the discussion of aspen decline in the West

and has high aesthetic appeal in autumn. However, the amount and quality of aspen cover in the West has been declining for many years. For example, aspen cover in the Dixie and Fishlake National forests in Utah has decreased by more than 60% from historic levels, and in the Uinta National Forest aspen cover has been reduced by nearly 40%

Qualitative variation in proanthocyanidin composition of Populus species and hybrids: genetics is the key.

The literature on proanthocyanidins (tannins) in ecological systems is dominated by quantitative studies. Despite evidence that the qualitative characteristics (subunit type, polymer chain length) of these complex polyphenolics are important determinants of biological activity, little is known about genetic and environmental controls on the type of proanthocyanidins produced by plants. We tested the hypothesis that genetics, season, developmental stage, and environment determine proanthocyanidin qualitative characteristics by using four Populus “cross types” (narrowleaf [P. angustifolia], Fremont [P. fremontii], F1 hybrids, and backcrosses to narrowleaf). We used thiolysis and HPLC analysis to characterize the proanthocyanidins, and found that genetics strongly control composition. The narrowleaf plants accumulate mixed procyanidin/prodelphinidins with average composition epicatechin11-epigallocatechin8-catechin2-catechin(terminal). Backcross genotypes produce mixed procyanidin/prodelphinidins similar to narrowleaf, while Fremont makes procyanidin dimers, and the F1 plants contain procyanidin heptamers. Less striking effects were noted for genotype × environment, while season and developmental zone had little effect on proanthocyanidin composition or chain length. We discuss the metabolic and ecological consequences of differences in condensed tannin qualitative traits.

Tree genotype and genetically based growth traits structure twig endophyte communities

PREMISE OF THE STUDY Fungal endophytes asymptomatically inhabit plant tissues where they have mutualistic, parasitic, or commensal relationships with their hosts. Although plant-fungal interactions at the genotype scale have broad ecological and evolutionary implications, the sensitivity of endophytes in woody tissues to differences among plant genotypes is poorly understood. We hypothesize that (1) endophyte communities in Populus angustifolia (Salicaceae) twigs vary among tree genotypes, (2) endophyte variation is linked to quantitative tree traits, and (3) tree genotype influences interspecific fungal interactions. METHODS Endophytes were isolated from twigs of replicated P. angustifolia genotypes in a common garden and characterized with PCR-RFLP and DNA sequencing. Twig length and diameter, aboveground tree biomass, and condensed tannins were also quantified. KEY RESULTS (1) Aspects of fungal community structure, including composition and total isolation frequency (i.e., abundance), varied among genotypes. (2) Aboveground biomass and twig diameter were positively associated with isolation frequency and covaried with composition, whereas twig length and condensed tannin concentration were not significantly correlated to endophytes. (3) Fungal co-occurrence patterns suggested negative species interactions, but the presence of significant co-occurrences was genotype dependent. CONCLUSIONS The species is often assumed to be the most important ecological unit; however, these results indicate that genetically based trait variation within a species can influence an important community of associated organisms. Given the dominance of plants as primary producers and the ubiquity of endophytes, the effect of host genetic variation on endophytes has fundamental implications for our understanding of terrestrial ecosystems.

Hybridization among foundation tree species influences the structure of associated understory plant communities

Understanding how genetic identity influences community structure is a major focus in evolutionary ecology, yet few studies examine interactions among organisms in the same trophic level within this context. In a common garden containing trees from a hybrid system (Populus fremontii S. Wats. Populus angustifolia James), we tested the hypothesis that the structure of establishing understory plant communities is influenced by genetic differences among trees and ex- plored foliar condensed tannins (CTs) and photosynthetically active radiation (PAR) as mechanisms. Several findings sup- port our hypothesis: (i) Understory biomass and cover increase along the genetic gradient from P. angustifolia to P. fremontii .( ii) Along the same hybridization gradient, species richness decreases and species composition shifts. (iii) Populus foliar CT concentrations and PAR decrease from P. angustifolia to P. fremontii .( iv) Understory species rich- ness increases with foliar CTs; however, biomass, cover, and composition show no relationship with CTs, and no under- story variables correlate with PAR. (v) Structural equation modeling suggests that foliar CTs are a primary mechanism linking overstory tree genetics with understory richness. Using an experimental system dominated by naturally colonizing exotic species, this study demonstrates that a genetic gradient created by tree hybridization can influence understory plants.

Genotype and soil nutrient environment influence aspen litter chemistry and in-stream decomposition

Abstract.  A growing body of genes-to-ecosystems research has documented the ecosystem-level consequences of intraspecific variation in plants caused in large part by variation in chemical composition. Understanding how this genetic variation in trees might interact with elevated nutrients resulting from increases in anthropogenic deposition may give us insight into how future riparian forests might influence adjacent streams through leaf-litter deposition. We examined the effects of tree genotype, soil nutrient environment, and their interaction on aspen (Populus tremuloides) litter chemistry and aquatic decomposition. We used litter collected from 5 aspen genotypes grown in a common garden under low and high nutrient availability and monitored decomposition over 112 d in a woodland stream. Genotype, environment, and genotype × environment interactions influenced litter chemistry and decomposition dynamics. Genotype and environment both strongly influenced initial litter chemistry, with significant genotype × environment interactions for bound condensed tannins and C∶N. Consistent with effects on litter chemistry, decomposition rates were significantly affected by genotype, environment, and genotype × environment interactions. These results suggest that future changes in intraspecific genetic variation of tree species and deposition of nutrients because of shifts in climate, land use, and related factors may influence decomposition processes in terrestrial systems and in the aquatic systems with which they are coupled via material transfer.