Using two genetic approaches and seven different plant systems, we present findings from a metaanalysis examining the strength of the effects of plant genetic introgression and genotypic diversity across individual, community and ecosystem levels with the goal of synthesizing the patterns to date. We found that (i) the strength of plant genetic effects can be quite high; however, the overall strength of genetic effects on most response variables declined as the levels of organization increased. (ii) Plant genetic effects varied such that introgression had a greater impact on individual phenotypes than extended effects on arthropods or microbes/fungi. By contrast, the greatest effects of genotypic diversity were on arthropods. (iii) Plant genetic effects were greater on above-ground versus below-ground processes, but there was no difference between terrestrial and aquatic environments. (iv) The strength of the effects of intraspecific genotypic diversity tended to be weaker than interspecific genetic introgression. (v) Although genetic effects generally decline across levels of organization, in some cases they do not, suggesting that specific organisms and /or processes may respond more than others to underlying genetic variation. Because patterns in the overall impacts of introgression and genotypic diversity were generally consistent across diverse study systems and consistent with theoretical expectations, these results provide generality for understanding the extended consequences of plant genetic variation across levels of organization, with evolutionary implications.
Roots play a critical, but largely unappreciated, role in aboveground anti-herbivore plant defense (e.g. resistance and tolerance) and root-leaf connections may therefore result in unexpected coupling between above- and belowground consumers. Using the tobacco (Nicotiana tabacum) system we highlight two examples of this phenomenon. First, the secondary metabolite nicotine is produced in roots, yet translocated aboveground for use as a foliar resistance trait. We demonstrate that nematode root herbivory interferes with foliar nicotine dynamics, resulting in positive effects on aboveground phytophagous insects. Notably, nematode-induced facilitation only occurred on nicotine-producing plants, and not on nicotine-deficient mutants. In the second case, we use stable isotope and invertase enzyme analyses to demonstrate that foliar herbivory elicits a putative tolerance response whereby aboveground nutritional reserves are allocated to roots, resulting in facilitation of phytoparasitic nematodes. Thus, plants integrate roots in resistance and tolerance mechanisms for leaf defense, and such root-leaf connections inherently link the dynamics of above- and belowground consumers.
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.
Recent studies have shown effects of host plant genetics on community and ecosystem processes, which makes understanding the impacts of genetically based traits on hidden or non-apparent organisms more important. Here we examined links among genetic variation in hybrid cottonwoods, plant phytochemistry, and twig fungal endophytes (i.e., a common hidden organism). We found three major patterns: (1) twig fungal endophyte infection was positively related to the introgression of Fremont cottonwood (Populus fremontii S. Wats.) RFLP genetic markers, (2) condensed tannin concentration in twig bark tissue was negatively correlated to the introgression of Fremont genetic markers, and (3) fungal endophyte infection was negatively related to condensed tannin concentration in twig bark. These data demonstrate that plant genotype can impact hidden ecological players (i.e., fungal endophytes) resulting in community and ecosystem consequences.Résumé : Comme de récentes études ont démontré les effets de la génétique de la plante hôte sur les processus communautaires et écosystémiques, la compréhension des impacts de caractères basés génétiquement sur des organismes cachés ou non apparents devient plus importante. Les auteurs examinent, chez des hybrides de peupliers deltoïdes, les liens entre la variation génétique, la phytochimie, et les endophytes fongiques (c.à.d., organismes généralement cachés). Ils retrouvent trois patrons principaux: (1) l'infection par des champignons endophytes des rameaux est positivement reliée à l'introgression de marqueurs génétiques RFLP du peuplier de Frémont (Populus fremontii S. Wats.); (2) la teneur en tannins condensés dans les tissus de l'écorce des rameaux est négativement corrélée avec l'introgression de marqueurs génétiques Frémont, et (3) l'infection par les endophytes est négativement reliée à la teneur en tannins condensés dans l'écorce des rameaux. Ces données montrent que le génotype du plant peut avoir des impacts sur des acteurs écologiques cachés (c.à.d., des endophytes fongiques) susceptibles d'affecter les communautés et les écosystè-mes.
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 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.
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.
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