Genetic structure of a foundation species: scaling community phenotypes from the individual to the region.

Understanding the local and regional patterns of species distributions has been a major goal of ecological and evolutionary research. The notion that these patterns can be understood through simple quantitative rules is attractive, but while numerous scaling laws exist (e.g., metabolic, fractals), we are aware of no studies that have placed individual traits and community structure together within a genetics based scaling framework. We document the potential for a genetic basis to the scaling of ecological communities, largely based upon our long-term studies of poplars (Populus spp.). The genetic structure and diversity of these foundation species affects riparian ecosystems and determines a much larger community of dependent organisms. Three examples illustrate these ideas. First, there is a strong genetic basis to phytochemistry and tree architecture (both above- and belowground), which can affect diverse organisms and ecosystem processes. Second, empirical studies in the wild show that the local patterns of genetics based community structure scale up to western North America. At multiple spatial scales the arthropod community phenotype is related to the genetic distance among plants that these arthropods depend upon for survival. Third, we suggest that the familiar species-area curve, in which species richness is a function of area, is also a function of genetic diversity. We find that arthropod species richness is closely correlated with the genetic marker diversity and trait variance suggesting a genetic component to these curves. Finally, we discuss how genetic variation can interact with environmental variation to affect community attributes across geographic scales along with conservation implications.

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.

From genes to geography: a genetic similarity rule for arthropod community structure at multiple geographic scales.

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.

Community heritability measures the evolutionary consequences of indirect genetic effects on community structure.

The evolutionary analysis of community organization is considered a major frontier in biology. Nevertheless, current explanations for community structure exclude the effects of genes and selection at levels above the individual. Here, we demonstrate a genetic basis for community structure, arising from the fitness consequences of genetic interactions among species (i.e., interspecific indirect genetic effects or IIGEs). Using simulated and natural communities of arthropods inhabiting North American cottonwoods (Populus), we show that when species comprising ecological communities are summarized using a multivariate statistical method, nonmetric multidimensional scaling (NMDS), the resulting univariate scores can be analyzed using standard techniques for estimating the heritability of quantitative traits. Our estimates of the broad-sense heritability of arthropod communities on known genotypes of cottonwood trees in common gardens explained 56-63% of the total variation in community phenotype. To justify and help interpret our empirical approach, we modeled synthetic communities in which the number, intensity, and fitness consequences of the genetic interactions among species comprising the community were explicitly known. Results from the model suggest that our empirical estimates of broad-sense community heritability arise from heritable variation in a host tree trait and the fitness consequences of IGEs that extend from tree trait to arthropods. When arthropod traits are heritable, interspecific IGEs cause species interactions to change, and community evolution occurs. Our results have implications for establishing the genetic foundations of communities and ecosystems.

A genetic similarity rule determines arthropod community structure.

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.

Positive interactions between leafrollers and other arthropods enhance biodiversity on hybrid cottonwoods.

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.