Simulating selection and evolution at the community level using common garden data.

A key issue in evolutionary biology is whether selection acting at levels higher than the individual can cause evolutionary change. If it can, then conceptual and empirical studies must consider how selection operates at multiple levels of biological organization. Here, we test the hypothesis that estimates of broad-sense community heritability, H C 2 , can be used to predict the evolutionary response by community-level phenotypes when community-level selection is imposed. Using an approach informed by classic quantitative genetics, we made three predictions. First, when we imposed community-level selection, we expected a significant change in the average phenotype of arthropod communities associated with individual tree genotypes [we imposed selection by favoring high and low NMDS (nonmetric multidimensional scaling) scores that reflected differences in arthropod species richness, abundance and composition]. Second, we expected H C 2 to predict the magnitude of the community-level response. Third, we expected no significant change in average NMDS scores with community-level selection imposed at random. We tested these hypotheses using three years of common garden data for 102 species comprising the arthropod communities, associated with nine clonally replicated Populus angustifolia genotypes. Each of our predictions were met. We conclude that estimates of H C 2 account for the resemblance among communities sharing common ancestry, the persistence of community composition over time, and the outcome of selection when it occurs at the community level. Our results provide a means for exploring how this process leads to large-scale community evolutionary change, and they identify the circumstances in which selection may routinely act at the community level.

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.

Genetics-based interactions of foundation species affect community diversity, stability and network structure.

We examined the hypothesis that genetics-based interactions between strongly interacting foundation species, the tree Populus angustifolia and the aphid Pemphigus betae, affect arthropod community diversity, stability and species interaction networks of which little is known. In a 2-year experimental manipulation of the tree and its aphid herbivore four major findings emerged: (i) the interactions of these two species determined the composition of an arthropod community of 139 species; (ii) both tree genotype and aphid presence significantly predicted community diversity; (iii) the presence of aphids on genetically susceptible trees increased the stability of arthropod communities across years; and (iv) the experimental removal of aphids affected community network structure (network degree, modularity and tree genotype contribution to modularity). These findings demonstrate that the interactions of foundation species are genetically based, which in turn significantly contributes to community diversity, stability and species interaction networks. These experiments provide an important step in understanding the evolution of Darwin's 'entangled bank', a metaphor that characterizes the complexity and interconnectedness of communities in the wild.

Genotypic variation in foundation species generates network structure that may drive community dynamics and evolution.

Although genetics in a single species is known to impact whole communities, little is known about how genetic variation influences species interaction networks in complex ecosystems. Here, we examine the interactions in a community of arthropod species on replicated genotypes (clones) of a foundation tree species, Populus angustifolia James (narrowleaf cottonwood), in a long-term, common garden experiment using a bipartite "genotype-species" network perspective. We combine this empirical work with a simulation experiment designed to further investigate how variation among individual tree genotypes can impact network structure. Three findings emerged: (1) the empirical "genotype-species network" exhibited significant network structure with modularity being greater than the highly conservative null model; (2) as would be expected given a modular network structure, the empirical network displayed significant positive arthropod co-occurrence patterns; and (3) furthermore, the simulations of "genotype-species" networks displayed variation in network structure, with modularity in particular clearly increasing, as genotypic variation increased. These results support the conclusion that genetic variation in a single species contributes to the structure of ecological interaction networks, which could influence eco-ogical dynamics (e.g., assembly and stability) and evolution in a community context.

Genetics-based interactions among plants, pathogens, and herbivores define arthropod community structure.

Plant resistance to pathogens or insect herbivores is common, but its potential for indirectly influencing plant-associated communities is poorly known. Here, we test whether pathogens' indirect effects on arthropod communities and herbivory depend on plant resistance to pathogens and/or herbivores, and address the overarching interacting foundation species hypothesis that genetics-based interactions among a few highly interactive species can structure a much larger community. In a manipulative field experiment using replicated genotypes of two Populus species and their interspecific hybrids, we found that genetic variation in plant resistance to both pathogens and insect herbivores modulated the strength of pathogens' indirect effects on arthropod communities and insect herbivory. First, due in part to the pathogens' differential impacts on leaf biomass among the two Populus species and the hybrids, the pathogen most strongly impacted arthropod community composition, richness, and abundance on the pathogen-susceptible tree species. Second, we found similar patterns comparing pathogen-susceptible and pathogen-resistant genotypes within species. Third, within a plant species, pathogens caused a fivefold greater reduction in herbivory on insect-herbivore-susceptible plant genotypes than on herbivore-resistant genotypes, demonstrating that the pathogen-herbivore interaction is genotype dependent. We conclude that interactions among plants, pathogens, and herbivores can structure multitrophic communities, supporting the interacting foundation species hypothesis. Because these interactions are genetically based, evolutionary changes in genetic resistance could result in ecological changes in associated communities, which may in turn feed back to affect plant fitness.

Community specificity: life and afterlife effects of genes.

Community-level genetic specificity results when individual genotypes or populations of the same species support different communities. Our review of the literature shows that genetic specificity exhibits both life and afterlife effects; it is a widespread phenomenon occurring in diverse taxonomic groups, aquatic to terrestrial ecosystems, and species-poor to species-rich systems. Such specificity affects species interactions, evolution, ecosystem processes and leads to community feedbacks on the performance of the individuals expressing the traits. Thus, genetic specificity by communities appears to be fundamentally important, suggesting that specificity is a major driver of the biodiversity and stability of the world's ecosystems.

A genetic basis to community repeatability and stability.

Recent studies have shown that genetically based traits of plants can structure associated arthropod and microbial communities, but whether the effects are consistent and repeatable across years is unknown. If communities are both heritable (i.e., related individuals tend to support similar communities) and repeatable (i.e., the same patterns observed over multiple years), then plant genetics may also affect community properties previously thought to be emergent, such as "stability." Using replicated clones of narrowleaf cottonwood (Populus angustifolia) and examining an arthropod community of 103 species, we found that (1) individual tree genotypes supported significantly different arthropod communities, which exhibited broad-sense heritability; (2) these findings were highly repeatable over three consecutive years (repeatability = 0.91) indicating that community responses to individual tree genotypes are consistent from year to year; (3) differences among tree genotypes in community stability (i.e., changes in community composition over multiple years) exhibited broad-sense heritability (H(C)2 = 0.32). In combination, these findings suggest that an emergent property such as stability can be genetically based and thus subject to natural selection.