REVIEWS A framework for community and ecosystem genetics: from genes to ecosystems Thomas G. Whitham*‡, Joseph K. Bailey*‡§, Jennifer A. Schweitzer ‡§||, Stephen M. Shuster*‡, Randy K. Bangert*‡, Carri J. LeRoy*‡¶, Eric V. Lonsdorf*‡#, Gery J. Allan*‡, Stephen P. DiFazio**, Brad M. Potts‡‡, Dylan G. Fischer¶, Catherine A. Gehring*‡, Richard L. Lindroth§§, Jane C. Marks*‡, Stephen C. Hart‡||, Gina M. Wimp|||| and Stuart C. Wooley §§ Abstract | Can heritable traits in a single species affect an entire ecosystem? Recent studies show that such traits in a common tree have predictable effects on community structure and ecosystem processes. Because these ‘community and ecosystem phenotypes’ have a genetic basis and are heritable, we can begin to apply the principles of population and quantitative genetics to place the study of complex communities and ecosystems within an evolutionary framework. This framework could allow us to understand, for the first time, the genetic basis of ecosystem processes, and the effect of such phenomena as climate change and introduced transgenic organisms on entire communities. 1 community energy flow Community and ecosystem Jeffry Mitton asserted that the elaboration of fundamental processes such as or nutrient genetics and ecosystem genetics could “herald a new era in evolu­ cycling. Examination of the role of genetic interactions The study of the genetic tionary biology” and that “if this comes about, evolution­ at the ecosystem level begins a new era of evaluating interactions that occur ary biology and ecology will be more tightly linked than ecosystems within an evolutionary framework. between species and their ever before.” Although great strides have been made in Although the genetic analysis of a complex commu­ abiotic environment in complex communities. understanding the ecology and evolution of two-species nity or ecosystem might seem to be a hopeless quagmire, interactions since Ehrlich and Raven2, only recently recent advances have made it possible to develop a model Community have scientists begun to consider evolution in a broader system that is centred on the Populus species. Populus is An association of interacting community3–22 and ecosystem23–32 context. Furthermore, the only system with documented links between a phy­ species that live in a particular multi-level selection 33–37 quantitative trait locus area. although theory has advanced , it tochemical , a community of diverse has not been incorporated into the prevailing models of organisms and important ecosystem processes19,21,27–30,41–43. Ecosystem community organization and ecosystem dynamics38–40. It is also the first tree genome to be sequenced44–46, which A biotic community and its A major deterrent to advancing community and will facilitate the integration of diverse disciplines. This abiotic environment. ecosystem genetics is the overwhelming number of spe­ review focuses on this gene-to-ecosystem integration cies that comprise even simple communities, and the and the implications of these links. We also discuss how complexity of the interactions that involve diverse taxa. similar findings in other systems support a community However, it is important that we make this conceptual and ecosystem genetics perspective, suggesting that these *Department of Biological leap because species do not evolve in a vacuum. Rather, findings are widely applicable. Sciences, Northern Arizona they are embedded within matrices of hundreds of spe­ The study of poplars — in the wild, in common gardens University, Flagstaff, Arizona 86011, USA. cies that coexist in variable environments. Understanding with replicated clones and with crosses of known pedi­ ‡Merriam-Powell Center for this frontier requires placing the community and ecosys­ gree — has allowed three conceptual advances. First, the Environmental Research, tem within an evolutionary framework that is defined by genetic analysis of foundation species can tell us much Northern Arizona University. the genetic interactions that exist among their compo­ about an ecosystem. Ecologists have long recognized that Correspondence to T.G.W. (BOX 1) e-mail: Thomas. nent species . From an ecosystem science perspec­ relatively few species ‘drive’ community structure and 47 [email protected] tive, this is an especially important advance as this field ecosystem processes . The genetic analysis of poplars, a doi:10.1038/nrg1877 has not previously incorporated genetics into studies of foundation species, reveals the structure and function of 510 | JULY 2006 | VOLUME 7 www.nature.com/reviews/genetics © 2006 Nature Publishing Group REVIEWS Multi-level selection a diverse ecosystem. Second, the predictable effects of such selection changes the nature of genetic interactions Selection that occurs when genes in foundation species extend to higher levels, among species, community evolution occurs. relative fitness depends on the which can be quantified as community and ecosystem properties of individuals, as phenotypes. Just as the genotype might have a ‘traditional’ Community and ecosystem phenotypes of genes well as on the properties of the phenotype that is expressed within the individual and The traditional phenotype is the sum of direct genetic group(s) to which individuals belong. its population, gene expression that leads to interactions and environmental influences on individual trait expres­ with other species extends to levels that are higher than sion. By contrast, community and ecosystem phenotypes Energy flow the population to produce community and ecosystem arise from interactions with other species that comprise The movement of energy from phenotypes27. Third, the community and ecosystem the community. Whether particular species contribute one species to another throughout an ecosystem (see heritability of these phenotypes can be quantified using to community phenotypes depends on how genetically also ‘trophic interactions’). standard community statistical tools, which can then be based traits within species interact to influence the fit­ analysed using established methods for population and ness of other species. Recent findings suggest that the Quantitative trait locus quantitative genetics analysis20,21. Documenting herita­ variation in community and ecosystem phenotypes that A genetic locus that is bility at levels higher than the population is an important is associated with a foundation species can indeed have a identified through statistical associations between mapped advance in community and ecosystem genetics. genetic basis and result from indirect genetic effects (IGEs), genetic markers and complex Because so few studies have merged the continuum in which the phenotype of one organism is part of the traits (such as growth rate or from gene to ecosystem, we believe advances with the environment of another36. This hypothesis is supported body form). Populus model system can illustrate emerging concepts by studies of multi-level selection33–35,48,49 in which the fit­ Common garden and areas for research in other systems. Although there ness consequences of IGEs among individuals of the same 50 An experimental approach are many challenges to this level of integration (see final species are important in group and social evolution . involving planting individuals at section), the widespread recognition of the importance of An analogous mechanism involves IGEs among the same field site so that all 20 integration by researchers and funding agencies provides species, or interspecific indirect genetic effects (IIGEs) , individuals experience the new opportunities that were previously unavailable. Here wherein the environmental influences on the pheno­ same environmental conditions. Observed differences in the we examine the logical and sometimes controversial type of one species are due to the expression of genes phenotypes among plants implications of community and ecosystem phenotypes. in another species. When IIGEs exist, genetically based are assumed to be genetically Do they feed back to affect the fitness of the individual ecological interactions between individuals in different based rather than 27,51 expressing the trait? Do communities and ecosystems species can evolve . Therefore, IIGEs provide a means environmentally based. evolve? Will the community and ecosystem phenotypes for communities to become genetically and demographi­ Foundation species of genetically modified organisms negatively affect cally distinct. In other words, these indirect interactions Species that structure a the environment? Is it important to conserve genetic result in different communities of organisms (such as community by creating locally variation in foundation species that are common? insects or microbes) becoming associated with geneti­ stable conditions for other 9,12,13,17,20,21 In the next three sections we argue that community cally distinct plants or animals to form unique species, and by modulating and stabilizing fundamental and ecosystem phenotypes exist, that their heritability community phenotypes. Genetically based variation ecosystem processes. can be quantified, and that the interactions of species can in community and ecosystem phenotypes have so far lead to community evolution. We emphasize that this trait- been found in eight systems (BOX 2). Community and ecoystem based approach, although computationally analogous phenotypes The effects of genes at levels to the analysis of quantitative traits, does not imply or Effects of tannin levels in leaves as an example. If the higher than