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A framework for community and ecosystem genetics: from genes to ecosystems

Key Points

  • The fact that genetic traits in one species can affect an entire ecosystem has important basic and applied implications that are only now being appreciated. The potential sphere of gene influence can be expanded from the individual and population level (that is, population genetics) to the higher levels included in community and ecosystem genetics. When this is done new fields of study are likely to emerge, such as community and ecosystem genomics.

  • Just as the genotype has a 'traditional' phenotype that is expressed in the individual and population, its expression could also extend to levels higher than the population, to produce community and ecosystem phenotypes.

  • Using traditional population and quantitative genetics methods we show that these community and ecosystem phenotypes are heritable and that some are likely to feed back to affect the fitness of the tree.

  • These combined effects provide a mechanism for exploring the controversial issue of community and ecosystem evolution (that is, the change in genetic interactions between species over time).

  • We show how a mapped trait in a common tree predictably affects the structure and composition of the arthropod community in the canopy of the tree, the microbial community in the soil, the detritivore community in an adjacent stream, the foraging of a mammalian herbivore, and the interactions of different trophic levels. In turn, these interactions predictably affect important ecosystem processes such as litter decomposition and nitrogen mineralization.

  • Future studies will need to evaluate how genetic changes in foundation species — brought about by exotic introductions, genetic engineering and climate change — will result in new community and ecosystem phenotypes. These new phenotypes can affect community structure, biodiversity and fundamental ecosystem processes such as nutrient cycling.

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.

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Figure 1: Genetic variation within species structures the arthropod community.
Figure 2: Feedback relationships.
Figure 3: Arthropod composition is correlated with genetic composition and diversity.

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Acknowledgements

We thank a US National Science Foundation Frontiers of Integrative Biological Research grant for bringing together diverse scientists to help integrate and develop the emerging field of community and ecosystem genetics. The Australian Research Council supported parallel studies in Australia. The Ogden Nature Center, the Utah Department of Natural Resources and the Bureau of Reclamation provided lands for common gardens, restoration and public outreach. We thank P. Keim for his support and comments. Thanks also to three anonymous reviewers for their thoughtful comments that improved the manuscript.

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Correspondence to Thomas G. Whitham.

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Related links

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DATABASES

Entrez Genome Project

Populus tremuloides

Populus trichocarpa

FURTHER INFORMATION

ARC Research Network for Understanding and Managing Australian Biodiversity

Carrie J. LeRoy's homepage

Dylan Fischer's laboratory

Genetic Improvement Program

Laboratory of Chemical Ecology — Rick Lindroth

Merriam-Powell Center for Environmental Research web site

Stephen C. Hart's homepage

The Cottonwood Ecology Group homepage

The International Populus Genome Consortium

UTAS School of Plant Science

Glossary

Community and ecosystem genetics

The study of the genetic interactions that occur between species and their abiotic environment in complex communities.

Community

An association of interacting species that live in a particular area.

Ecosystem

A biotic community and its abiotic environment.

Multi-level selection

Selection that occurs when relative fitness depends on the properties of individuals, as well as on the properties of the group(s) to which individuals belong.

Energy flow

The movement of energy from one species to another throughout an ecosystem (see also 'trophic interactions').

Quantitative trait locus

A genetic locus that is identified through statistical associations between mapped genetic markers and complex traits (such as growth rate or body form).

Common garden

An experimental approach involving planting individuals at the same field site so that all individuals experience the same environmental conditions. Observed differences in the phenotypes among plants are assumed to be genetically based rather than environmentally based.

Foundation species

Species that structure a community by creating locally stable conditions for other species, and by modulating and stabilizing fundamental ecosystem processes.

Community and ecoystem phenotypes

The effects of genes at levels higher than the population. These phenotypes result from interspecific indirect genetic effects, which can be summarized as a univariate trait.

Community and ecosystem heritability

The tendency for related individuals to support similar communities of organisms and ecosystem processes.

Community evolution

A genetically based change in the ecological interactions that occur between species over time.

Indirect genetic effects

An environmental influence on the phenotype of one individual that is due to the expression of genes in another individual of the same species.

Interspecific indirect genetic effects

An environmental influence on the phenotype of an individual in one species that is due to the expression of genes in another individual of a different species.

Fractal

A geometrical pattern, each part of which has the same statistical character as the whole.

Broad-sense heritability

The contribution of all genetic factors (additive, dominant, epistatic) to the total variance in phenotype. H2 is the broad-sense heritability of a traditional phenotype and H2C is the broad-sense heritability of a community or ecosystem phenotype.

Trophic interactions

Interactions within a community of species, each of which occupies a particular level in a food chain. Interaction across trophic levels represents the transfer of energy from primary producers to predators of herbivores.

Ordination technique

The ordering of multivariate data with respect to one or more axes.

Phenology

The study of the relationship of periodic biological phenomena such as flowering, breeding and migration to climatic conditions.

Endophyte

Describes organisms that at some time in their life cycle live within plant tissues without inducing symptoms in the host.

Line cross analysis and joint scaling test

A method of analysis that identifies the relative contributions of additive and dominant effects to the expression of a phenotype.

ANOVA

Analysis of variance. A statistical model for data analysis.

Narrow-sense heritability

The genetic component of phenotypic variance (additive only under random mating) that responds to natural selection.

Reciprocal transplant experiment

An experimental approach, which in this case involves quantifying the performance of individuals of two species when they are raised together. If coadaptation has occurred, individuals of both species that have had prolonged evolutionary contact should perform better together than individuals of the same species that have only recently come together or have not previously lived in association.

Geographical mosaic hypothesis

States that because species interactions vary geographically, a mosaic of population genetic structure will result that leads to different evolutionary trajectories.

Community and ecosystem genomics

The study of the composition and function of whole ecosystems using genomic data and methodology.

Bulked segregant analysis

A genome-wide scan for markers that differentiate pooled samples that have contrasting phenotypes.

Biodiversity

The number of species in an environment and their individual abundances.

Community metagenome

The amalgamated genetic composition of co-occurring species.

Microarray

A highly compact representation of a large number of diagnostic macromolecules (usually DNA) on glass slides or other solid substrates, allowing the assay of thousands of molecules simultaneously.

Genetic similarity rule

A rule according to which genetically similar plants should support similar communities, whereas genetically dissimilar plants should support dissimilar communities.

Minimum viable population size

The number of individuals required to sustain a population for a specific amount of time; for example, a probability of extinction of 1% in 1,000 years.

Minimum viable interacting population

The minimum size of a population that is required to maintain the genetic diversity at levels required by dependent and interacting species.

Exotic

A non-native species or even a gene that has been introduced into areas that are outside its native geographical distribution.

BT corn

Corn that has been genetically transformed with genes encoding insecticidal endotoxins that are derived from the bacterium Bacillus thuringiensis.

Roundup ready crops

Plants that have been genetically engineered to be resistant to the herbicide glyphosate.

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Whitham, T., Bailey, J., Schweitzer, J. et al. A framework for community and ecosystem genetics: from genes to ecosystems. Nat Rev Genet 7, 510–523 (2006). https://doi.org/10.1038/nrg1877

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