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The co-evolutionary genetics of ecological communities

Nature Reviews Genetics volume 8, pages 185–195 (2007)Cite this article

Key Points

  • Co-evolutionary genetics of ecological communities offers a new understanding of adaptation and gene function that cannot be obtained from genomic data without an ecological context.

  • Some interspecific interactions, such as those that involve host and pathogen or predator and prey, can be intensified by reciprocal co-evolution, whereas other interactions, such as competition over limiting resources, can be diminished by reciprocal co-evolution.

  • Molecular phylogenetics offers an historical context for studying species interactions, providing evidence for co-speciation and the means for distinguishing co-speciation from other processes, like duplication or host switching.

  • Genotype-by-environment interactions (G x E) have a central role in co-evolution. They have given rise to many unique co-evolutionary adaptations, such as the inducible defenses of many prey species, which are textbook cases of adaptive phenotypic plasticity and developmental switching.

  • Under some circumstances, G x E increases genetic diversity in both species that interact with each other. This kind of interspecific G x E holds the potential to be an engine of biodiversity by accelerating co-evolution and facilitating the co-speciation of hosts and pathogens, whenever ecological communities are subdivided and gene flow among them is reduced.

  • The same genetic theory that was used to describe the evolution of epistatic interactions (interactions between nuclear genes at different loci) can be used to describe the co-evolution of interacting species. Recognizing that co-evolution affects gene combinations between species (that is, interspecific epistasis), epistasis theory can be applied to co-evolution in ecological communities. Just as reductions in recombination facilitate selection on gene combinations, co-dispersal of hosts and symbionts facilitates selection on interspecific gene combinations and leads to a high degree of interspecific cooperation, as in reciprocal obligate symbioses.

  • The co-evolution of mitochondrial–nuclear gene combinations is a model to study the co-evolution of interspecific gene combinations.

Abstract

Co-evolution has produced many intriguing adaptations and made significant contributions to biodiversity through the co-adaptive radiations of interacting groups, such as pollinating insects and flowering plants or hosts and endosymbionts. New methods from molecular genetics and comparative genomics, in conjunction with advances in evolutionary genetic theory, are for the first time providing tools for detecting, investigating and understanding the genetic bases of the co-adaptive process and co-speciation. Advances in the emerging field of community genetics, which integrates genetics and community ecology, could revolutionize how co-evolution is studied, how genes are functionally annotated and how conservation geneticists implement preservation strategies.

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Figure 1: Example of an inducible defence in phytoplankton.
Figure 2: Co-evolutionary mutualism of figs and fig wasps.
Figure 3: Examples of tangled phylogenetic trees and co-speciation.
Figure 4: Co-dispersal of host and symbiont genes.

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Acknowledgements

I thank N. Priest, D. McCauley, J. Bever, Y. Brandvain, J. D. Van Dyken, T. Cruickshank, D. Drury, J. Thompson and D. Huestis for comments on the manuscript, and the US National Institutes of Health and the US National Science Foundation for support of this research.

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  1. Department of Biology, Indiana University, 1001 East Third Street, Bloomington, 47405-3700, Indiana, USA

    Michael J. Wade

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FURTHER INFORMATION

Figweb

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Myrmecos

Glossary

Geographic mosaic

A theory of community ecology that was founded on the premise that communities are genetically and ecologically subdivided so that the rate of co-evolution varies geographically, resulting in rapid co-evolution (hot spots) in some localities but slower co-evolution (cold spots) in others.

Congeners

Species that are members of the same genus.

Quorum sensing

Gene expression patterns in bacteria that are conditional on colony density.

Inducible defence

An adaptive phenotypic change in a prey species that develops in response to predation on conspecifics, which reduces vulnerability.

Trophic structure

The species interactions that make up food chains and energy flows through an ecological community.

Co-evolutionary arms race

The escalating and reciprocal co-evolution between the offensive ability of a predator and the defensive capability of its prey.

Life-history trade-off

A negative correlation between viability and the amount or timing of reproduction, such that an increase in one results in a concomitant decrease in the other.

Character displacement

Phenotypic differences between sympatric species that arise as an evolutionary response to competition for shared, limiting resources.

Red Queen hypothesis

The continual evolutionary change by a species that is necessary to retain its place in an ecosystem because of ongoing co-evolution by other species.

Darwinian extinction

A decline in mean fitness that occurs as a result of adaptation by natural selection, which reduces the size of the population until it becomes inviable.

Gene-for-gene model

A model of host–pathogen co-evolution that proposes that, for every gene in the host that confers resistance, there is a corresponding virulence gene in the pathogen.

Genotype-matching model

An ecological genetic model of host–pathogen co-evolution that proposes that rare host genotypes escape the more abundant pathogens, which are adapted to more common host genotypes, leading to oscillations in population size and genetic composition of both species.

Gene flow

The movement of genes from one population to another, as individuals leave their population of birth and become breeding members of another.

Synteny

The conservation of gene order over chromosome segments across taxa.

Random genetic drift

Random changes in allele frequency from one generation to the next.

Trophophoresy

The transporting of a species that is used for food by another species.

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Wade, M. The co-evolutionary genetics of ecological communities. Nat Rev Genet 8, 185–195 (2007). https://doi.org/10.1038/nrg2031

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