Experimental coevolution of species interactions

doi:10.1016/j.tree.2013.02.009

Trends in Ecology & Evolution

Volume 28, Issue 6, June 2013, Pages 367-375

https://doi.org/10.1016/j.tree.2013.02.009 Get rights and content

Coevolution, the process of reciprocal adaptation and counter-adaptation between ecologically interacting species, affects most organisms and is considered a key force structuring biological diversity. Our understanding of the pattern and process of coevolution, particularly of antagonistic species interactions, has been hugely advanced in recent years by an upsurge in experimental studies that directly observe coevolution in the laboratory. These experiments pose new questions by revealing novel facets of the coevolutionary process not captured by current theory, while also providing the first empirical tests of longstanding coevolutionary ideas, including the influential Red Queen hypothesis. In this article, we highlight emerging directions for this field, including experimental coevolution of mutualistic interactions and understanding how pairwise coevolutionary processes scale up within species-rich communities.

Section snippets

The rise of experimental coevolution

Naturalists have long recognized the importance of species interactions as a driving force of adaptation. Indeed, 19th-century evolutionary biologists often cited the conspicuous co-adaptations of interspecific pollination and mimicry mutualisms (see Glossary) as exemplars of evolution by natural selection. It is perhaps surprising then that coevolution, the process of reciprocal adaptation and counter-adaptation by ecologically interacting species, was not studied in earnest until the mid-20th

The tempo and mode of antagonistic coevolution

According to the Red Queen hypothesis, reciprocal selection arising from interspecific antagonisms, such as host–parasite interactions, should accelerate evolutionary rates through the need for continual adaptation and counter-adaptation 8, 9. (The history of the use of the Red Queen metaphor is described in 10, 11.) Recent tests of this prediction have compared evolutionary rates under coevolution against controls where coevolution is prevented, for example, in the presence versus absence of

Emerging directions in experimental coevolution

The major contributions of experimental coevolution thus far have been to provide direct evidence of the tempo and mode of antagonistic coevolutionary dynamics, the role of antagonistic coevolution in increasing diversity within and among populations, including the role of parasitism in maintaining sexual recombination, and the structure of specificity in coevolving antagonistic interactions. However, as the field matures, it is taking some exciting new directions; in what follows, we outline

Concluding remarks and potential for application

Overall, experimental evolution has afforded remarkable strides forward in understanding population-level responses to selection, the underlying genetics of adaptation, and the limits of evolution [64]. Although still in its infancy, experimental coevolution has great potential for informing understanding of community stability, species invasions, and the spread of disease and, as such, holds promise in more applied fields, most notably human health. Experimental coevolution techniques have

Acknowledgments

We are grateful to the reviewers for constructive comments on a previous version of this manuscript. This work was supported by a project grant (NE/H005080/1) to M.A.B. and a research fellowship (R16150) to B.K. from the Natural Environment Research Council (UK).

Glossary

Antagonistic coevolution and/or interspecific antagonism: coevolution is the reciprocal adaptation and counter-adaptation of species that interact ecologically. When the fitnesses of the two species are negatively correlated, such that an adaptation that increases fitness in one species decreases in the fitness of the other species and vice versa, these species interactions are termed ‘antagonistic’.
Antagonistic pleiotropy: a situation where one gene underlies more than one trait, and where one

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Trends in Ecology & Evolution

ReviewExperimental coevolution of species interactions

Section snippets

The rise of experimental coevolution

The tempo and mode of antagonistic coevolution

Emerging directions in experimental coevolution

Concluding remarks and potential for application

Acknowledgments

Glossary

Trends Ecol. Evol.

Trends Ecol. Evol.

Coevolution of mutualism between ants and acacias in Central America

Evolution

Butterflies and plants: a study in coevolution

Evolution

Host–parasite ‘Red Queen’ dynamics archived in pond sediment

Nature

Coevolution of Escherichia coli and bacteriophages in chemostat culture

Science

Co-evolution of a virus–alga system

Appl. Microbiol.

Complex community in a simple habitat: experimental study with bacteria and phage

Ecology

A new evolutionary law

Evol. Theory

The Masterpiece of Nature: The Evolution and Genetics of Sexuality

Running with the Red Queen: refelctions on ‘Sex versus non-sex versus parasite’

Oikos

Sex, death and the Red Queen

Science

Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite

Proc. Natl. Acad. Sci. U.S.A.

Antagonistic coevolution accelerates molecular evolution

Nature

Ongoing phenotypic and genomic changes in experimental coevolution of RNA bacteriophage Qβ and Escherichia coli

PLoS Genet.

Host–parasite coevolution and patterns of adaptation across time and space

J. Evol. Biol.

Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode

Evolution

Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways

Evolution

Modelling infection as a two-step process combining gene-for-gene and matching-allele genetics

Proc. R. Soc. Lond. B

Host–parasite coevolutionary arms races give way to fluctuating selection

Ecol. Lett.

Local adaptation and the geometry of host–parasite coevolution

Ecol. Lett.

Coevolution with viruses drives the evolution of bacterial mutation rates

Nature

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BMC Evol. Biol.

Influence of co-evolution with a parasite, Nosema whitei, and population size on recombination rates and fitness in the red flour beetle, Tribolium castaneum

Genetica

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Science

Coevolution drives temporal changes in fitness and diversity across environments in a bacteria–bacteriophage interaction

Evolution

Rapid diversification of coevolving marine Synechococcus and a virus

Proc. Natl. Acad. Sci. U.S.A.

Antagonistic coevolution with parasites maintains host genetic diversity: an experimental test

Proc. R. Soc. Lond. B

The role of parasites in sympatric and allopatric host diversification

Nature

The effect of migration on local adaptation in a coevolving host–parasite system

Nature

Adaptation varies through space and time in a coevolving host–parasitoid interaction

Nature

How does spatial dispersal network affect the evolution of parasite local adaptation?

Evolution

A meta-analysis of factors affecting local adaptation between interacting species

Am. Nat.

A synthesis of experimental work on parasite local adaptation

Ecol. Lett.

The Coevolutionary Process

The Geographic Mosaic of Coevolution

Abiotic heterogeneity drives parasite local adaptation in coevolving bacteria and phages

J. Evol. Biol.

The effect of spatial heterogeneity and parasites on the evolution of host diversity

Proc. R. Soc. Lond. B

Review
Experimental coevolution of species interactions