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Social evolution theory for microorganisms

Key Points

  • Microorganisms communicate and cooperate to perform a wide range of multicellular behaviours, such as dispersal, foraging, biofilm formation, 'chemical warfare' and quorum sensing.

  • Cooperative behaviour poses a problem to evolutionary theory, as it can potentially be exploited by cheaters who do not cooperate.

  • Kin selection theory provides an explanation for cooperation between individuals who share genes ? by helping a close relative to reproduce, an individual is still passing on its own genes to the next generation, albeit indirectly.

  • Kin selection can often be important in microorganisms because asexual reproduction and dispersal patterns mean that individual cells will often be surrounded by identical clones.

  • Cooperation between non-relatives, or even between species, can be explained if the cooperative behaviour provides a direct benefit to the individual who performs the behaviour, which outweighs the cost of performing the behaviour (that is, the cooperation is mutually beneficial).

  • A greater understanding of cooperation in microorganisms will come from combining evolutionary and mechanistic approaches.

Abstract

Microorganisms communicate and cooperate to perform a wide range of multicellular behaviours, such as dispersal, nutrient acquisition, biofilm formation and quorum sensing. Microbiologists are rapidly gaining a greater understanding of the molecular mechanisms involved in these behaviours, and the underlying genetic regulation. Such behaviours are also interesting from the perspective of social evolution ? why do microorganisms engage in these behaviours given that cooperative individuals can be exploited by selfish cheaters, who gain the benefit of cooperation without paying their share of the cost? There is great potential for interdisciplinary research in this fledgling field of sociomicrobiology, but a limiting factor is the lack of effective communication of social evolution theory to microbiologists. Here, we provide a conceptual overview of the different mechanisms through which cooperative behaviours can be stabilized, emphasizing the aspects most relevant to microorganisms, the novel problems that microorganisms pose and the new insights that can be gained from applying evolutionary theory to microorganisms.

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Figure 1: The problem of cooperation.
Figure 2: Some relationships between genetic relatedness (r) and social behaviours.
Figure 3: The costs and benefits of producing public goods.

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Acknowledgements

We thank M. Camara, B. Evans, K. Foster, N. Mehdiabadi, S. Molin, A. Ross-Gillespie, J. Strassman and P. Williams for useful discussion and comments on the manuscript, and the Royal Society, the Biotechnology and Biological Sciences Research Council and the Natural Environment Research Council (UK) for funding.

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Correspondence to Stuart A. West.

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DATABASES

Entrez Genome Project

Actinomyces naeslundii

Burkholderia cepacia

Dictyostelium discoideum

Escherichia coli

Myxococcus xanthus

Pseudomonas aeurginosa

Staphylococcus aureus

Streptococcus pneumoniae

Vibrio fischeri

FURTHER INFORMATION

The West group homepage

The Quorum Sensing website

Glossary

Virulence

The damage caused to the host by a parasite or pathogen, measured as the decrease in host fitness.

Cheater

An individual who does not cooperate (or cooperates less than their fair share), but can potentially gain the benefit from others cooperating.

Cooperation

A behaviour that benefits another individual (the recipient) and which is maintained (at least partially) because of its beneficial effect on the recipient.

Tragedy of the commons

A situation when individuals would do better to cooperate, but cooperation is unstable because each individual gains by selfishly pursuing their own short-term interests.

Public goods

A resource that is costly to produce, and provides a benefit to all the individuals in the local group or population.

Signal

Something that alters the behaviour of another individual, which evolved because of that effect, and which is effective because the receiver's response has also evolved.

Actor

A focal individual who performs a behaviour.

Direct fitness

The component of fitness gained through reproduction.

Repression of competiton

When the selfish advantage of cheats is removed.

Altruistic

A behaviour that increases another individual's fitness at a cost to one's own.

Kin selection

A process by which traits are favoured because of their beneficial effects on the fitness of relatives.

Indirect fitness

The component of fitness gained from aiding the reproduction of non-descendant relatives.

Hamilton's Rule

A condition (rb − c > 0) that predicts when a trait is favoured by kin selection, where c is the cost to the actor of performing the behaviour, b is the benefit to the individual who the behaviour is directed towards, and r is the genetic relatedness between those individuals.

Relatedness

A measure of genetic similarity.

Kin discrimination

When behaviours are directed towards individuals depending on their relatedness to the actor.

Cue

Something that can be used by an individual as a guide for future action.

Spiteful

A behaviour that decreases another individual's fitness at a cost to one's own.

Recipient

An individual who is affected by the behaviour of the actor.

Manipulate

When one behaviour alters the behaviour of another individual, usually to the benefit of the actor and to the cost of the other individual.

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West, S., Griffin, A., Gardner, A. et al. Social evolution theory for microorganisms. Nat Rev Microbiol 4, 597–607 (2006). https://doi.org/10.1038/nrmicro1461

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