Review
The evolution of mutualisms: exploring the paths between conflict and cooperation

https://doi.org/10.1016/S0169-5347(98)01529-8Get rights and content

Abstract

Mutualisms are of fundamental importance in all ecosystems but their very existence poses a series of challenging evolutionary questions. Recently, the application of molecular analyses combined with theoretical advances have transformed our understanding of many specific systems, thereby contributing to the possibility of a more general understanding of the factors that influence mutualisms.

Section snippets

Current theory of conflict, cooperation and constraint

The potential for conflicts of interest to shape or destabilize mutualistic associations will depend on the extent to which the survival and reproductive interests of the symbiont align with those of the host. Given that conflicts of interest can occur even within the genomes of single individuals5, 6, 20, it seems unlikely that the interests of mutualists will ever be completely concordant.

Although there is no general theory of mutualism, several factors that can help align mutualists'

Identifying the players

Determining the number and identities of the participants in mutualistic associations is a necessary first step for any evolutionary analysis, but it can be a surprisingly nontrivial task. Hosts and symbionts often lose characters found in their closest free-living relatives, or gain novel characters, making them difficult to distinguish and characterize taxonomically. The traditional solution for bacterial and fungal symbionts has been culturing. However, in some symbioses, what is

Patterns of ecological transmission and evolutionary association

For patterns of transmission, it is useful to distinguish between transmission over ecological (generation to generation) and longer evolutionary (lineage to lineage) timescales. For example, systems dominated by strict vertical ecological transmission might be expected to produce concordant phylogenies between host and symbiont at all taxonomic scales, whereas in systems dominated by horizontal transmission, this outcome might be thought to be less likely.

The explosion of systematic analyses

Trajectories of costs and benefits

Molecular data can provide a window on the taxonomic identities of mutualists, the structuring of their extant populations (e.g. patterns of spatial distribution and ecological transmission), their histories of phylogenetic associations and their evolutionary origins14, 28, 29, 34, but provide relatively little information about the often rapid, and sometimes convoluted, evolutionary trajectories of costs and benefits received4, 8.

From studies that compare outcomes across several populations of

Mutualisms and rates of molecular evolution

In those instances in which the host and mutualist cospeciate, the absolute times of divergence between pairs of cospeciating mutualists are effectively held constant. This allows a series of potentially instructive comparisons to be made in the accumulation of substitutions in homologous DNA sequences. First, comparisons can be made between the accumulation of substitutions at a given gene or set of genes in the ‘host’ and in the ‘symbiont’ (or parasite). Second, comparisons can be made

Conclusions

Most organisms are involved either directly or indirectly in mutualistic interactions. However, there is no general theory of mutualism that approaches the explanatory power that ‘Hamilton's Rule’ appears to hold for the understanding of within-species interactions. Underlying problems revolve around explicitly defining vague terms, such as ‘alignment of interest’, and employing biologically realistic currencies (i.e costs and benefits) at biologically relevant scales of organization. Ideally,

Unlinked references

44, 45, 46

Acknowledgements

We thank Koos Boomsma and Jack Werren for stimulating discussion. We thank Betsy Arnold, Jenny Apple, Egbert Leigh, Elisabeth Kalko, Sadie Jane Ryan, Andy Dobson, Jon Howe, Penny Barnes, Andrew Baker, Rob Rowan, DeWayne Shoemaker and Rod Page for help and useful comments during the evolution of this article. STRI Post Doctoral Fellowships supported SAR and UGM and made this collaboration possible.

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