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Review
.2006 Jun 22;2(2):209-12.
doi: 10.1098/rsbl.2005.0424.

As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi

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Review

As you reap, so shall you sow: coupling of harvesting and inoculating stabilizes the mutualism between termites and fungi

Duur K Aanen. Biol Lett..

Abstract

At present there is no consensus theory explaining the evolutionary stability of mutualistic interactions. However, the question is whether there are general 'rules', or whether each particular mutualism needs a unique explanation. Here, I address the ultimate evolutionary stability of the 'agricultural' mutualism between fungus-growing termites and Termitomyces fungi, and provide a proximate mechanism for how stability is achieved. The key to the proposed mechanism is the within-nest propagation mode of fungal symbionts by termites. The termites suppress horizontal fungal transmission by consuming modified unripe mushrooms (nodules) for food. However, these nodules provide asexual gut-resistant spores that form the inoculum of new substrate. This within-nest propagation has two important consequences: (i) the mutualistic fungi undergo severe, recurrent bottlenecks, so that the fungus is likely to be in monoculture and (ii) the termites 'artificially' select for high nodule production, because their fungal food source also provides the inoculum for the next harvest. I also provide a brief comparison of the termite-fungus mutualism with the analogous agricultural mutualism between attine ants and fungi. This comparison shows that--although common factors for the ultimate evolutionary stability of mutualisms can be identified--the proximate mechanisms can be fundamentally different between different mutualisms.

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Figures

Figure 1
Figure 1
Schematic representation of the propagation ofTermitomyces fungus within aMacrotermes termite colony based on Leutholdet al. (1989). Within a fungus garden young workers (a) consume nodules (b), which are modified unripe mushrooms, so that young termites suppress horizontal transmission (c). Nodules contain asexual, gut-resistant spores that are the inoculum for new substrate (d) constructed by young workers on top of the existing fungus garden from plant material collected by older workers (e). This propagation is associated with bottlenecks, since only a small fraction of the spores in one within-nest generation (shown in red) forms nodules, which produce all the inoculum for the next generation. Furthermore, there is selection for the production of nodules, as any non-nodule-producing mutant (shown in black) will be selected against (f). The lowest, oldest fragments (g) of fungus garden are consumed by older workers so that there is a continuous turn over of material from top to bottom within a fungus garden.
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References

    1. Aanen D.K, Boomsma J.J. Evolutionary dynamics of the mutualistic symbiosis between fungus-growing termites and Termitomyces fungi. In: Vega F, Blackwell M, editors. Insect–fungal associations: ecology and evolution. Oxford University Press; Oxford: 2005. pp. 191–211.
    1. Aanen D.K, Eggleton P, Rouland-Lefèvre C, Guldberg-Frøslev T, Rosendahl S, Boomsma J.J. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc. Natl Acad. Sci. USA. 2002;99:14 887–14 992.doi:10.1073/pnas.222313099 - DOI - PMC - PubMed
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