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On the origin of mutualisms

Pepijn Kooij
21 November 2016
Blog team: 
Pepijn Kooij, from Kew’s Comparative Plant and Fungal Biology department discusses the importance of understanding the evolution of mutualisms in reference to fungus-growing insects.

Despite what the title might suggest, it was not Charles Darwin but the Belgian researcher Pierre-Joseph van Beneden who first described the term ‘mutualism’ in 1876 in his book Animal Parasites and Messmates.

A mutualism (or mutualistic symbiosis) is a relationship between two or more organisms, where each partner benefits from living with the other. Mutualisms have shaped evolution in many ways, for example, animal and plant cells arose from a mutualism between different bacteria, with one forming the main cells and the other forming organelles such as mitochondria and chloroplasts. Therefore, trying to understand the evolution of mutualisms will help us understand the evolution of life in general.

Fungus-growing termites and leaf-cutting ants

Two famous examples of mutualisms are fungus-growing termites and leaf-cutting ants. These insects have a mutualistic relationship with a fungus that they have domesticated (Mueller et al, 2005). The insects depend on their fungal crops as a reliable food source, and, in return give protection to the fungi and aid their distribution.

Atta cephalotes leaf-cutting ants tending their fungus garden.jpg

Image showing Atta cephalotes leaf-cutting ants tending their fungus garden: the black and green fragments are plant material, white ‘fluff’ is the fungus, and the bright white dots are what the ants feed on, called gongylidia
Atta cephalotes leaf-cutting ants tending their fungus garden: the black and green fragments are plant material, white ‘fluff’ is the fungus, and the bright white dots are what the ants feed on, called gongylidia (Image: P. W. Kooij)

In both cases the insects have been farming their fungus for millions of years, which is a great deal longer than humans have practiced agriculture; a system that has been used for around 10,000 years.

This shows that the insects have been able to perfect their way of farming, with millions of years of experience; and we, as humans, might be able to learn something from them. For humans to be able to take advantage of this, it is important to know when it all started. But unfortunately, in both cases – as in many other mutualistic relationships – we have no idea what the domesticated partner’s closest ancestor is.

Why find the origin?

In most cases of mutualistic relationships, especially fungus-growing insects, it is likely that we will know the closest ancestor of only one of the partners (Ward et al, 2015; Legendre et al, 2015). For example, for both the ants and the termites there are well understood, established phylogenies. These phylogenies show us which non-fungus-farming species are related to those that use fungus as their food source. With this in mind, it is possible to make direct comparisons between mutualists and non-mutualists, to determine why the ants and termites evolved to farm fungi as their food source. Genome comparisons can reveal the genetic changes that allowed the insects to evolve in this way, but also why the fungus-growing insects are unable to live without their fungal crops.

The ancestry of the fungal crops, however, is still unknown. In general, it is assumed that the closest relative of the fungi cultivated by termites, Termitomyces, is the free-living species Tephrocybe rancida. However, with its distribution ranging from North America to Northern Europe, it is unlikely to be ancestor of Termitomyces, which, together with the termites has a distribution from South and Central Africa to Southeast Asia.

Termites on their fungus garden. The termites eat mostly the white bulbs called conidia. Picture by Duur K Aanen.jpg

Image showing termites on their fungus garden: the termites mostly eat the white bulbs called conidia
Termites on their fungus garden: the termites mostly eat the white bulbs called conidia (Image: D. K. Aanen)

The fungus cultivated by leaf-cutting ants is known to be related to the fungal genera Leucoagaricus and Leucocoprinus, but which species within these genera is still to be discovered. It is very important to thoroughly investigate this: performing comparison studies using the wrong species as the closest ancestor might lead to scientists drawing the wrong conclusions on the evolution and maintenance of the insect-fungus mutualisms.

Case study using the fungarium at Kew

At Kew we are the proud custodians of between 1 and 1.5 million fungal specimens, comprising a large part of known fungal diversity. In my attempt to find the closest ancestor of the fungus cultivated by leaf-cutting ants, Leucoagaricus gongylophorus, I descended into the fungarium to investigate any species that could possibly be related. By using this rich collection of fungal specimens and modern genetic tools I hope to trace the ancestor of the fungus cultivated by the leaf-cutting ants. I am still analysing data from over 300 specimens that I have been working with from the fungarium. Soon I hope to have a definitive answer as to which species of fungus started it all; and once I have achieved this, the results will open new ways of studying and understanding this intriguing collaboration between ants and their fungi. To be continued…

Me in the fungarium looking at mushrooms collected from an Atta cephalotes lab colony..jpg

Image showing me in the fungarium looking at mushrooms collected from an Atta cephalotes lab colony. Normally this fungus does not produce mushrooms, which makes this specimen very special.
Me in the fungarium looking at mushrooms collected from an Atta cephalotes lab colony. Normally this fungus does not produce mushrooms, which makes this specimen very special. (Image: A. C. Baquero Lozano)

- Pepijn -


References

Van Beneden, P. J. (1876). Animal parasites and messmates – The international scientific series Volume XIX, D. Appleton & Co, New York, 274p.

Legendre, F., Nel, A., Svenson, G. J., Robillard, T., Pellens, R., & Grandcolas, P. (2015). Phylogeny of dictyoptera: dating the origin of cockroaches, praying mantises and termites with molecular data and controlled fossil evidence. PLoS ONE 10 (7) e0130127. DOI: 10.1371/journal.pone.0130127. Available online

Mueller, U. G., Gerardo, N. M., Aanen, D. K., Six, D. L., & Schultz, T. R. (2005). The evolution of agriculture in insects. Annual Review Of Ecology Evolution And Systematics 36: 563–595. DOI: 10.1146/annurev.ecolsys.36.102003.152626. Available online

Ward, P. S., Brady, S. G., Fisher, B. L., & Schultz, T. R. (2014). The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Systematic Entomology 40(1), 6181. DOI: 10.1111/syen.12090. Available online

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