Insects: slaves in a fungal nation

Imagine you are a Yellow Dung-fly, let’s say a common species like Scathophaga stercoraria. It is a warm summer’s day and you are flying around a grassy meadow peppered with juicy cow-pats. Just the sort of cow-pats frequented by the other flies you prey upon, and where your species’ larvae will develop. Marvellous. Then however, you get a strange urge. The urge is telling you to climb to the top of a tall grass stem. You obey. When you get there, the urge tells you to do the following:

1. Turn so that your head is facing downwards;
2.  Evert your proboscis and attach it to the plant;
3. Raise your abdomen and spread your wings;
4. Stay!

And this is exactly what you do, until some hours later you die in this position and sporangia erupt from your remains, spore dispersal enhanced by the position you have adopted... Yes, you were infected by a fungus of the genus Entomophthora (literally ‘insect-destroyer’) which parasitised you, changed your behaviour (causing what is sometimes known as ‘summit disease’), then killed you, after which spores were dispersed physically (e.g. by wind) or directly to male flies that tried to mate with you. But how did the fungus do that?

The changed behaviour described above was investigated by Maitland (1994) and has been written about widely, including no doubt many ‘Introductory Mycology’ texts and modules. Unsurprisingly however, fewer column-inches seem to have been devoted to the detailed processes that occur after infection by spores, particularly what takes place after hyphae reach the fly’s brain.

Scathophaga stercoraria assumes the position - note released spores...

...and in plan view.

Looking at somewhat older work, Humber (1976) noted that fungi of the related genus Strongwellsea produced numerous fungal nuclei in the brain neuropile and thoracic ganglia of host flies. Having penetrated the abdominal nerves, hyphae grew forward between the neurons without apparent damage and without affecting host's behaviour. Could this be the route through which Entomophthora subsequently does affect host behaviour? Possibly, but this still doesn’t explain how behaviour is changed, only how the fungus gets into a position to do so.

One reason why a clear answer isn’t forthcoming is that, as yet, there isn’t a clear one – however, research is ongoing e.g. at Harvard’s Rowland Institute where they are investigating whether the neural circuitry infected by Entomophthora includes geotactic (‘which way’s up?’) Polarity Control Neurones.

[** STOP PRESS ** Ben de Bivort from the Harvard lab mentioned above has just been in touch to let me know that their research on Entomophthora has ceased, for now at least. They have a working culture system  for the fungus, but couldn't establish an infection in their model system, Drosophila melanogaster, even by injecting high concentrations of cultured cells directly into the abdomen. Research may restart at some point, but for now it seems that either D. melanogaster was resistant, cell injection doesn't work (maybe another process is needed prior to infection?), and/or something else is going on entirely.]

There are however interesting parallels with Entomophthora infection in other species groups. For example, in Wood Ants Formica rufa, the fungus E. ovispora appears to release a dormant Hymenopteran sleeping behaviour which manifests as ‘summit disease’ as the ants climb grass stems which they then grip with their mandibles; some individuals are even glued to the stem by fungal attachments (Roy et al. 2006). Infected ants contain the greatest density of hyphae around the sub-oesophageal and protocerebral nerve ganglia (Loos-Frank & Zimmermann 1976) and it will be interesting to see how this compares with findings from the Rowland Institute. Certainly, Salwiczek & Wickler (2009) consider that parasites such as Entomophthora can only utilise existing, if dormant, behaviour rather than inducing entirely new behaviours.

The taxonomy bit: The genus Entomophthora is generally placed in the family Entomophthoraceae, order Entomophthorales within the Zygomycetes, those fungi which produce sexual spores and have a vegetative mycelium largely lacking septa. For more detailed descriptions of relevant taxa, see here. Taxonomic and descriptive work is ongoing although not all molecular systematic evidence agrees, for example see James et al. (2006) and Thorn et al. (2007).

References

Humber, R.A. (1976). The systematics of the genus Strongwellsea (Zygomycetes: Entomophthorales). Mycologia 68: 1042-1061.

James, T. Y., Kauff, F., Schoch, C.L., Matheny, P.B., Hofstetter, V., Cox, C.J. & Celio, G. (2006). Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-823.

Loos-Frank, B. & Zimmermann, G. (1976). Über eine dem Dicrocoelium-Befall analoge Verhaltensänderung bei Ameisen der Gattung Formica durch einen Pilz der Gattung Entomophthora. Zeitschrift für Parasitenkunde 49: 281-289.

Maitland, P. (1994). A parasitic fungus infecting yellow dungflies manipulates host perching behaviour. Proceedings of the Royal Society of London B 258: 187–193.

Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E. & Pell, J.K. (2006). Bizarre interactions and endgames: Entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology 51: 331-357.

Salwiczek, L.H. & Wickler, W. (2009). Parasites as scouts in behaviour research Ideas in Ecology and Evolution, 2, 1-6 DOI: 10.4033/iee.2009.2.1.c

Thorn, R.G., Tibell, L., Untereiner, W.A, Walker, C., Wang, Z., Weir, A., Weiss, M., White, M.M., Winka, K., Yao, Y.-J. & Zhang, N. (2007). A higher-level phylogenetic classification of the Fungi. Mycological Research 111(5): 509-547.