Molecular mechanisms of fungal manipulation of ant behaviour
One of the most dramatic examples of parasites changing host behaviour is that of Ophiocordyceps fungi infecting and manipulating ants. Fungal spores infect ants while they forage for food. During the course of infection, the fungus gradually changes the behaviour of its ant host, ultimately making the ant leave the nest to climb up the vegetation where it latches on with its mandibles (Fig. 1). This manipulated biting is a completely novel behaviour induced by the fungus and is not part of the regular behaviour as observed in healthy ants. It is also called the “death grip” since manipulated ants will stay in this position where the fungus finally kills them. The parasite then uses the ant’s tissues as a carbon source to grow a fruiting body from between the ant’s thorax and head, which releases infective ascospores for transmission (Fig. 2) [1,2].
Figure 1: Lab-infected manipulated ant
Figure 2: Naturally infected manipulated ant with fungal fruiting body
This parasite-host interaction represents a great model system for studies into parasitic manipulation of host behaviour since the manipulation is a) very apparent, b) clearly adaptive to the parasite, and c) reproducible in controlled laboratory infections.
Infection studies combined with behavioural observations and metabolomics analyses of he fungal secretome suggest that the interactions between the fungal parasite and the ant brain that lead to manipulated biting are very species-specific . Moreover, genomics and transcriptomics analyses revealed that Ophiocordyceps unilateralis employs a rather unique set of genes during the manipulated biting event when compared to the genomes of other fungal entomopathogens of the order Hypocreales . These studies have also led to the reporting of the very first candidate genes, compounds and pathways that could be involved in the fungal manipulation of ant behaviour.
Having established these recent advances I am now asking the following research questions:
- How has the parasitic ability to control the insect brain evolved?
I am using comparative genomics techniques towards answering this question.
- Which fungal genes are essential to establish behavioural manipulation and what is their function?
I am currently developing the molecular tools to functionally analyse the proposed “manipulator genes”
- How could the molecular biological clock be involved in the parasite-host interactions that eventually lead to an altered behavioural output?
I am using experimental chronobiology set ups to elucidate the molecular clock of Ophiocordyceps unilateralis and study the influence of circadian rhythms in infection and manipulation. This work is done in collaboration with the lab of Prof. Martha Merrow at the Institute of Medical Psychology within the Medical Faculty of the LMU.
1. Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J et al. (2009) The life of a dead ant: The expression of an adaptive extended phenotype. American Naturalist 174: 424-33
2. Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC ecology 11:13
3. de Bekker C, Quevillon LE, Smith PB, Fleming KR, Ghosh D, Patterson AD et al. (2014) Species-specific ant brain manipulation by a specialized fungal parasite. BMC evolutionary biology 14:166
4. de Bekker C, Ohm RA, Loreto RG, Sebastian A, Albert I, Merrow M et al. (2015) Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC genomics 16:620
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