Open Access Highly Accessed Research article

Species-specific ant brain manipulation by a specialized fungal parasite

Charissa de Bekker1*, Lauren E Quevillon1, Philip B Smith2, Kimberly R Fleming1, Debashis Ghosh3, Andrew D Patterson24 and David P Hughes1*

Author Affiliations

1 Department of Entomology and Department of Biology, Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, State College, Pennsylvania 16802, PA, USA

2 Metabolomics Core Facility, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, State College, Pennsylvania 16802, PA, USA

3 Department of Statistics and Public Health Sciences, Pennsylvania State University, University Park, State College, Pennsylvania 16802, PA, USA

4 Center for Molecular Toxicology and Carcinogenesis, Department of Veterinary and Biomedical Sciences, Pennsylvania State University, University Park, State College, Pennsylvania 16802, PA, USA

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BMC Evolutionary Biology 2014, 14:166  doi:10.1186/s12862-014-0166-3

Published: 29 August 2014

Abstract

Background

A compelling demonstration of adaptation by natural selection is the ability of parasites to manipulate host behavior. One dramatic example involves fungal species from the genus Ophiocordyceps that control their ant hosts by inducing a biting behavior. Intensive sampling across the globe of ants that died after being manipulated by Ophiocordyceps suggests that this phenomenon is highly species-specific. We advance our understanding of this system by reconstructing host manipulation by Ophiocordyceps parasites under controlled laboratory conditions and combining this with field observations of infection rates and a metabolomics survey.

Results

We report on a newly discovered species of Ophiocordyceps unilateralis sensu lato from North America that we use to address the species-specificity of Ophiocordyceps-induced manipulation of ant behavior. We show that the fungus can kill all ant species tested, but only manipulates the behavior of those it infects in nature. To investigate if this could be explained at the molecular level, we used ex vivo culturing assays to measure the metabolites that are secreted by the fungus to mediate fungus-ant tissue interactions. We show the fungus reacts heterogeneously to brains of different ant species by secreting a different array of metabolites. By determining which ion peaks are significantly enriched when the fungus is grown alongside brains of its naturally occurring host, we discovered candidate compounds that could be involved in behavioral manipulation by O. unilateralis s.l.. Two of these candidates are known to be involved in neurological diseases and cancer.

Conclusions

The integrative work presented here shows that ant brain manipulation by O. unilateralis s.l. is species-specific seemingly because the fungus produces a specific array of compounds as a reaction to the presence of the host brain it has evolved to manipulate. These studies have resulted in the discovery of candidate compounds involved in establishing behavioral manipulation by this specialized fungus and therefore represent a major advancement towards an understanding of the molecular mechanisms underlying this phenomenon.

Keywords:
Behavioral manipulation; Host specificity; Secretome; Metabolomics; Ophiocordyceps unilateralis