Zombie Ants: Towards a Mechanistic Understanding of the Precise Control of Animal Behavior by a Microbial Parasite

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One of the most complex examples of symbiosis in nature is the precise manipulation of animal behavior by a microbe. Ophiocordyceps is a fungus that infects zombie ants. Infection of ant workers by thousands of these fungal cells causes the workers to leave the colony and die attached by their mandibles to plants that overhang the trails of ant colonies. There the fungus uses the dead ant bodies to produce spores that infect other ants. The manipulation is complex and spectacular given the fact that an organism without a brain controls the behavior of one with a brain. In this project the research team will use an integrative approach to ask how fungi change ants from being productive members of their colony to "fungi in ant's clothing?". The project will use measurement of gene expression, metabolism and tissue structure to ask how, during the 3 week period of infection, the fungi effectively take control of the ant. This work will provide many general insights into the nature of parasitism and may have broader societal relevance because these fungi are known to be important sources of small molecules with medical relevance. The work is relevant to the broader mission of NSF to increase scientific literacy as the zombie ant system has been shown to be a very useful tool for communicating the elegance and beauty of natural systems. How can a microbe control the central nervous system of an animal? Animals are intimately associated with microbes that span the symbiotic spectrum from mutualism to parasitism. In some cases, microbial parasites of animals have evolved to control animal behavior in ways that enhance parasite transmission. The zombie ants represent one prominent example. In this system a fungal parasite (Ophiocordyceps unilateralis) has evolved a precise level of behavioral control over the ants it infects. Worker ants infected by O. unilateralis move out from their colonies at precise times of day to highly specific locations on leaves in forests, where they bite into vegetation before dying. This altered behavior provides a platform for the eventual release of spores from a long fungal stalk that grows from the cadaver of the ant. This striking system involves an organism in one kingdom of life (Fungi) that controls the behavior of an organism in another (Animalia). How does an organism without a brain control the behavior of one with a brain? The investigators will address this using time series infectionstudies to measure chemical changes in both the parasite and its host. By using three different but complementary tools (serial block face scanning electron microscopy, metabolomics and transcriptomics) to examine these changes across time, the investigators hope to understand the basis of these behavioral changes.