CAREER: Connecting behavioral phenomes with functional genomes in ants, manipulated by a fungal parasite

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Infected animals generally behave differently from healthy animals. These changes can go beyond mere sickness behaviors to reflect precise manipulations induced by parasites to increase that parasite’s chances to spread. How manipulative parasites can alter host behavior is currently unknown. The behaviorally tractable “zombie ant system” has the potential to expose the mechanisms underlying parasitic behavioral manipulation and fundamentally transform perceptions of parasite-host interactions and their behavioral ecology effects. This project uses fungus-infected “zombie ants” as a model to systematically quantify disease progression and accompanying behavioral phenotypes, to determine where sickness behavior ends, where manipulation begins, and which intricate molecular mechanisms are involved. Knowledge of the regulation of insect behavior and how to effectively disrupt it can be used in evolutionarily more robust methods to battle pests. Additionally, the novel fungal effectors discovered are potentially applicable in human medicine. The project will leverage the public’s interest in zombie-making parasites to create immersive pedagogies for teaching biology to a diverse student population. As such, the investigators will develop a research-based, educational virtual reality experience about microbial infections and insects to take to K-12 schools, museums and fairs. Undergraduate students at a large, ethnically and socio-economically diverse university will get the opportunity to involve themselves in the scientific process through a research-intensive course on insect behavior and manipulation. Multiple graduate and undergraduate students will also be involved in the integrative research activities of this project, preparing them for an increasingly cross-disciplinary STEM job market.The research seeks to 1) examine how ant behavior changes throughout infection; 2) how ant and fungal tissues interact throughout this progression; 3) reveal which genes and pathways from both parasite and host give rise to behavioral phenotypes; and 4) elucidate the exact functions of these genes and pathways. The work spans the integration of multiple technological approaches to understand how zombie-making fungi of the genus Ophiocordyceps interact with ants from the molecular level to the behavioral output displayed by the whole organism. Manipulated climbing and biting of Ophiocordyceps-infected ants represent common behavioral phenotypes among zombie makers. Thus, answering how these fungal parasites modify host behavioral pathways will also form a springboard for mechanistic hypotheses in other model systems. Specifically: 1) Comparative infection studies and quantifiable behavioral assays will reveal how normal behavior progresses beyond mere sickness phenotypes to parasite-adaptive manipulation phenotypes. 2) Three-dimensional X-ray microtomography models of whole ants will show how fungal cells physically interact with ant tissues throughout the disease progression. 3) Mixed RNA-Seq will provide accompanying gene expression profiles of both organisms that underlie these detailed morphological and behavioral phenotypes. This will lead to the discovery of novel fungal effectors, and the insect pathways they potentially target. 4) The genetic modification of fungal effectors of interest, followed by functional behavioral assays with those modified strains or their produced compounds, will expose their true function and involvement in the manipulation of host behavior.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.