Zombie-Ant Fungi Emerged from Non-manipulating, Beetle-Infecting Ancestors

Abstract

The manipulation of animal behavior by parasitic organisms is one of the most complex adaptations to have arisen via natural selection. Among the most impressive examples of behavioral manipulation are the zombie-ant fungi [1]. In this association, ants are controlled to leave the colony and perform a stereotyped death grip behavior, where they bite onto vegetation over foraging trails, before being killed for the post mortem fungal growth. Manipulation functions to provide a platform outside the nest, from which fungal parasites actively shoot out spores, targeting foraging ants because within colony transmission is prevented by strong social immunity exhibited by social insect societies [2, 3]. It is not clear how such complex examples of host manipulation arose. To address this, we performed a broad-scale phylogenetic reconstruction of the order Hypocreales, to which the zombie-ant fungi, Ophiocordyceps, belong. In order to understand the patterns of host association and host switching along the evolution of Ophiocordyceps, we performed ancestral character state reconstruction analysis. We found that zombie-ant fungi likely arose from an ancestor that infected beetle larvae residing in soil or decaying wood, similar to extant beetle-infecting Ophiocordyceps species. Surprisingly, the jump led to an extensive species radiation observed after the development of behavioral manipulation. We suggest that the jump from solitary beetle larva to ants within a colony exposed the fungus to the robust social immunity of ant societies.

Keywords: Hypocreales; Ophiocordyceps; Phylogenetics; ancestral state reconstruction; entomopathogenic fungi; evolution of fungi; fungal ecology; host-shift; host-switch; zombie-ant fungi.