The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype

Abstract

Specialized parasites are expected to express complex adaptations to their hosts. Manipulation of host behavior is such an adaptation. We studied the fungus Ophiocordyceps unilateralis, a locally specialized parasite of arboreal Camponotus leonardi ants. Ant-infecting Ophiocordyceps are known to make hosts bite onto vegetation before killing them. We show that this represents a fine-tuned fungal adaptation: an extended phenotype. Dead ants were found under leaves, attached by their mandibles, on the northern side of saplings approximately 25 cm above the soil, where temperature and humidity conditions were optimal for fungal growth. Experimental relocation confirmed that parasite fitness was lower outside this manipulative zone. Host resources were rapidly colonized and further secured by extensive internal structuring. Nutritional composition analysis indicated that such structuring allows the parasite to produce a large fruiting body for spore production. Our findings suggest that the osmotrophic lifestyle of fungi may have facilitated novel exploitation strategies.

Field Trial of Aqueous and Emulsion Preparations of Entomopathogenic Fungi Against the Asian Citrus Psyllid (Hemiptera: Liviidae) in a Lime Orchard in Mexico

“…1) (Andersen et al 2009;Pontoppidan et al 2009). Hirsutella citriformis could use of the host as a vehicle for dispersion.…”

Animal–microbe interactions and the evolution of nervous systems

“…B 371: 20150052 produce outcomes that are favourable to the microbe but not the host. For example, the fungal pathogen Ophiocordyceps unilateralis infects the nervous system of ants (Camponotus leonardi), leading the ants to attach themselves to leaves for several days until a fruiting body erupts from the ant's head, scattering fungal spores [67]. Other Ophiocordyceps species infect other species of Camponotus, and the ability to manipulate the ants' behaviour is unique to its naturally occurring pathogen [68,69].…”

The zombie ants parasitized by the fungi Ophiocordyceps camponotiatricipis (Hypocreales: Ophiocordycipitaceae): new occurrence and natural history

“…These interactions often occur as epizootics, contaminating a large number of ant specimens in small forest regions (Andersen et al 2009, Pontoppidan et al 2009). The possibility of acting directly and indirectly on the abundance of its hosts and, therefore, presenting an important function on communities' energy flow, makes studies on ant-fungi interactions highly recommended (Hudson et al 2006).…”

“…The authors observed parasite-infected ants fixed through its mandibles to the abaxial veins of leaves, a behavior which is not apparent in healthy ants of this species. According to Andersen et al (2009), this behavior is adaptable to the fungus, ensuring a stable microclimatic niche for its development after the host's death and facilitating aerial dispersion of the spores. Araújo et al (2015) described three species of Ophiocordyceps that infect Camponotus ants, among them O. camponoti-atricipis, the target species of this study.…”

“…Species belonging to O. unilateralis complex triggers a series of synchronized events within the host to induce it to leave the colony towards the understory, where it dies in an elevated and strategic position, characteristically attaching itself to abaxial vein or edges of leaves. Once there, the spore-producing structure (stroma) emerges from the anterior intersegmental region to the pronotum, from which the ascospores actively release their spores after a few weeks of maturation (Andersen et al 2009, Araújo et al 2015. After releasing, the spores are deposited on the forest floor, where they will infect other ants that eventually pass through the site.…”