Thursday, August 16, 2012

Castrating the Zombie Ant

Last year I posted Attack of the Zombie Ant! A post that turned out to be quite popular. To sum it up, there are fungal parasites (genus Ophiocordyceps) that infect ants and take control of their bodies. The fungus then compels the ant to crawl up into the forest canopy and clamp down on a leaf while the fungus grows inside the body, eventually producing a hyphae and stroma (fruiting body) that grows out of the head and produces and releases spores. And repeat.

A recent paper in PLoS ONE takes a closer look the coevolution between ant colonies and these rare, specialized fungi. Broadly, the term coevolution is used to describe how two or more species reciprocally affect each other's evolution. In the case of the zombie ants, it is host-parasite coevolution. The parasite evolves to infect the host, and the host evolves to resistant to the parasite. An arms race, if you will. The virulence and defense traits of specialized parasites, such as the zombie-ant fungi, are shaped by these arms races. This is even more true in species like Ophiocordyceps that rely on host behavior for their reproductive success. On the other side of the coevolutionary coin, ant colonies (in this case Formica and Camponotus ants) are long-lived and live in high density, continuously interacting colonies. This behavior has been shown to be a type of social immunity where there is a strong selection for efficient prophylactic defenses and where ant parasites pose a limited threat to infecting an entire colony. Meaning that individual ants my die from the fungal disease but that the mortality of the colony is low.

This paper specifically looks at the trade-offs experienced by Ophicordyceps manipulating ants into dying in nearby graveyards. When the fungus compels an ant to leave their nest and die close to their host colony, many infected individuals will end up in one area, forming high-density ant graveyards that may persist for years. Considering the life span of your average ant, that is a long time. The authors of this paper used data from previous studies of O. unilateralis in Thailand and collected a new data set from O. camponoti-rufipedis from Brazil to construct a developmental-stage-structured model describing this ant-fungus interaction. In this new collection, they identified ants infected with O. camponoti-rufipedis and marked areas covering entire graveyards, tagging all dead infected ants. Each cadaver ant was then characterized in terms of parasite development: (1) freshly killed ant, (2) dead ant with parasite stroma, (3) dead ant with mature fruiting body, (4) dead ant at stage 2 or 3, but hyperparasitized by other fungi, or (5) dead ant whose status could not be identified. To estimate the infectivity of the fungi's fruiting bodies, they collected a sample of dead ants and brought them to the lab for study. From these data, they were able to formalize the "life-cycle" of parasitized ants and calculate a growth rates and fungal developmental stage distributions of the graveyards.

The researchers found that only 6.5 percent of the O. camponoti-rufipedis fruiting bodies were effectively producing spores. Most of the dead ants that they found were sterile because they were either immature, damaged or hyperparasitized (secondarily parasite develops within a previously existing parasite). They also found that only 42 percent of the fruiting bodies were shooting spores at a particular time interval. When the apparently "healthy" cadaver ants were dissected, they found them to have been invaded by the larvae of small unidentified arthropods which may have reduced the likelihood of the fungi reaching maturity. Add to this that out of all of the ant colony members, only the foragers face the risk of encountering spores, then you end up seeing a rather low infection and transmission rate. So only if graveyards are stable or growing will infection levels be stable.

Interestingly, the authors found that the zombie-ant fungi are themselves vulnerable to attack by other parasites. Their model suggests that the stroma life stages or immature fruiting body stages are highly vulnerable to biotic attack. So much so that hyperparasitism is nearly negligible in the mature life stage. Whether that is because the mature life stage has a much more efficient immune defense or some other cause is unclear. What is clear is that hyperparasitic fungi prevent the infected zombie-ant fungus from spreading spores which, in turn, means that fewer of the ants will become zombies. This means that the rate of infections is much less than the size of some graveyards might suggest. It is known that O. unilateralis has a range of asexual stages (synanamorphs) with spores adapted for persistence or aerial dispersal. However, O. camponoti-rufipedis is known to produce a single anamorph. So the horizonatal transmission of this species may depend on the movement of the infected ants themselves. And that means all kinds of other intriguing studies may be in the works. Can't wait!

ResearchBlogging.orgSandra B. Andersen, Matthew Ferrari, Harry C. Evans, Simon L. Elliot, Jacobus J. Boomsma, & David P. Hughes (2012). Disease Dynamics in a Specialized Parasite of Ant Societies PLoS ONE, 7 (5) DOI: 10.1371/journal.pone.0036352

About the Authors:
Sandra Andersen's bio
David Hughes' Lab (includes zombie-ant videos on his Projects page)

Penn State Science "The Zombie-Ant Fungus Is Under Attack, Research Reveals"
Discover Magazine "Zombie Ant Parasite Has Its Own Parasite - a Fungus that Attacks Fungi"
The Guardian "Zombie-ant parasitic fungus kept in check by hyperparasitic fungus"

(image from the Hughes Lab website)

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