The Occasional Hymenoptera: Ancient zombie ants

Among the more arresting sections of the BBC’s documentary series Earth was a segment on ants being preyed on by the endoparasitoid fungus Cordyceps. The fungus caused the infected ant to exhibit bizarre behavior and then climb onto a limb, clamp itself down firmly, then die. When other workers noticed this behavior, they transported the afflicted ant away from the rest of the colony to die. And then, after death, a fruiting structure sprouted from the head of the ant, which, when ripe, exploded and ejected the spores of the fungus.

[You may recall the terms from the discussion of hymopteran parasitoids, like the ichneumon wasp. Parasitoids are not true parasites because they kill their hosts. Thus, they spend only part of their lives with the host. The ichneumon wasps, for example, deposit their eggs in the host and the developing larvae use the host’s tissue as food. In the case of the Cordyceps fungus, mycelia (the long, branching, filament-like structure of the fungus) grow and replace the host’s tissue. (Endoparasitoids are the kind of parasitoids that live within the host.)]

The Cordyceps fungus came to the attention of the Western public, not because of their relationship with ants (or any other insect), but as a result of peculiar success of certain Chinese women runners in 1993–all coached by Ma Junren. A group of then unknown runners captured all three medals in the 3,000 metres and the  gold and silver in the 10,000 meters at the world championships in Stuttgart. The surprising success of the athletes of this notoriously competitive coach prompted rumors that he was doping his runners. Ma denied the use of illegal performance enhancers and attributed the success to “intense high altitude training, turtle blood and Cordyceps sinensis.” Turtle blood and the fungus were not among the proscribed performance-enhancing substances. See Winkler, “Cordyceps sinensis: A precious parasitic fungus infecting Tibet,” 11 Field Mycology 60, 65 (2010) (pdf copy). Peddlers of faux-Eastern herbalism soon began promoting the consumption of the dried fungus for all sorts of reasons, including increasing sperm count, strengthening immune system, and reinforcing “the Qi.” Seven years later, six of Ma’s runners were dropped from the Chinese team destined for the Sidney Olympics in 2000 (after testing for the substance erythropoietin), and two were banned in 2001 for illegal doping (see The Guardian, Wednesday July 25, 2001). Ma’s 1993 “success” is nevertheless still being touted on internet sites that offer the fungus for medicinal and performance enhancing uses. See, for example, here.

An aside on taxonomy: In 2007 Gi-Ho Sung of Oregon State University had published in Studies in Mycology an article entitled “Phylogenetic classification of Cordyceps and the clavicipitaceous fungi” (full article). The paper sorted out the relationships among the 400 or so species of fungus then grouped in the family Clavicipitaceae. Sung showed by molecular phylogenetic analysis of multigene DNA sequence data that the family Clavicipitaceae was not monophyletic (i.e., the organisms did not arise from a single common ancestor). Even the genus Cordyceps was found to be paraphyletic. Instead he erects three clades:

1. The family Cordycipitaceae includes most Cordyceps species that possess brightly coloured, fleshy stromata.

2. Sung erects a new family Ophiocordycipitaceae, based on the Ophiocordyceps genus described by T. Petch seventy years ago.

3. He amends the family Clavicipitaceae s. s. to include thecore clade of grass symbionts (e.g., Balansia, Claviceps, Epichloë,etc.), and the entomopathogenic genus Hypocrella and relatives.

In the course of this analysis he places Cordyceps sinesis in the genus Ophiocordyceps (which he revises).

The phylogeny of these parisitoid funguses is complicated because their evolution involved “inter-kingdom host jumping.” Thus there are some Clavicipitaceae fungi that parasitize other fungi but are nevertheless closely related to other Clavicipitaceae fungi whose hosts are arthropods.

Certain Clavicipitaceae fungi have unusual neuro-pharmacological effects on the host. The Ophiocrdycep sinesis (formerly Cordyceps sinesis) known in Tibet as yartsa gunbu, the “summer grass-winter worm,” invades the body of a Thitarodes ghost moth caterpillar about to overwinter  in the roots of certain alpine grasses. The fungus, however, causes the host to move closer to the surface and then begins consuming the body. Before it devours vital organs, it causes the host to move itself to a position that optimizes the ability of the mycelium to “sprout” from the ground. A picture of the parisitized host and the “sprouting” mycelium can be found on the second page of the Winkler pdf file.

A mature O. unilateralis growing from an ant (Camponotus leonardi) it has killed a few weeks before. The "P" points out the perithecial plates where spores are released. (The American Naturalist)

The fungus Ophiocordyceps unilateralis is found world-wide in humid tropical forests. The host is the Camponotus leonardi, a species of tropical carpenter ant, which lives high in the tree canopy. The parasitoid fungus, however, must live in a different forest zone owing to its adaptation to certain humidity levels and other requirements. So when it parasitizes the ant,  it causes the ant to move to parts of the forest that best accommodate the fungus”s survival and “bite down” on leaves at that level to secure it when it dies. (See parasitized ant, now long dead, biting down on the leaf near the stem in the picture to the right.) According to a study by Sandra B. Andersen and others in the American Naturalist last year (abstract; article behind pay wall), the fungus causes the ant to locate itself in a very specific environment, with the following characteristics: on the north side of the plant, about 25 centimeters above the ground, in an environment with 94 to 95% relative humidity and with a temperature between 20° C and 30° C.

In a study published in the open-access journal PLoS One by Maj-Britt Pontoppidan of the University of Copenhagen and others observed that some but not all of the “graveyards” of parasitized ants in a 1,360 square meter plot in Southern Thailand correlated with temperature, humidity and vegetation cover. They did find that live carpenter ants avoided the “graveyards.”

The BBC video narrated by David Attenborough at the beginning of this post shows worker ants of a different species (the “Bullet Ant”) actively carrying infected ants to places to prevent the spores released by the fungus to reach the colony. The Bullet Ant, Paraponera clavata, is found in the New World, from Nicaragua to Paraguay. It received its common name from the pain its stinger can inflict. Locals call it Hormiga Veinticuatro–the 24 hour ant, because the intense pain lasts for at least 24 hours.

Leaf and magnified "death grip bite marks" in leaf fossil from Messel Shale formation in Germany. (Photo: Hughes, et al.)Now all this leads up to the point of this entry. In a pre-print communication in the Royal Society’s Biology Letters (abstract; sadly the Royal Society has ended its free access policy to celebrate its 350th Anniversary) Harvard’s David P. Hughes and two others reveals evidence of ancient “zombie ants.” (Hughes was one of the additional authors on each of the two previous, linked papers.) They describe the features of a “bite,” like a “death grip,” in fossilized leaves from a site in Messel, Germany of Eocene shale (84 million years ago). In an article in Nature News on August 17, Professor Hughes describes why he believes he can eliminate other explanations for the tears near the central vein of the leaf.

So if this conjecture is correct two conclusions are evident: The Eocene of Germany was similar in some respects to the environment of present day Southern Thailand. And, more importantly, the neuro-pharmacological effects of the parasitoid fungus had evolved at least as early as 84 million years ago.

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