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From ecology to mechanisms of the extended phenotype

Final Report Summary - ANT FUNGI EP (From ecology to mechanisms of the extended phenotype)

The scientific project funded by the commission, From ecology to mechanisms of the extended phenotype, centers on a host-parasite interaction between a fungus, Cordyceps (now Ophiocordyceps) and its ant host (mainly Camponotus). The fellowship followed directly on from an EIF to Dr Hughes (University of Copenhagen) in which he examined the relationship between this parasite and its host in a local context of a tropical forest in Southern Thailand. The OIF sought to view the relationship at different scales. The first scale was geographic and to examine the relationship across the world. The second scale was temporal and attempted to examine the evolutionary history and the third scale was cellular to understand the molecular biology of the relationship.

The Project

The behavior of ants has inspired generations of biologists-many at the Harvard Museum of Natural History, where the Out-going phase occurred . Evolution by natural and kin selection has shaped these behaviors to lever ant genes into the next generation. But other genes- those belonging to parasites- can also lead to spectacular ant behaviors. This is the Extended Phenotype concept developed by Dawkins . One of the most dramatic examples is the death grip induced by the fungus, Ophiocordyceps.
In Thai rainforests, where I carry out my fieldwork, infected ants leave their colony in the high canopy, descend to the forest floor and –with high synchronicity around noon- bite the underside of North facing leaves within a narrow manipulative zone 25 cm above the forest floor. The fungus then kills the ants to grow a large a stalk from its head from where spores are discharged to infect new hosts (Fig 1). Experiments I performed with my students established that the location where ants die has a significant effect on fungal fitness (see publication list).
My vision is that Cordyceps manipulation of ant behavior can become the model system for understanding the mechanisms by which a parasite controls host behavior. And since perturbations are often how we deduce the workings of a biological system-think of the role Drosophila mutants have played - then parasite manipulation may be a tool for understanding the neurobiological and genetic basis of insect behavior. For this reason the Incoming Host, Univeristy of Exeter and Prof Nick Talbot’s lab, was chosen as they have pioneered the molecular basis of phenotypes in fungi.
The mechanisms of behavioral control: preliminary data
Using LM and TEM we discovered that the heads of behaviorally manipulated ants are packed with fungal cells (Fig 2). As befits a parasite that induces a death grip, the fungus causes a characteristic atrophy of mandibular muscles. Mitochondria and sarcoplasmic reticula were significantly reduced (Fig 2). The z-lines of myofibrils were commonly broken or distorted. I suggest that these effects induce a rigor state leading to lock jaw. (Once dead the ant is effectively glued to the leaf by the fungus and the purpose of lockjaw is to keep the upside down, dead, ant in place until the fungus produces this glue which is between 48-72 hours post mortem, Fig 1b, Fig 2e).
Motor neuron damage is one cause of muscular atrophy (e.g. spinal cord injuries and carpal tunnel syndrome). Rather than targeting sarcoplasmic reticula and mitochondria I suggest the atrophy is due to motor neuron damage upstream of the myofibrils. A closely related fungus, Claviceps purpurea, which infects rye, has a notable history of inducing convulsions, muscle spasms, and hallucinations in humans, called either ergotismus convulsivus or St Anthony’s Fire . This fungus is of local interest as it is the suggested agent of mass hallucinations surrounding the Salem Witch trials . It was also the precursor of the psychedelic drug LSD . It is likely that some interesting bioactive compounds, possibly an alkaloid, cause muscle atrophy via the nerve cell damage. The behavioral observation of synchronized biting at noon on North facing leaves suggests solar cues are important and this in the parasite manipulation literature is associated with serotonin modulation.