Master Manipulators of the Micro-world

Parasites are perhaps the greatest master manipulators out there in nature. Even though they are tiny, their numbers are mighty and they have a huge impact on individuals and even entire ecosystems. For a parasite the primary objective is to increase its numbers and successfully manipulate its host to help it accomplish this goal. One of the easiest ways to do this is to induce changes that increase transmission of the parasite between hosts. In this sense, the manipulation can be thought of as a characteristic of some parasites and, unbeknownst to the host, the end result can be some very odd behaviors indeed.

When it comes to fear of new objects it is well known that wild rats are among the most neophobic creatures around. They stay away from things that are unfamiliar, including novel food sources. This tendency for extreme caution is helpful when it comes to surviving out there in the big bad world. As you may have noticed there is no shortage of rats, at least not of the usual variety. You might be inclined to believe that predators and people are the biggest threat to rats. In one sense this is accurate, but a far more insidious danger lurks in water sources that may be tainted with a parasite called Toxoplasma gondii.

Many people are familiar with this little protozoan because of the risk to pregnant women. Cats are the principal host for this parasite because it can only reproduce in the gut of a cat, but there are many suitable intermediate mammal hosts, including humans and rats. This parasite is one of the most ubiquitous, with infection rates ranging from 38-70% of animals such as bears, deer, domestic chickens, cattle, sheep, sea otters, and rabbits-to name a few. The easiest way to catch it is by consuming undercooked meat. This is how cats usually acquire the infection; from the mice or birds they catch and eat.

It is thought that one of the reasons this protozoan is so successful may be related to the unusual changes in behavior that are induced in the host, particularly intermediate hosts. This has been well studied in mice and rats. If you recall, rats are some of the wariest mammals out there- a fact that contributes to their success. Once they are infected with toxoplasmosis, however, they lose their fear, and not just of novel objects or food. They specifically lose their fear of cats!

Researchers tested laboratory rats for their aversion to cat odor and compared individuals that were infected with those that were not. Despite many generations of not being exposed to cats, uninfected rats had a strong aversion to cat odor. Not only did some infected rats show reduced aversion to cat odors, some actually preferred the smell of cats! Essentially, being infected with toxoplasmosis can make some rats suicidal, in that they want to be close to a dangerous predator.

This mind-bending, fatal-attraction manipulation only affects their fear of cats and doesn?t seem to alter any other behaviors in rats-except perhaps that female rats seem to find infected males more attractive. The precision of the parasite to change the behavior of rats has to do with brain lesions centered on the amygdala, which you can think of as the fear center of the brain. It is possible that we, as humans, may also be behaviorally affected by infection. Though inconclusive, some researchers suspect infected females are more attractive to men and are more sociable. There is also some evidence that both men and women infected with toxoplasmosis reduce novelty-seeking behavior (the opposite of rats) and have reduced reaction times, leading to a higher incidence of motor-vehicle accidents.

More recently, a far more unpleasant psychological side effect may be linked with infection: schizophrenia. Toxoplasmosis infection in humans has an impact on dopamine levels in the brain and dopamine imbalance is also associated with the development of schizophrenia. Whether or not this is the definitive mechanism, there is a correlation between toxoplasmosis infection in humans and schizophrenia that one day may provide new treatment options for this debilitating disorder.

You might be inclined to think this is extreme, but toxoplasmosis infection is just the tip of the iceberg when it comes to behavioral manipulation. For instance, in crickets and grasshoppers there is a little worm that causes them to behave very strangely indeed. This modest worm, a hairworm, lives as a youngster inside arthropods (insects, spiders, etc.), but is free-living as an adult in rivers, lakes, and streams. They reproduce in water environments, but develop inside non-aquatic invertebrates. This sets up a conundrum: how to transition from one environment to the other without, um, dying? It seems the clever solution that they have come up with is to make their non-water seeking insect host suddenly look for water and dive right in.

Of course! Problem for the insect is that it doesn?t swim, so this is rather detrimental to the host. As with Toxoplasma gondii, adult hairworms so precisely manipulate the behavior of their host that suddenly, one night, out of the blue, it is all the cricket or grasshopper can do to stay away from water. Naturally this is beneficial, and really vital, for the hairworm to survive and guarantee it?s life cycle will continue. One study looking at protein expression in both the grasshopper and the hairworm revealed that proteins in the grasshopper?s central nervous system were expressed more when it was seeking water, suggesting manipulation down to the level of proteins!

Things get stranger and stranger as we look at moths, gypsy moths in particular. This is really the stuff of nightmares and science fiction. Imagine an evil virus laughing sadistically in the background. Like butterflies, moths go through several stages of development. The first stage is as an egg placed on the underside of a host plant leaf. Gypsy moths are a little less particular. They will lay their eggs on tree trunks, tree branches, anywhere that provides the tiniest bit of shelter.

The eggs are laid in clusters and the larvae hatch in the spring. Once they hatch the larvae go through several stages, molting (shedding their outer covering) as they grow. This larval stage is what we know as caterpillars. When they are ready to pupate it can take several days to two weeks. This wonderful process is rudely interrupted for those individuals unfortunate enough to catch a virus. A baculovirus, to be exact.

Moth larvae infected with this type of virus become like zombies on a mission to climb and climb to the treetops. This phenomenon is well known and was described in silk worms as wilting disease. Another phrase ?Wipfelkrankeit?, or tree top disease has also been used. Why are they induced to perform this odd behavior? Apparently they climb to the tops of the trees just before they die and begin to liquefy. Yes, you read that correctly, liquefy. The end result: excellent dispersal for the virus by raining down on the unfortunate caterpillars below. In the ?liquid? of the infected, now deceased, caterpillar, are millions and millions of virus particles.

I suppose it is rather like an awful sneeze. When we sneeze we disperse the virus through the air. When the caterpillars liquefy they disperse the virus downward. As it turns out, there is a single gene in the virus that halts the molting process and causes them to move into the treetops in broad daylight (unwise behavior for tasty caterpillars). How does a gene in the virus accomplish this? The gene produces an enzyme that stops the molting process of the caterpillar. Unlike the protozoan that caused brain lesions in rats, or the worm that affected protein expression in crickets, here we have a situation where a gene in one species affects the physiology and behavior of another species.

Can it get weirder? Oh yes, yes indeed. Fungi that turn ants into zombies and give them ?lockjaw?? caused by Ophiocordyceps fungi. The first step in the manipulation is to get the ant to leave the nest. The second step is to make the ant climb up something, a blade of grass will do nicely thank you very much. The third step is to make the ant bite down and never let go. The ant dies, the fungus emerges out of the brain of the ant and is dispersed. Score one fungus, score zero ant.

It really is worse than that. The fungal spores enter into the ant when it breathes. At some point, when the fungus is ready to produce spores (think baby fungi) it migrates to the brain of the ant. It grows and this causes the ant to behave in a way uncharacteristic for the ant (you think?). At some point when the ant climbs and bites down on plant tissue the muscles of the mandible (jaw) atrophy meaning the ant cannot undo the bite. The fungus then eats the ant?s brain before sprouting out from its head and sending its spores out into the world to find more ants.

The fungus can only reproduce after it makes this kind of stalk that comes out of the back of the ants head and it needs to get the ant outside of the nest because other ants will remove dead pals quickly. Here is how precisely the ants can be manipulated to eat. It seems they can be induced to bite into leaves all around the same time: noon, and facing a similar direction: NNW. Go figure. Researchers have not quite figured out why the ants need to bite down around noon or face in this peculiar direction.

From other species of ants that, when infected with the larvae of a liver fluke, saunter outside at night biting onto a blade of grass in the hopes that a sheep will come along and consume them, to snails that are induced to wiggle and jiggle their tentacles in order to attract birds so they can be eaten, these microscopic critters are some of the most successful manipulators around. Lest you believe we, as humans, are immune to being influenced by these mini-masters of the biological world, think again. Toxoplasma induced behavioral changes may just be the start of unraveling the effects of parasites, bacteria, and viruses on human behavior. As we uncover more parasite driven effects, we may very well start to wonder: Are we really who we think we are?

Images:

1. Cat with mouse in the mouth by Lxowle at Wikimedia commons; 2. Ant infected with ophiocordyceps by Alex Wild, with Permission; 3. Gypsy moth caterpillar by Materialscientist at Wikimedia commons.

References:

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Biron, D.G., March?, L., Ponton, F., Loxdale, H.D., Gal?otti, N., Renault, L., Joly, C., and Thomas, F. 2005. Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach. Proceedings Royal Society B. 272:2117-2126 (doi:10.1098/rspb.2005.3213).

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Hughes, D.P., Andersen, S.B., Hywel-Jones, N.L., Himaman, W., Billen, J., and Boomsma, J.J. 2011. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology 11:13 (doi:10.1186/1472-6785-11-13).

Moore, J. 2002. Parasites and the behavior of animals. Oxford University Press.

Mortensen P., Norgaard-Pedersen B., Waltoft B., Sorensen T., Hougaard D., Yolken R. 2007. Early infections of toxoplasma gondii and the later development of schizophrenia. Schizophrenia Bulletin (doi:10.1093/schbul/sbm009).

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Vyas, A., Kim, S., Giacomini, N., Boothroyd, J., and Sapolsky, R. 2007. Behavioral changes induced by toxoplasma infection of rodents are highly specific to aversion of cat odors. PNAS 104: 6442-6447.

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