The Parasite Manipulation Hypothesis: How To Get Where You Need To Be

By: Helen Beilinson

           In 1990, after students proposed a project asking whether frogs can hop in zero gravity, six Japanese tree frogs went to space. This question, as well as many others, was answered in the “frog in space” experiment (FRIS) of the early 1990’s. Two decades later, the mating calls of male Japanese tree frogs were the inspiration for an algorithm to create efficient wireless networks. Recently, these frogs, and their mating calls, have made it into the news again when a group from Korea showed that when these male frogs are infected with the fungus Batrachochytrium dendrobatidis, their mating calls become ‘sexier’.

            B. dendrobatidis infects various amphibian species, including the Japanese tree frog. This fungus causes a wide range of changes to the bodies of its host, including electrolyte and fluid imbalance, leading to heart failure and rapid death of immune cells. While some amphibians are susceptible to B. dendrobatidis and will die when infected, some, including the Japanese tree frog, are not. The Japanese tree frog is tolerant to the infection, meaning that after being infected, instead of destroying the pathogen (this occurs in resistant hosts), the pathogen remains within the host, but does not cause significant damage to the host (as occurs in susceptible hosts). Interestingly, even though no detectable changes occur in infected male Japanese tree frogs, other than very slight weight gain and lethargy, their mating calls change.

            After collecting and analyzing mating calls from male Japanese tree frogs, the authors found that those frogs infected with B. dendrobatidis had calls that made them more attractive to females. The scientists analyzed the calls for number of pulses per note, the repetition rate of the pulses, the number of notes, and the duration of the calls. The infected males’ calls were faster and longer, traits female frogs are known to find more attractive. The fungus and the tree frogs have evolved a relationship that presumably increases the fungus’ ability to spread, as the more females their host interacts with as a result of their more sultry call, the more new hosts the fungus can spread to.

            The manipulation of host behavior by fungi and other parasites in order to facilitate transmission to new hosts is not a new idea. The ‘parasite manipulation hypothesis’, first described in the early twentieth century, describes this phenomenon in which parasites purposefully alter the behavior of their host to increase the probability that they interact with a new potential host. A well-known example of such a parasite is Toxoplasma gondii, a protozoan that infects a broad spectrum of warm-blooded animals.

            T. gondii is a protozoan (a unicellular eukaryotic organism) whose life cycle has two components. The first is asexual, where it replicates by fission, and can happen in almost all warm-blooded species. The second is sexual, where two individual T. gondii ‘mate’ to form genetically different progeny, and only can occur in feline species’ intestinal cells. Famously, mice infected with T. gondii no longer have an innate aversion for cat urine odor, making them more likely to be caught, and eaten, by cats. It is thought that this behavior change makes it easier for T. gondii to spread to cats, their preferred host and the only host in which they can sexually replicate (sexual reproduction is preferred because it increases the genetic diversity of the species). Humans can also be a host for T. gondii; in fact, it’s one of the most common parasites in the western world, with nearly half of the population being infected. Fortunately, the infection does not seem to induce disease (toxoplasmosis) unless the infected human is immunocompromised (like infants, AIDS patients, and patients on chemotherapy). However, there are some interesting correlation studies showing that infected human men no longer find the smell of cat urine unpleasant.

            Humans are not a good intermediate host for T. gondii to infect, because we no longer have natural feline predators. Chimpanzees, however, have one known feline predator… the leopard. When scientists studied the influence of T. gondii infection on chimpanzee behavior, they found similar results as has been noted for years in mice: infected chimps lost their innate aversion to leopard urine. Presumably, the protozoan induces this phenomenon to increase the probability that its chimpanzee host is predated by leopards, such that the protozoan can replicate in the leopard. Interestingly, when the scientists studied the chimps’ attraction or aversion to another feline’s urine compared to leopard urine, they found that the affect of T. gondii only affected the chimps’ attraction to leopard urine, not lion urine. This result indicates that the lack of aversion to urine induced by T. gondii in chimps is specific to the urine of felines residing in proximity to their hosts. Additionally, in the previous study mentioned where infected human men do not find cat urine unpleasant, they still found tiger urine to have an irksome smell. The studies done in T. gondii infected chimps and humans were correlative, but they do produce stimulating evidence for the parasite manipulation hypothesis.

            B. dendrobatidis and T. gondii are nowhere near the only parasites able to manipulate the behavior of their hosts. A tapeworm infection in stickleback fish, native to cold saltwater regions, and malaria infection in female great tits, a common bird species in Europe, Central Asia, and North Africa, causes the species more bold in exploring new territories, making them more susceptible to predation. In humans, parasite manipulation may not be of concern, as we are no longer prey to other animals, but it is a predominant effect in the animal world. Not only does this effect point to the incredibly intricate relationships that are formed between host and parasite, but also show the importance of innate animal behaviors keeping them away from potentially dangerous situations.