One goal of the young science of “Darwinian medicine” is to understand how infectious microorganisms might actually manipulate the host’s behavior to facilitate the microorganisms’ own transmission. This is nothing new to evolutionists—we have several examples of larger parasites, like flukeworms or fungi, making their hosts behave in a way that helps the parasite complete its life cycle—but it’s a phenomenon of evolutionary biology that is at once fascinating to contemplate, tricky to understand (what chemicals can a simple parasite produce that can affect the host’s brain or behavior?), and of potential value in treating disease.
Evolutionists have speculated, for example, that cold viruses leave you ambulatory because they have to spread by person-to-person transmission, while the malaria parasite makes you prostrate, because mosquitoes (their vehicle of transmission) are more likely to bite successfully when the victim is laid out and unable to slap the insect.
By “adaptive” in the title, then, I mean “adaptive for the malarial parasite”, which in this case is the the sporozoan Plasmodium falciparum—a protozoan. The parasite infects mosquitoes of the species Anopheles gambiae, and those parasites migrate to the mosquito’s salivary gland, from where they get injected into humans when mosquito bites. They then multiply first in the human liver and then in the red blood cells before being re-ingested by a subsequent mosquito bite. (That’s if they don’t first kill the human!) It’s essential for mosquitoes to bite humans because that’s the only way they can multiply both sexually and asexually and then spread from mosquito to mosquito. Without the infected mosquitoes biting, the parasite goes extinct. Ergo, any adaptation in the parasite that makes its mosquito host bite more readily will be an adaptive trait.
Falciparum malaria, as you may know, is the deadliest form of malaria, and virtually all malarial deaths are caused by this one sporozoan species (770,000 per year!) rather than by other forms of Plasmodium. At present 200 million people have the disease, which is one reason why the Gates Foundation has targeted eradication of the disease in the next decade or so. Such eradication can be achieved by eliminating transmission of the parasite between mosquitoes for three years, something that was achieved in the U.S. by 1951.
Here, from a Wiki Commons site, is a photo of a human blood smear containing P. falciparum gametocytes—the sexually reproductive stage of the parasite, The page notes that “At the peak of infection time, the infected person may carry up to 2 million parasites per microlitre of blood.” That is two million parasites per one-millionth of a liter of blood! I find that hard to believe.
Which brings us to the paper. In a report in the latest PLoS ONE (link and free download below), R. C. Smallegange and colleagues report a simple experiment: they looked at the feeding behavior of mosquitoes that were either uninfected or infected with P. falciparum. It was already known that another species of mosquito (Aedes aegypti) that carries bird malaria (P. gallinaceum) bit guinea pigs more readily when the insects were infected than when uninfected.
What Smallengange did was simply replicate this experiment with two changes: using human rather than guinea pig odor, and using mosquitoes infected (or uninfected) with P. falciparum. The “bioassay” was a nylon sock worn for 20 hours by a Dutch volunteer (a single male who had been shown to be the most attractive to mosquitoes among 47 volunteers exposed to the insects). The socks were put in a cage containing either infected and uninfected mosquitoes, and the landings of each type of mosquito on the sock were recorded (this was done blind, of course).
The results were clear cut: infected mosquitoes landed far more frequently on the sock when infected than when uninfected. Here’s the figure from the paper. No odor, no bites. With human odor, significantly more bites when the mosquitoes were infected than uninfected.
I suspect that it would prove real on replication, although the authors should test this with odors of nonhuman animals as well. (It would also behoove them to repeat this experiment with more than one odiferous Dutchman, for the effect is, after all, supposed to be general.) If the result is replicable, it implies that the sporozoan parasite is doing something to the mosquito to make it bite more avidly. That, as I said, is to the parasite’s advantage.
If the parasite is indeed manipulating the mosquito to bite, how does it do this? We don’t know. As far as I know, in fact, in none of the cases of parasites manipulating hosts do we understand the biochemical/physiological basis of the manipulation. The authors report one study of the same mosquito, but infected with the rodent malaria parasite Plasmodium berghei, in which infected mosquitoes showed altered expression of 12 proteins expressed in their heads—including proteins possibly involved in the olfactory system. Smallengange et al. suggest that whatever the parasite is doing to the mosquito, it’s possibly doing it by changing the mosquito’s sense of smell, perhaps through changing how the olfactory receptor (OR) proteins bind to airborne stimulants.
It’s fascinating to contemplate how very simple organisms can induce complex behavioral changes in their hosts. It all goes to show the truth of the old dictum, “Evolution is smarter than you are.”
Smallegange, R. C., G.-J. van Gemert, M. van de Vegte-Bolmer, S. Gezan, W. Takken, R. W. Sauerwein, and J. G. Logan. 2013. Malariai infected mosquitoes express enhanced attraction to human odor. PLoS ONE 8:e63602 EP -.