One of the most effective methods for the control of spread of malaria is the use of bed nets infused with insecticides. Most species of mosquitoes (the Anopheles genus) that carry the malarial parasite (Plasmodium falciparum) are considered to be strictly nocturnal - they are active only during the night.
Thus, sleeping under the net provides protection against getting bitten by the insect vectors of the disease. The net does it in two ways - by providing a mechanical barrier between the mosquito and the human, and by killing mosquitoes that get in contact with the infused insecticide.
As we have learned many times, often the hard way, evolution tends to find a way around such tricks. A number of Anopheles species or local populations have evolved resistance to pyrethroid insecticides usually used in the nets. Yet, the mechanical protection of the net should still be effective, right?
Not so fast! A new study published in September 21 in the Journal of Infectious Diseases documents a behavioral change in a local mosquito population that effectively works around the safety protection of bed nets. What do they do that's new? They changed the time of day when they bite!
Malaria-carrying mosquitoes are thought to all be strictly nocturnal. Recently, this dogma has started to be questioned, mainly because the rates of malaria did not significantly diminish in areas where bed nets have been implemented. Perhaps they fly and bite during the day, yet nobody bothered to test that hypothesis yet? A previous study noticed a shift in timing of activity and biting from middle of the night into early night. This study was quite systematic - repeating the experiment in two locations in Benin at three time-points: before, during and after the full implementation of bed nets in both locations.
What did they do? They collected mosquitoes in large numbers and recorded the time of day they caught mosquitos. In addition, they used morphology to identify the genus, and PCR to identify the species. Every single mosquito was Anopheles funestus. They tested the caught mosquitoes for pyrethrin resistance and did not detect any - every single mosquito died. Thus all the changes were strictly behavioral.
How did they collect them? They placed humans in strategic places as living targets. It looks pretty much like this video, except they actually captured the insects into vials, then transferred them into small bags:
During the period of just a few years as the bed nets got implemented in the two villages, local mosquitoes dramatically shifted the timing of activity. Instead of 2 or 3am, they now predominantly bit humans around 5am:
What does that mean?
First, we don't know yet if this was an evolutionary (i.e., genetic) change or a purely behavioral change. It is possible that there was quite a lot of genetic variation in timing of activity in the population a few years ago and that the bed nets provided a selective regimen that skewed the population to consist mainly of late night and dawn-active individuals. It is also possible that there is sufficient behavioral plasticity in the mosquito allowing it to learn the new best time of day to go out foraging. I'd love to see the mosquitoes placed in isolation chambers to monitor purely genetic patterns of circadian rhythms of activity.
But let's think more in ecological terms. There are several players here: the Plasmodium parasite, the Anopheles vector, the human host, and predators that eat mosquitoes, notably bats. I have written at length about this a few years ago. Here's a simple schematic of how the system works when undisturbed:
If the mosquito shifts to almost dawn, what happens?
First, the humans are up and about, outside of nets, readily available to bite. If the humans are healthy but mosquitos are carriers, this is a good way to transmit malaria to them.
But the humans who are sick, the sources of malaria, are still not available. At the times when they undergo "quaternary fevers", which are the times when malarial parasites are present in their blood (I explained this in great detail before), they are safely hidden by the nets in the middle of the night and they are not bitten by late-biting mosquitos.
Second, a mosquito that bites a human around dawn is much more likely to get detected by that human and be swiftly turned into a small, bloody mush.
Third, while a mosquito that flies around dawn may be able to avoid some of the bats (though not all of them - many bats hunt until the break of dawn), they are now increasingly vulnerable to other predators - frogs, lizards and birds - that tend to hunt at dawn.
As it often happens, there are pros and cons when it comes to evolving new adaptations. The bed nets are now selecting for new adaptations in mosquitoes. It is hard to predict what will be the pros and cons of those adaptations for human health, or the pros and cons of those adaptations for mosquitoes and their survival, or pros and cons of these adaptations to insects' predators. Future research on this will be both very interesting to watch and very useful for control of malaria.
Nicolas Moiroux, Marinely B. Gomez, Cédric Pennetier, Emmanuel Elanga, Armel Djènontin, Fabrice Chandre, Innocent Djègbé, Hélène Guis and Vincent Corbel, Changes in Anopheles funestus Biting Behavior Following Universal Coverage of Long-Lasting Insecticidal Nets in Benin, J Infect Dis.(2012) doi: 10.1093/infdis/jis565