The mosquito is so small it takes almost nothing to ruin it.--Mary Oliver
Mosquitoes devour some people and ignore others. If they like you, swat a dozen and a dozen more appear in their place, inserting their mouthparts into your capillaries and imbibing as quickly as they can. Why? We can consider this question in two ways. The version we usually think of is “why me?” What is it about my body that calls the mosquitoes in? But there is also a bigger why. Why does variation in human attractiveness to mosquitoes exist in the first place?
With regard to the second why, let’s be responsible and begin with some hypotheses. Mosquitoes are one of the most deadly groups of organisms on Earth, more deadly than tigers, snakes or even other humans. Mosquitoes kill by proxy. They transmit pathogens such as dengue, yellow fever and, that real devil among demons, big daddy malaria.
Over the last twelve thousand years (since the dawn of agriculture) malaria has killed enough people, particularly children, that those human populations exposed to malaria have evolved in response. Malaria's sickle altered human genomes in nearly all of the regions in which it was historically present. It was the high jump over which much of humanity never made it and those that did make it often did so at a cost. Populations long-exposed to malaria are more likely to have sickle cell anemia but also each of tens of other adaptations that either prevent infection or make its consequence less deadly. Nearly all of these adaptations have side effects, sometimes dangerous ones, just less dangerous than malaria. No organism has influenced human evolution more than the malaria parasite (and its chariots, the Anopheles mosquitoes). This leads me to three hypotheses.
Hypotheses—First, we might imagine that the descendants of those peoples who have lived with malaria might be less attractive to mosquitoes (because those who were more attractive died). Let's call this hypothesis "odorant camouflage." It will be my focus here. A second (and, frankly, less exciting) hypothesis might be that humans just happen to vary in terms of whatever it is that attracts mosquitoes. Perhaps some humans just happen to be more apparent to mosquitoes, lovely by accident. A third, but not final, hypothesis is that mosquitoes choose people whose smells indicate they will be better hosts.
Everyone attracts mosquitoes to some extent, so as long as they shall breathe. From the perspective of mosquitoes the world is composed of rivers of carbon dioxide flowing from the headwaters of animal’s mouths. Carbon dioxide flows from us all. Mosquitoes fly in the direction of higher carbon dioxide concentration and this leads them close enough, having found a warm body, to make more discerning decisions.
Because all adult humans breathe about the same amount (our hearts require this basic parity) the differences among us in our appeal to mosquitoes have to do not with our carbon dioxide but instead with our bodily odors. Most of your up close and personal odor, the mlange of you, is produced by the bacteria on and in you. You are densely covered in a fine and fuzzy patchwork of hundreds of species of bacteria. Kill all the bacteria in a patch of skin and that skin will be odorless (save a hint of whatever cleaning agent you used). When it comes to odor, you are your bacteria.
The perfect test—If we were to test our first hypothesis, we would want to compare the attractiveness of people from different regions to mosquitoes. Based on this hypothesis, we expect that malaria mosquitos, for example Anopheles gambiae, should be less attracted to the smell of the bacteria of humans from malarial zones, since any of the humans from these regions who were less attractive to mosquitoes would have been more likely to survive. One might then isolate which microbes or other sources produce the attractive (or unattractive) smell (and maybe even use them as a probiotic mosquito repellent).
After completing such a study with Anopheles gambiae, we would then need to test other mosquitoes. You might be surprised to learn that there are no fewer than three thousand species of mosquitoes on Earth and perhaps as many as six, seven or even ten thousand. There is no reason for the stories of these different species of mosquitoes (most of which avoid humans altogether), or what they are attracted to, to be terribly similar. They all perceive the river systems of carbon dioxide, but choose differently once they near bodies. To take one example, the common native mosquito species of eastern North America were never exposed to primates until humans came over the Bering straight and then wandered over the Rockies all the way to North Carolina. One can guess that these mosquitoes were then attracted to those humans who smelled most like the hosts that the mosquitoes had evolved to be attracted to, bison, elk, deer, giant sloths and the like. There are many mosquito stories.
But back to what we might discover. It appears no one has addressed the evolutionary “why” behind the differences among humans in their attractiveness to mosquitoes. Recent studies have, however, considered many aspects of “why me." Studies initially found variation in attractiveness to mosquitoes that could not be associated with diet, body size or gender. More recent studies, found that these differences appeared to be due to host odor. Then, in 2006, researchers found that cultured skin bacteria would attract mosquitoes.
Most recently, Dutch scientist Niels Verhulst led a study in which he and his team gently rolled beads on the feet of forty-eight volunteers (A. gambiae, the mosquito being studied, is an ankle biter). The beads were then put in a bag which was then presented to the mosquitoes (for their judgement). Based on the relative attraction of the mosquitoes to the different bags of beads the scientists established a kind of Zagat score for the discerning proboscis. Anopheles gambiae appears to have evolved to live with humans with the dawn of agriculture. But it loves some humans more than others. Perhaps, Verhulst reasoned, this is because of the specific mix of bacteria species on the ankles of each human. All but two of Verhulst's volunteers were Caucasian. I’ll note here that this is not the group of individuals it makes the most sense to expose to malaria mosquitoes for the simple reason that Anopheles gambiae and its malaria have never lived in the Netherlands. Yet, the researchers were in the Netherlands and it was a start. If Caucasian folks of the Netherlands differ in their appeal to mosquitoes, it might add insight into the “why me?"
The results were fascinating. The odors of seven of the volunteers were strongly preferred by the mosquitoes. Verhulst studied the bacteria on the feet of those and all of the other volunteers. The individuals with more kinds of bacteria (on their feet) tended to have fewer individual bacteria (you either have lots of kinds or lot of individuals, but not both). Those individuals whose odors mosquitoes preferred tended to have a lower diversity and higher abundance of microbes. Boom. The microbes did it, at least when it comes to 48 Dutch guys and a bunch of African mosquitoes. Or at least this is what we know so far (Verhulst thinks that where the diversity of bacteria is high, those diverse bacteria actually suppress the populations and odors of the bacteria that would otherwise be common. Were this true, these bacteria could be considered to be actively helping to disguise our odor, our stinking mutualists.).
But what about the other mosquito species? What about populations historically exposed to malaria versus those that have not been? What about inoculating people with bacteria that reduce bacteria odor? Nothing, none of it. We don’t know.
Stuck mid-story--For millions of people, the specific attractiveness of their skin is a thing of life or death. Hundreds of studies have considered why some people attract mosquitoes and others don’t. Bacteria were only invoked recently, but appear to be a big part of the story. The evolutionary context of this attractiveness has not been well considered. Given the strong impact malaria has had on human survival, it would be very surprising if there were no evolutionary element to the story of why some of us are more edible than others. But because the approach to malaria mosquitoes has primarily been medical, the lens has been narrow. Here is call for a big lens.
The good news is that at least as concerns hypothesis one, it would be easy to test the hypotheses that can be generated using evolution’s big lens. All Niels Verhulst and his colleagues would have to do would be to repeat their initial study and see if individuals from different ethnic groups differ in their bacteria as a function of the historic exposure of their peoples to malaria (surely the diversity of immigrants to Holland would help this endeavor) and if those bacteria differ in predictable ways in terms of their attractiveness to mosquitoes. This wouldn't be fully conclusive, but it would be a start. There are other approaches too.
In the meantime, if you are highly attractive to mosquitoes, you can thank your odor, an odor produced by your bacteria which might or might not have been influenced by the evolutionary history of your people.
I ended this article here and then I emailed Niels Verhulst to check that I hadn't missed something important about his work. He read the article and wrote," I agree." This, I thought, was good news, but he continued... " however we have some evidence that HLA genes are involved. HLA genes determine our body odor (and probably skin bacterial profile) and we found that individuals with a particular gene were more attractive to this mosquito (...) this gene occurs less frequently in Africa (where the most deadly malaria has long been prevalent) than in Europe or the US (where malaria's history has been more patchy)."
Here was a tantalizing result, a result that makes me want to start studying mosquitoes, a result that while it neither confirms nor rejects any of the hypotheses laid out above, offers the tantalizing suggestion that our relative attractiveness to mosquitoes is/might be/could be part of a more ancient story of agriculture, immigration, agriculture, mosquitoes and malaria. Unless, of course, it is not.
I love you science.