Is matching wing beats the key to maintaining genetic diversity in malarial mosquitoes?
Mosquitoes can impress potential mates by harmonizing the high-pitched whine of their tiny wings. Now, scientists have discovered how this musical matchmaking helps the insects to pick their perfect partner.
Research on one of the main malaria carriers in Africa, Anopheles gambiae, shows that the insects use subtle differences in tone to distinguish between forms of mosquito that appear to be physically identical.
The preference for harmony is so strong that it seems to be causing two forms of mosquito living in the same region to become separate species. This strict mating policy may be a key factor in maintaining the genetic diversity that makes the insect so adaptable to different environments, and could point to other ways to disrupt mosquito reproduction in malaria-ridden countries.
A. gambiae is actually a complex of seven species that are physically indistinguishable but with slightly different behavioural traits. In Burkina Faso, one of these species includes two forms — Mopti (M) and Savannah (S) — and additional forms exist in other parts of Africa.
The sheer diversity of the mosquito has puzzled scientists. "People studying this mosquito have wondered how it manages to speciate so quickly," says sensory physiologist Gabriella Gibson at the University of Greenwich, UK. Also unclear is how two forms that swarm together can avoid mating with one another, thereby preventing their genetic diversity from being diluted.
In 2006, Gibson and Ian Russell of the University of Sussex, UK, showed that the hum of the mosquitoes' wings might hold the answer. They found that Toxorhynchites brevipalpis mosquitoes change the frequency of their wing beats to match that of potential mates, yet diverge from that of members of the same sex1.
Both Gibson's team2 and a group led by Ron Hoy3 at Cornell University in Ithaca, New York, later found that in species in which the males and females have very different wing-beat frequencies — owing to size differences — mates tune their wing beats to the nearest harmonic frequency, usually a multiple of the slower wing-beat's frequency.
Now, Gibson and her colleagues have shown that this tuning can help mosquitoes to distinguish between the M and S forms of A. gambiae — the first directly observable behaviour that can tell the two apart. "There's always been a question of how they sort each other out," says Hoy. "What these acoustic studies are doing is opening a new window on the mosquito's sexual behaviour." The research is published this week in Current Biology4.
Gibson and her colleagues conducted their research at a field station in Burkina Faso. The M and S forms of A. gambiae coexist there, yet hybrids of the two are very rare, suggesting that they do not usually interbreed. The scientists captured mosquitoes of both types and glued them to the ends of pins. The tethered insects continued to beat their wings at frequencies close to those used in free flight. The team then used a microphone to measure the frequency both alone and in combination with potential mates.
Males of both forms are slightly smaller than females, and consequently fly with a higher wing-beat frequency of about 690 hertz, compared with females' 460 hertz. In both sexes, M mosquitoes beat their wings slightly faster than S.
When either sex of mosquito was placed within 2 centimetres of members of the opposite sex they sped up their wing beats and shifted up and down in pitch. If their partner was the same type of mosquito, the two insects would settle on wing-beat frequencies that were a ratio of 3:2, and together produced a harmonic tone at about 1,500 hertz. "It's like two singers trying to harmonize with each other, and if one goes sharp or flat the other one goes with them so they sound the same," Gibson says. Different types of mosquito, however, simply didn't harmonize.
Mosquitoes mate in flight, and Gibson speculates that this harmonizing behaviour helps to minimize turbulence as the male approaches the female.
Although Hoy's research has suggested that mosquitoes can hear up to 2,000 hertz, Gibson contends that the male and female mosquitoes cannot actually hear the high-pitched harmonic tone. Instead, they converge on the right note by minimizing the pulsing sound — or 'difference tones' — produced when the two notes are slightly off key. In A. gambiae, these difference tones were less than 22 hertz, and produced a characteristic electrical response in the antennae, the researchers found.
As Hoy and Gibson have studied different mosquito species, Hoy now hopes that they can work together to come to a firm conclusion about the auditory range of the insects. "It's an honest disagreement," he says, "and at some point I'd like them to come over for experiments in my lab."
Gibson, G. & Russell, I. Curr. Biol. 16, 1311-1316 (2006).
Warren, B., Gibson, G. & Russell, I. J. Curr. Biol. 19, 485-491 (2009).
Cator, L. J., Arthur, B. J., Harrington, L. C. & Hoy, R. R. Science 323, 1077-1079 (2009).
Pennetier, C., Warren, B., Dabire, R., Russell, I. J. & Gibson, G . Curr. Biol. doi:10.1016/j.cub.2009.11.040 (2009).
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Borrell, B. Mosquitoes mate in perfect harmony. Nature (2009). https://doi.org/10.1038/news.2009.1167