Quantifying flight aptitude variation in wild A. gambiae s.l. in order to identify long-distance migrants

Background In the West African Sahel, mosquito reproduction is halted during the 5-7 month-long dry season, due to the absence of surface waters required for larval development. However, recent studies have suggested that both Anopheles gambiae s.s and An. arabiensis repopulate this region via migration from distant locations where larval sites are perennial. An. coluzzii engages in more regional migration, presumably within the Sahel, following shifting resources correlating with the ever-changing patterns of Sahelian rainfall. Understanding mosquito migration is key to controlling malaria—a disease that continues to claim more than 400,000 lives annually, especially those of African children. Using tethered flight data of wild mosquitoes, we evaluated the distribution of flight parameters as indicators of long-range migrants vs. appetitive flyers, compared species specific seasonal differences and gonotrophic states on flight activity. We also evaluated morphometrical differences in the wings of mosquitoes exhibiting high flight activity (HFA) vs. low flight activity (LFA). Methods We used a novel tethered-flight assay to characterize flight in the three primary malaria vectors- An. arabiensis, An. coluzzii and An. gambiae s.s. The flights of tethered wild mosquitoes were audio-recorded from 21:00h to 05:00h in the following morning and three flight aptitude indices were examined: total flight duration, longest flight bout, and the number of flight bouts during the assay. Results The distributions of all flight indices were strongly skewed to the right, indicating that the population consisted of a majority of low-flight activity (LFA) mosquitoes and a minority of high-flight activity (HFA) mosquitoes. The median total flight was 586 seconds and the maximum value was 16,110 seconds (~4.5 h). In accordance with recent results, flight aptitude peaked in the wet season, and was higher in gravid females than in non-bloodfed females. Flight aptitude was also found to be higher in An. coluzzii compared to An. arabiensis, with intermediate values in An. gambiae s.s., but displaying no statistical difference. Evaluating differences in wing size and shape between LFA individuals and HFA ones, the wing size of HFA An. coluzzii was larger than that of LFAs during the wet season—its length was wider than predicted by allometry alone, indicating a change in wing shape. No statistically significant differences were found in the wing size/shape of An. gambiae s.s. or An. arabiensis. Conclusions The partial agreement between the tethered flight results and recent results based on aerial sampling of these species suggest a degree of discrimination between appetitive flyers and long-distance migrants although identifying HFAs as long-distance migrants is not recommended without further investigation.