Despite extensive research on malaria for over a century, critical gaps remain in our understanding of the vectors; gaps that also limit our success in malaria control. We address some of the most critical gaps, namely the strategies used by African malaria mosquitoes to persist through the long dry season without surface waters for several months. Combining field and laboratory studies, our results provide compelling evidence that malaria vectors persist through the dry season by a form of dormancy (aestivation) and also engage in wind-assisted long-distance migration probably over hundreds of kilometers. These fundamental facets of vector biology have been controversial and, until now, were ignored due to insufficient evidence. Conventional and novel malaria and vector control strategies cannot afford to ignore aestivation and long-distance migration as processes that may hinder or aid the ultimate outcome. Last year, Nature has published our investigation of this problem based on five-years time series analysis. We extracted and compared the seasonal components of these population dynamics between the vector species. Strong species-specific pattern provided evidence for the vector strategy of persistence. For example, density peaks during the dry season, coupled with a rapid population growth closely following the first rain provided evidence for aestivation in A. coluzzii, whereas total absence throughout the dry season coupled with with 6-8 weeks delay in timing of normal population growth of A. gambiae (after than of A. coluzzii) was consistent with long-distance migration. These results build on other studies we have carried out based on mosquito mark-release-recapture experiments, variation in spatial distribution, aerial mosquito sampling (100-200 m above ground), seasonal changes in reproductive activity, flight activity, cuticular hydrocarbons, and responses to changes in photoperiod and temperature. This year we have published on the roles of morphological and cuticular hydro-carbon variation in underpinning aridity tolerance in these mosquitoes (Arcaz et al. 2016). One key finding was the dry-season reduction in the size of the mosquito spiracles (breathing openings) relative to body size, probably as an adaptation to reduce water loss. This morphological character may allow to identify aestivating mosquitoes in the field. Based on our findings, follow-up experiments have been designed to (i) find the hidden shelters used by aestivating A. coluzzii mosquitoes during the dry season, (ii) Sample mosquitoes flying in high altitudes (>100 m above ground) using traps tethered to helium filled balloons, (iii) determine the conditions promoting long-distance mosquito flights 10--200 m above ground, (iv) monitor flight aptitude of wild mosquitoes to measure seasonal and inter-species differences that could reflect long distance flight behavior, among other experiments. Over the past three years, we have been able to collect 30 A. gambiae s.l. flying in the lower jet stream among 3,000 mosquitoes and half a million insects. These results and ongoing studies using novel approaches provide fresh insights in malariology and vector biology. The findings that Anopheline vector of malaria and other disease vectors engage in long-distance flights and some are capable of dry-season dormancy open new frontiers of basic and applied research.

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2016
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Faiman, Roy; Solon-Biet, Samantha; Sullivan, Margery et al. (2017) The contribution of dietary restriction to extended longevity in the malaria vector Anopheles coluzzii. Parasit Vectors 10:156
Lehmann, Tovi; Weetman, David; Huestis, Diana L et al. (2017) Tracing the origin of the early wet-season Anopheles coluzzii in the Sahel. Evol Appl 10:704-717
Huestis, Diana L; Artis, Monica L; Armbruster, Peter A et al. (2017) Photoperiodic responses of Sahelian malaria mosquitoes Anopheles coluzzii and An. arabiensis. Parasit Vectors 10:621
Arcaz, Arthur C; Huestis, Diana L; Dao, Adama et al. (2016) Desiccation tolerance in Anopheles coluzzii: the effects of spiracle size and cuticular hydrocarbons. J Exp Biol 219:1675-88
Dubey, J P; Lehmann, T; Lautner, F et al. (2015) Toxoplasmosis in sentinel chickens (Gallus domesticus) in New England farms: Seroconversion, distribution of tissue cysts in brain, heart, and skeletal muscle by bioassay in mice and cats. Vet Parasitol 214:55-8
Wagoner, Kaira M; Lehmann, Tovi; Huestis, Diana L et al. (2014) Identification of morphological and chemical markers of dry- and wet-season conditions in female Anopheles gambiae mosquitoes. Parasit Vectors 7:294
Artis, Monica L; Huestis, Diana L; Lehmann, Tovi (2014) The effects of oviposition-site deprivation on longevity and bloodfeeding rate in Anopheles gambiae. Parasit Vectors 7:163
Dao, A; Yaro, A S; Diallo, M et al. (2014) Signatures of aestivation and migration in Sahelian malaria mosquito populations. Nature 516:387-90
Huestis, Diana L; Lehmann, Tovi (2014) Ecophysiology of Anopheles gambiae s.l.: persistence in the Sahel. Infect Genet Evol 28:648-61
Lehmann, Tovi; Dao, A; Yaro, A S et al. (2014) Seasonal variation in spatial distributions of Anopheles gambiae in a Sahelian village: evidence for aestivation. J Med Entomol 51:27-38

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