Dry Season Ecology of Malaria Vectors

National Institute Of Allergy And Infectious Diseases

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Abstract

With a billion cases and one million deaths annually, vector borne diseases remain important. Malaria is still prevalent worldwide with an especially heavy burden in Africa. Outstanding gaps remain in our understanding of vector biology, including the strategies used by African malaria mosquitoes to persist through the long dry season. 1. We evaluated the contribution of aestivation to the persistence of mosquitoes in the Sahel by tracking mosquitoes marked by deuterium (2H) from the end of the wet season until the beginning of the subsequent wet season. If local aestivation is the only way An. coluzzii persists, the frequency of marked mosquitoes should remain stable, whereas finding no marked mosquitoes would be evidence against aestivation. After an initial enrichment, 33% of An. coluzzii were strongly marked. Seven months following enrichment, multiple analysis methods supported the ongoing presence of marked mosquitoes, compatible with the prediction that the fraction of marked mosquitoes should remain stable throughout the dry season if local aestivation is occurring. The results suggest that aestivation is a major persistence mechanism of An. coluzzii, contributing at least 20% of the adults at the onset of rains. This persistence strategy could influence mosquito control and malaria elimination campaigns. Faiman et al. 2022:Nature Ecology and Evolution:In Press. 2. Using aerial sampling of insects 40-290 m above ground in the Sahel, we have demonstrated regular and massive migration of Anopheles (Huestis et al. 2019: Nature) and showed that wild Anopheles withstood >11 hours high-altitude flight and subsequently reproduce and blood-feed on new hosts (Sanogo et al. 2021). Here, we describe this migration modality across Malian Culicidae. As well as Anopheles, 6 genera- Culex, Aedes, Mansonia, Mimomiya, Lutzia, and Eretmapodites comprised 90% of the 2,340 mosquitoes intercepted at altitude. Of the 50 species identified, 33 represented by multiple specimens were considered high-altitude windborne migrants. At altitude, females outnumbered males 6:1, and 93% of the females have taken at least one blood meal on a vertebrate host prior to departure. High-altitude flight coincided with peak disease transmission between June and November. These hallmarks bolster the role of windborne mosquitoes as carriers of mosquito-borne pathogens (MBPs). The infection rate in these high-altitude migrants for animal plasmodia was 2.4%, providing a proof of concept that vertebrate pathogens are transported by windborne mosquitoes at altitude. Fourteen of the 33 windborne mosquito species had been reported as vectors to 25 MBPs in West Africa, which represent 32% of the MBPs known in that region and include malaria, dengue, and Rift Valley fever. Further development of surveillance to map the sources and destinations of vectors and pathogens is key to understand, predict, and mitigate threats for public health. Yaro et al. 2022: bioRxiv: preprint & Frontiers in Epidemiology: Under Review. 3. To determine if mosquitoes engage in high-altitude flights beyond the Sahel, we have expanded aerial sampling into the savannas ecozones (Mali) and into the woodland and equatorial forests (Ghana). A total of 36 mosquito species were found (in 516 sequenced >150 m), belonging to 7 genera. Windborne mosquitoes occurred more commonly above perennial ecosystems including the equatorial forests than above the Sahel. Twelve mosquito species (33%) were found in a single ecozone, and 6 (17%) prevailed across all ecozones, suggesting that most mosquito species move between neighboring ecozones. Yet, movement between the equatorial forest to the Sahel >750 km also occur. 4) Dr. Bamou has been working on pathogen detection in the mosquitoes collected at altitude. Metagenomics analysis of few specimens indicated infection with insect specific viruses e.g., Aedes phasmavirus and Araticum virus, bacteria e.g., Wolbachia spp. and Asaia spp., a Trypanosoma spp. and Plasmodium spp. Targeted pathogen detection using pan-Plasmodium primers revealed 49 positives of 1,003 samples tested and confirmed using primers targeting the ribosomal 18S gene. Infectiousness ratemeasured as thoracic infectionwas 2.8%. Culex perexiguus, a known vector of avian plasmodia showed the highest prevalence (50%). The variation among ecozones was not significant (P>0.12) as expected if these pathogens are spread by mosquitoes that cross all ecozones (above). Additionally, infection of high-altitude mosquitoes with filariid nematodes was 0.7% (N=300) and several positives for flaviviruses. For the first time, we report detection of arboviruses, bacteria, and eukaryotic pathogens in high-altitude mosquitoes, thus providing proof of concept for their long-distance spread by windborne mosquitoes. 5. Mrs. Rita Frimpong, who has started a PhD program working on the insects collected at altitude in Mali and Ghana, focusing on species impacting public health and food security and comparing them to other taxa in terms of their seasonal and spatial high-altitude flight patterns. 6) To understand the scope of mosquito windborne migration, a literature survey of African mosquito borne diseases has been undertaken to generate a unique database of the African mosquito borne diseases from a One Health perspective. Initial analysis of the database produced important new insights into disease surveillance and for assessment of new regional and global threats of mosquito borne diseases. Lehmann et al. 2021: a preprint in bioRxiv. 7) Dormancy (aestivation) in Anopheline mosquitoes through the long dry season was demonstrated in An. coluzzii by several studies, but it has not been replicated in laboratory conditions, hindering progress on key questions such as how this state affects malaria vector competence. Following on progress made in our lab (Krajacich et al. 2020), Mr. Kouam (Postbac) compares survivorship and nutritional reserves of mosquitoes under conditions that mimic the late rainy and dry seasons and include specific larval priming conditions including increased salinity. 8) Mark release recapture experiments (MRRE) are key to address vector dispersal and survival. Our new marking method using synthetic DNA tags in a fluorescent solution (Faiman et al. 2021) was used in to track movement of mosquitoes between clusters of houses assigned to transmission-blocking-vaccine (TBV) or placebo. Tailored to determine if the movement of mosquitoes can undermine the measurement of the vaccine efficacy, we marked 33,922 Anopheles spp. and recaptured 253. Dispersal across the village, spanning 700 m was common within 3-7 d after releasethe maximum distance between release and capture, showing that mosquito movement undermine this TBV evaluation between clusters of compounds at the same village. Most MRREs on mosquitoes have been carried out within a single village with <2 km between the most distant possible capture and release sites. To assess inter-village dispersal, we used our new marking method (Faiman et all 2021) in 3 focal villages and 4 satellite villages from August to November 2021. Every 3 days, mosquitoes were captured in each focal village, marked, and released with unique color/DNA tags, identifying their date and site of release. The satellite villages extended the distance of capture to 12 km. A total of 42,367 mosquitoes were marked/released and 645 were recaptured. Preliminary results revealed that 2.1-3.6% found 3-6 km away, and 0-1% found 12 km away. Given the area around the focal villages, we estimate the fraction of mosquitoes that successfully emigrated from their village to others is 20%, with 7% reaching between up to 6 and up to 12 km. These results will impact models of disease spread by changing dispersal and survival distribution kernels.