Dry Season Ecology of Malaria Vectors

National Institute Of Allergy And Infectious Diseases

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Abstract

With a billion cases worldwide and one million deaths annually, vector borne diseases remain important. Malaria is prevalent worldwide with an especially heavy burden in Africa. Outstanding gaps remain in our understanding of vector biology, limiting our impact on vector-borne disease control. 1. To resolve the 'dry season malaria paradox' (above), We evaluated the contribution of aestivation to the persistence of mosquitoes in the Sahel by tracking wild 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 analyses revealed the presence of marked mosquitoes. 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 (Faiman et al. 2022:Nature Ecology and Evolution). This persistence strategy could influence mosquito control and malaria elimination campaigns. 2. Extending previously published results on aerial sampling of mosquitoes 40-290 m above ground in the Sahel (Huestis et al. 2019: Nature, Sanogo et al. 2021: J. Med Ent.), we describe how other mosquito species use this migration modality (Yaro et al. 2022: Frontiers in Epidemiology). A total of 7 genera- Culex, Aedes, Anopheles, Mansonia, Mimomiya, Lutzia, and Eretmapodites comprised 90% of the 2,340 mosquitoes intercepted at altitude over the Sahel of Mali. Of the 50 species identified, 33 represented by multiple specimens were considered high-altitude windborne migrants. At altitude, females outnumbered males 6:1, and >90% 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 7%, 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, including malaria, dengue, and Rift Valley fever. These results suggest that the development of aerial pathogen/disease surveillance to map the sources and destinations of vectors and pathogens my complement traditional methods and supply unique information to mitigate public health threats. 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) as well as in Kenya (East Africa). A total of 36 mosquito species were found in these West African ecozones (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 may also occur. A one-year study in Kenya has demonstrated that windborne mosquitoes and other insects are common across the continent (Atieli et al. 2023). 4) Dr. Bamou has been working on pathogen detection in the mosquitoes collected at altitude. Pan-genus pathogen detection followed by metagenomics analysis of select specimens indicated infection with arboviruses, including human zoontotic viruses: West Nile virus and M'Poko virus. Additionally, insect specific viruses e.g., Aedes phasmavirus and Araticum virus, were detected, as well as bacteria: Wolbachia spp. and Asaia spp. Fourteen species of avian Plasmodia were identified by sequencing of 49 positive mosquitoes. Infectiousness rate measured as thoracic infection was 2.8%. Culex perexiguus, a known vector of avian plasmodia showed the highest prevalence (50%). Between-ecozone variation was not significant (P>0.1) as expected if these pathogens are spread by mosquitoes that travel across ecozones. Additionally, infection of high-altitude mosquitoes with filariid nematodes was 0.7% (N=300). 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. Mr. Zachary Dankowicz (High School volunteer/summer intern) has discovered high-altitude ceratopogonid species that may include arbovirus vectors. 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: Submitted. The revised paper is being submitted to a journal. 7) Dormancy (aestivation) in Anopheline mosquitoes through the long dry season was demonstrated in An. coluzzii (above), but it has not been replicated in laboratory conditions, hindering progress on questions such as how this state affects malaria vector competence. Following earlier advance in our lab (Krajacich et al. 2020), Mr. Kouam (Postbac) compared 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) In a new collaboration with West African Center for Emerging Infectious Diseases (WAC-EID of NIAID CRIED, led by Dr. Scott Weaver, UTMB and Mawlouth Diallo, Institute Pasteur, Dakar) we initiated new studies in Kedougou Senegal on windborne spread of arboviruses and other pathogens in mosquitoes. In this novel study, we compare aerial and ground samples of msoaquitoes and their pathogens above Kedougou--a well-known hotspot for arbovirus activity that has been studies for >50 years with a an aerial station located 110 km in Mali near the border of Senegal to address if arboviruses can spread in windbronem mosquitoes from enzootoic (sylvatic) cycles into new areas and forms outbreaks tens or hundreds of kilometers away.