The African mosquito-borne diseasosome: Geographical patterns and range expansion

Abstract

Mosquito-borne diseases (MBDs) such as malaria, dengue, and Rift Valley fever threaten public health and food security globally. Despite their cohesive nature, they are typically treated as distinct entities. Applying biological system analysis to the African MBDs from a One Health perspective, we provide the first biogeographic description of the African mosquito fauna corresponding with the pathogens they transmit. After compiling records accumulated over a century, we find that there are 677 mosquito species in Africa, representing 16 genera, and 151 mosquito-borne pathogens (MBPs) circulating primarily among wild tetrapods, dominated by viruses (95) and protozoans (47). We estimate that reported MBPs represent ~1% of the actual number. Unlike mosquitoes, African arboviruses and mammalian plasmodia represent a higher share of the World's total based on the area- species richness relationship (P<0.0001), explaining the disproportional large share of global MBPs that originated from Africa. Species richness of African mosquitoes and MBPs are similarly concentrated along the equator, peaking in central Africa, with a secondary ridge along eastern Africa. Moderate diversity and low endemicity in mosquitoes across the Sahel reveals a fauna with high propensity for long-range migration. Regional differences in species richness, endemicity, and composition agreed with country-based results. The composition of mosquitoes and MBPs separates sub-Saharan Africa from north Africa, in accordance with the Palearctic and Afrotropical faunal realms, and west and central Africa are clustered together distinctly from the cluster of eastern and southern Africa. With ~25% of the species occupying a single country, ~50% in 1-3 countries and <5% found in >25 countries, the typical ranges of both mosquitoes and MBPs are surprisingly small. The striking similarity in diversity and especially in range distributions of mosquitoes and MBPs suggest that most MBPs are transmitted by one or few narrow-range mosquito vectors. Exceptionally widespread mosquito species (e.g., Ae. aegypti, Cx. quinquefasciatus, and 10 Anopheles species) feed preferentially on people and domestic animals, and nearly half are windborne migrants. Likewise, exceptionally widespread MBPs are transmitted between people or domestic animals and are vectored by one or more of the aforementioned widespread mosquitoes. Our results suggest that few MBPs have undergone a dramatic range expansion, after adapting to people or domestic animals as well as to exceptionally-widespread mosquitoes. During the intermediate phase of range expansion, MBPs extend their vector and vertebrate host ranges with a concomitant gradual increase in geographical range. Because range size may serve as a marker of the phase of range expansion, ranking the African MBPs according to range, we identified several MBPs that pose elevated risk for disease emergence (e.g., Wesselsbron virus). Taken together, our database, approach, and results can help improve MBD surveillance and lead to a better understanding of disease emergence. This knowledge has the potential to improve capacity to prevent and mitigate new and emerging MBD threats.

Diversity, composition, altitude, and seasonality of high-altitude windborne migrating mosquitoes in the Sahel: Implications for disease transmission

“…Mosquitoes are not captured on the control panels not only because of their short duration but also because launch stations were set in open fields away from humans, animals, and shelters and because most mosquito species are nocturnal, while launch and retrieval occurred during the day. As it was found in over 55% of the genera, i.e., six (or seven) of the 11 genera in Mali (Lehmann et al, 2021;Wilkerson et al, 2021): Culex, Aedes, Anopheles, Mansonia, Mimomiya, Lutzia, and Eretmapodites (Table S1), this migration modality is rather common in mosquitoes. Likewise, high proportion of the species in Mali engage in high-altitude migration because depending on whether species sampled by a single specimen are included, our estimate ranges between 31% and 47%.…”

“…Data on vectorial status of the mosquito species at altitude was extracted from an extensive literature search summarized by (Lehmann et al ., 2021)[preprint]. Here, we included only mosquito species that were reported as probable or likely vectors of pathogens in West Africa based on the references listed in Table S3).…”

“…mcintoshi vectors at least 10 MBPs in Africa, but this species was conservatively excluded from the present analysis because no record pertained to West Africa. West Africa was defined to include the following countries: Benin, Burkina Faso, Gambia, Ghana, Guinea, Guinea Bissau, Ivory Coast, Liberia, Mali, Mauritania, Senegal, Sierra Leone, Togo (Lehmann et al ., 2021)[preprint]. The evidence used by these sources to implicate vectors includes one or more of the following findings as shown in Table S3: a) multiple isolations of a pathogen from wild vector from whole body or midgut [Win], b) from salivary glands/saliva [WIs], c) from legs [WIL], d) from Thorax and Head [WIth], e) detection of pathogen by circumsporozoite ELISA [WIc], f) laboratory experiments demonstrating vectorial competence (physiological capacity to support the pathogen to the infectious stage and capacity to transmit to a new host, following blood feeding on infectious blood meal), provided the mosquito naturally feeds on relevant hosts [LF], g) transovarial transmission, provided the mosquito naturally feeds on relevant hosts [TF], h) synchronous appearance of vector that feeds on relevant hosts during outbreak/peak transmission [Epi].…”

“…In West Africa, mosquitoes are known to transmit 79 pathogens (Lehmann et al, 2021). Of these, 25 MBPs (32%) are at risk for being transported and introduced into distant sites by one or more of the 14 windborne mosquito species that were reported as probable or partially implicated vectors (Fig 4 . and Table S3).…”

“…gambiae, and Cx. pipiens (Table S1) 842 (Braack et al, 2018;Lehmann et al, 2021;Wilkerson et al, 2021). An additional concern, we cannot 843 entirely rule out is that during the early phase of the molecular identification, certain specimens used as 844 positive control might have resulted in possible laboratory error due to contamination.…”