Gene Flow, Subspecies Composition, and Dengue Virus-2 Susceptibility among Aedes aegypti Collections in Senegal

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Abstract
Aedes aegypti, the “yellow fever mosquito”, is the primary vector to humans of the four serotypes of dengue viruses (DENV1-4) and yellow fever virus (YFV) and is a known vector of Chikungunya virus. There are two recognized subspecies of Ae. aegypti sensu latu (s.l.): the presumed ancestral form, Ae. aegypti formosus (Aaf), a primarily sylvan mosquito in sub-Saharan Africa, and Ae. aegypti aegypti (Aaa), found globally in tropical and subtropical regions typically in association with humans. The designation of Ae. aegypti s.l. subspecies arose from observations made in East Africa in the late 1950s that the frequency of pale “forms” of Ae. aegypti was higher in populations in and around human dwellings than in those of the nearby bush. But few studies have been made of Ae. aegypti s.l. in West Africa. To address this deficiency we have been studying the population genetics, subspecies composition and vector competence for DENV-2 of Ae. aegypti s.l. in Senegal. A population genetic analysis of gene flow was conducted among 1,040 Aedes aegypti s.l. from 19 collections distributed across the five phytogeographic regions of Senegal. Adults lacking pale scales on their first abdominal tergite were classified as Aedes aegypti formosus (Aaf) following the original description of the subspecies and the remainder were classified as Aedes aegypti aegypti (Aaa). There was a clear northwest–southeast cline in the abundance of Aaa and Aaf. Collections from the northern Sahelian region contained only Aaa while southern Forest gallery collections contained only Aaf. The two subspecies occurred in sympatry in four collections north of the Gambia in the central Savannah region and Aaa was a minor component of two collections from the Forest gallery area. Mosquitoes from 11 collections were orally challenged with DENV-2 virus. In agreement with the early literature, Aaf had significantly lower vector competence than Aaa. Among pure Aaa collections, the disseminated infection rate (DIR) was 73.9% with a midgut infection barrier (MIB) rate of 6.8%, and a midgut escape barrier (MEB) rate of 19.3%, while among pure Aaf collections, DIR = 34.2%, MIB rate = 7.4%, and MEB rate = 58.4%. Allele and genotype frequencies were analyzed at 11 nuclear single nucleotide polymorphism (SNP) loci using allele specific PCR and melting curve analysis. In agreement with a published isozyme gene flow study in Senegal, only a small and statistically insignificant percentage of the variance in allele frequencies was associated with subspecies. These results add to our understanding of the global phylogeny of Aedes aegypti s.l., suggesting that West African Aaa and Aaf are monophyletic and that Aaa evolved in West Africa from an Aaf ancestor. We conducted a population genetic study with 1,040 Aedes aegypti sensu latu (s.l.) collected from 19 sites distributed across the five phytogeographic regions of Senegal. Adult mosquitoes without pale scales on their first abdominal tergite were classified as Aedes aegypti formosus (Aaf) and those having pale scales as Aedes aegypti aegypti (Aaa). We found the two forms distributed along a northwest–southeast cline. Northern Sahelian collections contained only Aaa while the southern Forest gallery collections consisted of only Aaf. The two subspecies were sympatric in four collections north of The Gambia. Aaa was a minor component of two collections from the Forest gallery area. Eleven of these collections were fed a dengue-2 virus–infected bloodmeal. Consistent with the early literature, Aaf had lower vector competence than Aaa. In agreement with a recently published isozyme gene flow study in Senegal, analyzes of allele frequencies indicated only a small, nonsignificant percentage of the variance associated with subspecies. These results improve our understanding of the global phylogeny of Aedes aegypti s.l., suggesting that West African Aaa and Aaf are monophyletic and that Aaf, the black “sylvan” species, is the ancestor of Aaa, the lighter “domestic” species in West Africa.