Spatio-temporal genetic structure of Anopheles gambiae in the Northwestern Lake Victoria Basin, Uganda: implications for genetic control trials in malaria endemic regions

Abstract

BackgroundUnderstanding population genetic structure in the malaria vector Anopheles gambiae (s.s.) is crucial to inform genetic control and manage insecticide resistance. Unfortunately, species characteristics such as high nucleotide diversity, large effective population size, recent range expansion, and high dispersal ability complicate the inference of genetic structure across its range in sub-Saharan Africa. The ocean, along with the Great Rift Valley, is one of the few recognized barriers to gene flow in this species, but the effect of inland lakes, which could be useful sites for initial testing of genetic control strategies, is relatively understudied. Here we examine Lake Victoria as a barrier between the Ugandan mainland and the Ssese Islands, which lie up to 60 km offshore. We use mitochondrial DNA (mtDNA) from populations sampled in 2002, 2012 and 2015, and perform Bayesian cluster analysis on mtDNA combined with microsatellite data previously generated from the same 2002 mosquito DNA samples.ResultsHierarchical analysis of molecular variance and Bayesian clustering support significant differentiation between the mainland and lacustrine islands. In an mtDNA haplotype network constructed from this and previous data, haplotypes are shared even between localities separated by the Rift Valley, a result that more likely reflects retention of shared ancestral polymorphism than contemporary gene flow.ConclusionsThe relative genetic isolation of An. gambiae on the Ssese Islands, their small size, level terrain and ease of access from the mainland, the relative simplicity of the vectorial system, and the prevalence of malaria, are all attributes that recommend these islands as possible sites for the testing of genetic control strategies.

Reduced-representation sequencing identifies small effective population sizes of Anopheles gambiae in the north-western Lake Victoria basin, Uganda

“…A variety of molecular markers have been used to explore genetic differentiation in continental populations including microsatellites, mitochondrial DNA, allozymes, and SNPs [ 61 , 69 ]. That all of these marker systems identify the same pattern of low genetic differentiation on the continent suggests that the heightened differentiation estimated in this study is not attributable to different marker systems, an assertion strengthened by the previous Ssese island studies of Kayondo et al [ 21 ] and Lukindu et al [ 70 ] using microsatellites and mtDNA, respectively.…”

A differential expression of pyrethroid resistance genes in the malaria vector Anopheles funestus across Uganda is associated with patterns of gene flow

“…Our results corroborate the previous microsatellite study in An . gambiae in Uganda, where Rift valley shows a great barrier to gene flow [ 16 , 17 ]. However, the greater estimates of F ST at two loci located at the vicinity of a known pyrethroid resistance genomic region (rp1) [ 14 ], suggests that the genetic differentiation observed between Arua and the other locations in Uganda could also be influenced by a difference in local selection as the FUNO and AFND6 loci have previously be shown to be under selection due to location of the cluster of pyrethroid resistance CYP6 P450 genes in this region [ 7 , 47 ].…”

“…This is further the case in the context of ecological landscape changes such as the Rift Valley that spans East Africa and previously shown to restrict gene flow in An. gambiae [16,17]. Indeed, based on microsatellite markers, the magnitude of genetic differentiation (F ST ) between populations on opposite sides of the continent (~6000 km apart) was~0.03, while the corresponding value between populations on either side of the Rift Valley (~400-500 km) was~0.1 [17][18][19][20].…”

Effects of indoor residual spraying and outdoor larval control on Anopheles coluzzii from São Tomé and Príncipe, two islands with pre-eliminated malaria

“…coluzzii after long-term interventions [70] which were similar to the present findings in STP. Differentiation of vector population by mitochondrial DNA marker in the large lake area have also been found in the lacustrine islands located in the Lake Victoria which borders Kenya, Uganda and Tanzania [71]. Due to the small area and the relative simplicity of human mobility and vectorial-parasitological system on islands, it is much easier to eliminate malaria compared to the continental areas.…”