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Genetic Diversity of Anopheles coustani (Diptera: Culicidae) in Malaria Transmission Foci in Southern and Central Africa.

ABSTRACT: Despite ongoing malaria control efforts implemented throughout sub-Saharan Africa, malaria remains an enormous public health concern. Current interventions such as indoor residual spraying with insecticides and use of insecticide-treated bed nets are aimed at targeting the key malaria vectors that are primarily endophagic and endophilic. Anopheles coustani s.l., an understudied vector of malaria, is a species previously thought to exhibit mostly zoophilic behavior. Like many of these understudied species, An. coustani has greater anthropophilic tendencies than previously appreciated, is often both endophagic and exophagic, and carries Plasmodium falciparum sporozoites. The aim of this study was to explore genetic variation of An. coustani mosquitoes and the potential of this species to contribute to malaria parasite transmission in high transmission settings in Zambia and the Democratic Republic of the Congo (DRC). Morphologically identified An. coustani specimens that were trapped outdoors in these study sites were analyzed by PCR and sequencing for species identification and bloodmeal sources, and malaria parasite infection was determined by ELISA and qPCR. Fifty An. coustani s.s. specimens were confirmed by analysis of mitochondrial DNA cytochrome c oxidase subunit I (COI) and ribosomal internal transcribed spacer region 2 (ITS2). Maximum likelihood phylogenetic analysis of COI and ITS2 sequences revealed two distinct phylogenetic groups within this relatively small regional collection. Our findings indicate that both An. coustani groups have anthropophilic and exophagic habits and come into frequent contact with P. falciparum, suggesting that this potential alternative malaria vector might elude current vector control measures in northern Zambia and southern DRC.

SUBMITTER: Ciubotariu II

PROVIDER: S-EPMC7899271 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Anopheles albimanus is a malaria vector in Central America, northern South America and the Caribbean. Although a public health threat, An. albimanus precopulatory mating behaviors are unknown. Acoustics play important roles in mosquito communication, where flight tones allow males to detect and attract potential mates. The importance of sound in precopulatory interactions has been demonstrated in Toxorhynchites brevipalpis, Aedes aegypti, Culex quinquefasciatus and Anopheles gambiae; convergence in a shared harmonic of the wing beat frequency (WBF) during courtship is thought to increase the chance of copulation. To our knowledge, An. albimanus precopulatory acoustic behaviors have not been described to date. Here, we characterized An. albimanus (i) male and female flight tones; (ii) male-female precopulatory acoustic interactions under tethered and free flight conditions; and (iii) male-male acoustic interactions during free flight. RESULTS:We found significant increases in the WBFs of both sexes in free flight compared to when tethered. We observed harmonic convergence between 79% of tethered couples. In free flight, we identified a female-specific behavior that predicts mate rejection during male mating attempts: females increase their WBFs significantly faster during mate rejection compared to a successful copulation. This behavior consistently occurred during mate rejection regardless of prior mating attempts (from the same or differing male). During group flight, males of An. albimanus displayed two distinct flying behaviors: random flight and a swarm-like, patterned flight, each associated with distinct acoustic characteristics. In the transition from random to patterned flight, males converged their WBFs and significantly decreased flight area, male-male proximity and the periodicity of their trajectories. CONCLUSIONS:We show that tethering of An. albimanus results in major acoustic differences compared to free flight. We identify a female-specific behavior that predicts mate rejection during male mating attempts in this species and show that male groups in free flight display distinct flying patterns with unique audio and visual characteristics. This study shows that An. albimanus display acoustic features identified in other mosquito species, further suggesting that acoustic interactions provide worthwhile targets for mosquito intervention strategies. Our results provide compelling evidence for swarming in this species and suggests that acoustic signaling is important for this behavior.

Project description:BackgroundIn Brazil, the autochthonous transmission of extra-Amazonian malaria occurs mainly in areas of the southeastern coastal Atlantic Forest, where Anopheles cruzii is the primary vector. In these locations, the population density of the mosquito varies with altitude (5-263 m above sea level), prompting us to hypothesise that gene flow is also unevenly distributed. Describing the micro-geographical and temporal biological variability of this species may be a key to understanding the dispersion of malaria in the region. We explored the homogeneity of the An. cruzii population across its altitudinal range of distribution using wing shape and mtDNA gene analysis. We also assessed the stability of wing geometry over time.MethodsLarvae were sampled from lowland (5-20 m) and hilltop (81-263 m) areas in a primary Atlantic Forest region, in the municipality of Cananéia (State of São Paulo, Brazil). The right wings of males and females were analysed by standard geometric morphometrics. Eighteen landmarks were digitised for each individual and a discriminant analysis was used to compare samples from the hilltop and lowland. A 400-bp DNA fragment of the mitochondrial cytochrome oxidase gene subunit I (CO-I) was PCR-amplified and sequenced.ResultsWing shapes were distinct between lowland and hilltop population samples. Results of cross-validated tests based on Mahalanobis distances showed that the individuals from both micro-environments were correctly reclassified in a range of 54-96%. The wings of hilltop individuals were larger. The CO-I gene was highly polymorphic (haplotypic diversity = 0.98) and altitudinally structured (Фst = 0.085 and Jaccard = 0.033). We found 60 different haplotypes but only two were shared by the lowland and hilltop populations. Wing shape changed over the brief study period (2009-2013).ConclusionsWing geometry and CO-I gene analysis indicated that An. cruzii is vertically structured. Wing shape varied rapidly, but altitude structure was maintained. Future investigations should identify the biotic/abiotic causes of these patterns and their implications in the local epidemiology of malaria.

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Project description:Fragmentation of natural environments as a result of human interference has been associated with a decrease in species richness and increase in abundance of a few species that have adapted to these environments. The Brazilian Atlantic Forest, which has been undergoing an intense process of fragmentation and deforestation caused by human-made changes to the environment, is an important hotspot for malaria transmission. The main vector of simian and human malaria in this biome is the mosquito Anopheles cruzii. Anthropogenic processes reduce the availability of natural resources at the tree canopies, An. cruzii primary habitat. As a consequence, An. cruzii moves to the border of the Atlantic Forest nearing urban areas seeking resources, increasing their contact with humans in the process. We hypothesized that different levels of anthropogenic changes to the environment can be an important factor in driving the genetic structure and diversity in An. cruzii populations. Five different hypotheses using a cross-sectional and a longitudinal design were tested to assess genetic structure in sympatric An. cruzii populations and microevolutionary processes driving these populations. Single nucleotide polymorphisms were used to assess microgeographic genetic structure in An. cruzii populations in a low-endemicity area in the city of São Paulo, Brazil. Our results show an overall weak genetic structure among the populations, indicating a high gene flow system. However, our results also pointed to the presence of significant genetic structure between sympatric An. cruzii populations collected at ground and tree-canopy habitats in the urban environment and higher genetic variation in the ground-level population. This indicates that anthropogenic modifications leading to habitat fragmentation and a higher genetic diversity and structure in ground-level populations could be driving the behavior of An. cruzii, ultimately increasing its contact with humans. Understanding how anthropogenic changes in natural areas affect An. cruzii is essential for the development of more effective mosquito control strategies and, on a broader scale, for malaria-elimination efforts in the Brazilian Atlantic Forest.

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Genetic Diversity of Anopheles coustani (Diptera: Culicidae) in Malaria Transmission Foci in Southern and Central Africa.

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