Biogeography of the two major arbovirus mosquito vectors, Aedes aegypti and Aedes albopictus (Diptera, Culicidae), in Madagascar

Abstract

Background: In the past ten years, the Indian Ocean region has been the theatre of severe epidemics of chikungunya and dengue. These outbreaks coincided with a high increase in populations of Aedes albopictus that outcompete its sister taxon Aedes aegypti in most islands sampled. The objective of this work was to update the entomological survey of the two Aedes species in the island of Madagascar which has to face these arboviroses.

Methods: The sampling of Aedes mosquitoes was conducted during two years, from October 2007 to October 2009, in fifteen localities from eight regions of contrasting climates. Captured adults were identified immediately whereas immature stages were bred until adult stage for determination. Phylogenetic analysis was performed using two mtDNA genes, COI and ND5 and trees were constructed by the maximum likelihood (ML) method with the gene time reversible (GTR) model. Experimental infections with the chikungunya virus strain 06.21 at a titer of 107.5 pfu/mL were performed to evaluate the vector competence of field-collected mosquitoes. Disseminated infection rates were measured fourteen days after infection by immunofluorescence assay performed on head squashes.

Results: The species Aedes aegypti was detected in only six sites in native forests and natural reserves. In contrast, the species Aedes albopictus was found in 13 out of the 15 sites sampled. Breeding sites were mostly found in man-made environments such as discarded containers, used tires, abandoned buckets, coconuts, and bamboo cuts. Linear regression models showed that the abundance of Ae. albopictus was significantly influenced by the sampling region (F = 62.00, p < 2.2 × 10(-16)) and period (F = 36.22, p = 2.548 × 10(-13)), that are associated with ecological and climate variations. Phylogenetic analysis of the invasive Ae. albopictus distinguished haplotypes from South Asia and South America from those of Madagascar, but the markers used were not discriminant enough to discern Malagasy populations. The experimental oral infection method showed that six Ae. albopictus populations exhibited high dissemination infection rates for chikungunya virus ranging from 98 to 100%.

Conclusion: In Madagascar, Ae. albopictus has extended its geographical distribution whereas, Ae. aegypti has become rare, contrasting with what was previously observed. Changes are predominantly driven by human activities and the rainfall regime that provide suitable breeding sites for the highly anthropophilic mosquito Ae. albopictus. Moreover, these populations were found to be highly susceptible to chikungunya virus. In the light of this study, Ae. albopictus may have been involved in the recent outbreaks of chikungunya and dengue epidemics in Madagascar, and consequently, control measures should be promoted to limit its current expansion.

Figure 1

Distribution of Aedes mosquitoes in eight regions of Madagascar. Empty triangle Aedes albopictus and empty circle Aedes aegypti in the 1980s (Ravaonjanahary, 1978; Fontenille et al., 1989). Filled triangle Aedes albopictus and filled circle Aedes aegypti at the end of 2009 (this study). Encircled symbols highlighted changes in species distribution. Black filled square, town. Mosaic square, forest areas.

Figure 2

View of mosquito breeding sites. A: sites of immature stages; B: sites of adults.

Figure 3

Phylogeny inference from concatenated COI and ND5 genes of Aedes albopictus by the maximum likelihood (ML) method based on the general time reversible (GTR) model. Percentage bootstrap supports (1000 replicates) superior to 50% are given at each node. Branch lengths represent estimated substitutions per site. Code sequence is as follows: An (Ankazobe), DG (Diego-Suarez), MAH (Mahajanga), Man (Mananjary), MDA (Montagne d'Ambre), MR (Morondava), RN (La Réunion), TO (Toamasina), TS (Tsimbazaza). Sequences retrieved from Genbank belonged to specimens from Brasil (AJ971003.1 and AJ971014.1), Vietnam (AJ971004.1 and AJ971010.1), Thailand (AJ971015.1), Cambodia (AJ971006.1), France (AJ971009.1 and AJ971008.1), Hawai (AJ971011.1), USA (AJ971005.1), La Reunion (AJ971013.1 and AJ971012.1), and Madagascar (AJ971007.1).