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Open Access Research

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

Fara Nantenaina Raharimalala12, Lala Harivelo Ravaomanarivo2, Pierre Ravelonandro3, Lala Sahondra Rafarasoa2, Karima Zouache1, Van Tran-Van1, Laurence Mousson4, Anna-Bella Failloux4, Eléonore Hellard5, Claire Valiente Moro1, Bakoly Olga Ralisoa2 and Patrick Mavingui16*

Author Affiliations

1 UMR CNRS 5557 Ecologie Microbienne, Université Lyon 1, 43 boulevard du 11 Novembre 1918, Villeurbanne cedex 69622, France

2 Département d'Entomologie, de la Facultés des Sciences d'Antananarivo, Antananarivo, Madagascar

3 Centre National de Recherche sur l'Environnement, Antananarivo, Madagascar

4 Institut Pasteur, Département de Virologie, Laboratoire Arbovirus et Insectes Vecteurs, Paris, France

5 CNRS; UMR 5558, Laboratoire de Biométrie et Biologie Evolutive, Université Lyon 1, Université de Lyon, Lyon, Villeurbanne F-69622, France

6 Laboratoire Arbovirus et Insectes Vecteurs, Institut Pasteur, Paris, France

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Parasites & Vectors 2012, 5:56  doi:10.1186/1756-3305-5-56

Published: 20 March 2012

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.