Genetic Diversity and Phylogeny of Aedes aegypti, the Main Arbovirus Vector in the Pacific

Abstract

Background: The Pacific region is an area unique in the world, composed of thousands of islands with differing climates and environments. The spreading and establishment of the mosquito Aedes aegypti in these islands might be linked to human migration. Ae. aegypti is the major vector of arboviruses (dengue, chikungunya and Zika viruses) in the region. The intense circulation of these viruses in the Pacific during the last decade led to an increase of vector control measures by local health authorities. The aim of this study is to analyze the genetic relationships among Ae. aegypti populations in this region.

Methodology/principal finding: We studied the genetic variability and population genetics of 270 Ae. aegypti, sampled from 9 locations in New Caledonia, Fiji, Tonga and French Polynesia by analyzing nine microsatellites and two mitochondrial DNA regions (CO1 and ND4). Microsatellite markers revealed heterogeneity in the genetic structure between the western, central and eastern Pacific island countries. The microsatellite markers indicate a statistically moderate differentiation (FST = 0.136; P < = 0.001) in relation to island isolation. A high degree of mixed ancestry can be observed in the most important towns (e.g. Noumea, Suva and Papeete) compared with the most isolated islands (e.g. Ouvea and Vaitahu). Phylogenetic analysis indicated that most of samples are related to Asian and American specimens.

Conclusions/significance: Our results suggest a link between human migrations in the Pacific region and the origin of Ae. aegypti populations. The genetic pattern observed might be linked to the island isolation and to the different environmental conditions or ecosystems.

Fig 1. Pacific map locating Ae. aegypti sampling sites, 2013.

The nine sample sites are represented by the red dots.

Fig 2. Correlation between the geographic and genetic distance matrices.

The regression line corresponds to the standard major axis regression between pairwise genetic distances and logarithmic geographic distances with equation: Fst = - 0.1620 + 0.09113·log (geographic distance). The relationship was significant (Mantel test: Z = 16.3746; r = 0.6164; P < 0.001).

Fig 3. Model-based clustering of 270 Ae. aegypti individuals using STRUCTURE software.

Each individual is represented by a single vertical line; sample sites are separated by a black line; the whole sample is divided into K colors representing the number of clusters assumed. The colors show the estimated individual proportions of cluster membership.

Fig 4. Representation of the MtDNA haplotype frequencies within the sample sites.

The left circles indicate the CO1 haplotype frequencies and the right circles the ND4 haplotype frequencies. The arc length of each slice is proportional to the haplotype frequencies (as an example a semicircle represents 15 samples). Haplotype frequencies are indicated in S1 Table.

Fig 5. Median-joining network obtained with the haplotypes of all samples.

A- Representation for the mtDNA CO1 sequences. B- Representation for mtDNA ND4 sequences. The diameters of grey circles represent the frequency of each haplotype for all individuals. The red number indicates the position of the mutation on the analyzed sequences.

Fig 6. Phylogenetic tree obtained with a Bayesian inference of concatenated CO1 and ND4 sequence data.

Numbers in parentheses indicate the number of samples belonging to this haplotype. For the Australian sample, only the CO1 sequence was available. Rooting was inferred from DNA sequences of Anopheles pullus and Culex quinquefasciatus but were not represented for clarity