Origin and expansion of the mosquito Aedes aegypti in Madeira Island (Portugal)

Abstract

Historically known as the yellow fever mosquito, Aedes aegypti invaded Madeira Island in 2005 and was the vector of the island's first dengue outbreak in 2012. We have studied genetic variation at 16 microsatellites and two mitochondrial DNA genes in temporal samples of Madeira Island, in order to assess the origin of the invasion and the population structure of this mosquito vector. Our results indicated at least two independent colonization events occurred on the island, both having a South American source population. In both scenarios, Venezuela was the most probable origin of these introductions, a result that is in accordance with the socioeconomic relations between this country and Madeira Island. Once introduced, Ae. aegypti has rapidly expanded along the southern coast of the island and reached a maximum effective population size (N_e) in 2012, coincident with the dengue epidemic. After the outbreak, there was a 10-fold reduction in N_e estimates, possibly reflecting the impact of community-based vector control measures implemented during the outbreak. These findings have implications for mosquito surveillance not only for Madeira Island, but also for other European regions where Aedes mosquitoes are expanding.

Figure 1

Madeira Island map showing sampling sites: Pául do Mar, a fishing village in the western point of Ae. aegypti distribution in the island; Funchal, the capital, where the main harbour is present; Santa Cruz, near the only Airport of the island. Below each locality name is the year of the first report of the introduction of the species. Pie charts indicate proportions of individuals assigned (Tq = 0.50) to each of the three genetic clusters determined by STRUCTURE (See text). Grey colour indicate admixed individuals with no cluster assignment. The map was produced using ArcGIS 10.2 (Esri, Redlands, CA).

Figure 2

Genetic structure of Madeira Ae. aegypti populations using 15 microsatellite markers. Each bar represents an individual with the colour of the bar giving the probability of the individual belonging to a genetic population or cluster. (a,b,c) STRUCTURE plots of Madeira populations with K number of clusters as indicated. An asterisk indicates the plot representing the optimal K as determined by the delta K method. Legend: 1–9: Funchal populations; 10–12: Paúl do Mar populations; 13- Santa Cruz population. For additional population details, see Table 1.

Figure 3

Discriminant analysis of principal components (DAPC) of Ae. aegypti populations in Madeira. Same populations depicted in the STRUCTURE plot shown in Fig. 2.

Figure 4

Analyses of Ae. aegypti from Madeira using 11 microsatellite markers. (a) STRUCTURE plot separating Aaa = Ae. ae. aegypti, red cluster; Aaf = Ae. ae. formosus, blue cluster. (b) Genetic structure of pantropical Ae. aegypti populations. (c) Genetic relationships between Madeira and South American populations. Colors of (a,b) are presented as in Gloria-Soria et al.. Legend: SS – São Sebastião, Brazil; Cali – Cali, Colombia; Bol – Bolivar, Venezuela; Zu – Zulia, Venezuela; Car – Caracas, Venezuela.

Figure 5

Discriminant analysis of principal components (DAPC) of Ae. aegypti populations using a Madeira/South America subset. Same populations depicted in the STRUCTURE plot shown in Fig. 4c.

Figure 6

Median-joining network based on haplotypes obtained from the mtDNA concatenated COI and ND4 sequences as generated by Network version 5. The size of the nodes corresponds to the number of individuals with corresponding haplotypes. The number indicates the number of mutations between each haplotype.

Figure 7

Phylogenetic tree obtained with a Bayesian inference of concatenated COI and ND4 sequences. Sequence number AY072044.1 is an outgroup Aedes albopictus specimen.