Global genetic diversity of Aedes aegypti

Abstract

Mosquitoes, especially Aedes aegypti, are becoming important models for studying invasion biology. We characterized genetic variation at 12 microsatellite loci in 79 populations of Ae. aegypti from 30 countries in six continents, and used them to infer historical and modern patterns of invasion. Our results support the two subspecies Ae. aegypti formosus and Ae. aegypti aegypti as genetically distinct units. Ae. aegypti aegypti populations outside Africa are derived from ancestral African populations and are monophyletic. The two subspecies co-occur in both East Africa (Kenya) and West Africa (Senegal). In rural/forest settings (Rabai District of Kenya), the two subspecies remain genetically distinct, whereas in urban settings, they introgress freely. Populations outside Africa are highly genetically structured likely due to a combination of recent founder effects, discrete discontinuous habitats and low migration rates. Ancestral populations in sub-Saharan Africa are less genetically structured, as are the populations in Asia. Introduction of Ae. aegypti to the New World coinciding with trans-Atlantic shipping in the 16th to 18th centuries was followed by its introduction to Asia in the late 19th century from the New World or from now extinct populations in the Mediterranean Basin. Aedes mascarensis is a genetically distinct sister species to Ae. aegypti s.l. This study provides a reference database of genetic diversity that can be used to determine the likely origin of new introductions that occur regularly for this invasive species. The genetic uniqueness of many populations and regions has important implications for attempts to control Ae. aegypti, especially for the methods using genetic modification of populations.

Keywords: Aedes aegypti; Aedes mascarensis; history; invasion; microsatellites.

Figure 1

Sampling locations of Aedes aegypti and Aedes mascarensis collections used in this study. Population codes are as labeled in Table 1. Putative Aedes aegypti queenslandensis is indicated as population 80 and Aedes mascarensis as population 81. Approximate locations are displayed in order to accommodate all labels.

Figure 2

Global genetic structure of Aedes aegypti. A) STRUCTURE bar plot indicating genetic groupings of 79 geographic locations based on 12 microsatellite loci. Each vertical bar represents an individual. The height of each bar represents the probability of assignment to each of K = 2 clusters as determined using the Delta K method. Each cluster is indicated by different colours: Aaa: red and Aaf: blue. Population code numbers are in Table 1. B) Discriminant Analysis of Principal Components (DAPC) on microsatellite allele frequencies showing two clear genetic clusters with minimal overlap; colors are as in A. C) Scatter plot of the first two principal components of the same data analysed in A and B. Groups corresponding to the Aaa and Aaf genetic clusters are plotted using the same colors as in A. Most of the variation is captured by the first and second PCA, as shown by the eigenvalue graph. D) STRUCTURE bar plot of those individual populations showing admixture in A, colors are consistent in A, B, and C.

Figure 3

Genetic structure of Aedes aegypti A) out-of-Africa and B) within Africa. STRUCTURE bar plots indicating relatedness among geographic locations. Population codes in A are as labeled in Table 1. Abbreviations in A top: C. A. = Central America, E. = Europe, Pac. = Australia, Tahiti, and Hawaii. Populations are sorted by countries and by longitude (W: west to E: east).

Figure 4

Genetic differentiation of major geographic regions. A) Scale of geographic genetic differentiation. Genetic distance is given as the linearized F_ST (F_ST/(1−F_ST) for the analysis of 12 microsatellite loci. Statistical significance was evaluated using a Mantel test and were all significant positive slopes (p<0.05) except for the Caribbean (p= 0.18) and S. America (p= 0.07) populations. B) Gene flow network between the continents or regions. The thickness of the lines is proportional to F_ST.

Figure 5

Genetic structure of Aedes aegypti within the American continent. Panels are A) All continental America, B) North America (excluding Exeter, California), and C) Mexico. STRUCTURE bar plots indicating relatedness among geographic locations. Plots representing the optimal K as determined by the Delta K method are indicated by an asterix (*). Discriminant Analysis of Principal Component plots for these data are shown in Fig S1.

Figure 6

Genetic structure of Aedes aegypti in the Caribbean and Asia/Pacific regions. A) STRUCTURE plots of Caribbean populations (including Florida Keys) with K number of clusters as indicated. Plots representing the optimal K as determined by the Delta K method are indicated by an asterix (*). B) Same populations in A in a Discriminant Analysis of Principal Components (DAPC). C) and D) same analyses as A) and B) for Asia and the Pacific (Australia, Tahiti, and Hawaii).

Figure 7

Evolutionary scenarios of Aedes aegypti colonization of Asia, evaluated using Approximate Bayesian Computation inference as implemented by the DIYABC software (Cornuet et al. 2014). Scenarios include three populations: Africa, America, and Asia, N=200 for each continent. T0 represents the most recent time point and increasing values of T go back in time. Scenario 1: Africa to America to Asia; Scenario 2: Africa to Asia to America; Scenario 3: Africa to America + Africa to Asia (after America colonization); and Scenario 4: Africa to America + Africa to Asia (before America colonization. Posterior probabilities are shown for each scenario. For more details see Materials and Methods and Table S1.

Figure 8

Genetic structure among Aedes aegypti and Aedes mascarensis populations. A) STRUCTURE bar plots for the 26 Ae. mascarensis sampled and, to avoid sample size artifacts, fifty random individuals subsampled from the large Aaa and Aaf dataset, excluding those populations with large admixture levels (Fig 2D). B) Discriminant Analysis of Principal Components for the same samples depicted in the STRUCTURE plot.