Population structure of a vector of human diseases: Aedes aegypti in its ancestral range, Africa

Abstract

Aedes aegypti, the major vector of dengue, yellow fever, chikungunya, and Zika viruses, remains of great medical and public health concern. There is little doubt that the ancestral home of the species is Africa. This mosquito invaded the New World 400-500 years ago and later, Asia. However, little is known about the genetic structure and history of Ae. aegypti across Africa, as well as the possible origin(s) of the New World invasion. Here, we use ~17,000 genome-wide single nucleotide polymorphisms (SNPs) to characterize a heretofore undocumented complex picture of this mosquito across its ancestral range in Africa. We find signatures of human-assisted migrations, connectivity across long distances in sylvan populations, and of local admixture between domestic and sylvan populations. Finally, through a phylogenetic analysis combined with the genetic structure analyses, we suggest West Africa and especially Angola as the source of the New World's invasion, a scenario that fits well with the historic record of 16th-century slave trade between Africa and Americas.

Keywords: Aedes aegypti; Africa; SNP‐chip; genetics; migration; population structure.

Figure 1

Locations of Ae. aegypti sampled from mainland Africa and Reunion Island. Two of the sampling localities, Yaounde and Lope, include 5 and 2 sampling sites, respectively. The multiple sampling points in these localities are less than 3 km apart. The blue sampling site represents Ae. mascarensis used as outgroup

Figure 2

STRUCTURE bar plots for all Ae. aegypti populations and Ae. mascarensis. Population names are reported on the x‐axis. The y‐axis reports the probability of each individual (Q‐value) assigned to one of the genetic groups identified by fastSTRUCTURE, which are represented by different colors. Each bar represents an individual. Individuals with 100% assignment to one group are identified by a single color. Individuals with mixed ancestry are represented by bars with different percentages of colors. The thick black lines within the plots indicate population limits. Abbreviations: SA: South Africa, BF: Burkina Faso, ANG: Angola, masc: Ae. mascarensis

Figure 3

STRUCTURE bar plots for all African Ae. aegypti populations. Population names are reported on the x‐axis. For details, see legend of Figure2

Figure 4

Principal components analysis (PCA) on the broad dataset including all the Ae. aegypti populations as well as the Ae. mascarensis (a) and including only the African populations (b). PCA implemented and plotted in LEA R package, presenting the projection of all individual mosquitoes on the first two PCs. Populations originated from different regions are presented with different colors as shown in the inset

Figure 5

Discriminant analysis of principal components (DAPC) for the African populations as implemented and plotted in “adegenet” R package. The graph represents the individuals as dots and the groups as inertia ellipses. A bar plot of eigenvalues for the discriminant analysis (DA eigenvalues) is displayed in the inset. The bars in the inset represent the number of discriminant functions retained in the analysis, the first two of which are used in the plot. Population codes are as shown in Table 1

Figure 6

Isolation‐by‐distance plots for all pairs of populations from continental Africa. Statistical significance was evaluated through a Mantel test as implemented in the “ade4” R package. The original value of the correlation between the two matrices (geographic distance and genetic distance) is represented by a dot, while the histogram (a) represents the permutated values assuming the absence of spatial structure. Significant spatial structure results in the original value being out of the reference distribution. The correlation between geographic and genetic distance was plotted using the R package “MASS.” The scatterplot (b) shows one single consistent cloud of points. The colored gradient from light blue to red indicates the density of the points which are also shown as red points in the background of the graph. The blue dashed line represents the regression line between the geographic and genetic distance

Figure 7

Maximum likelihood (ML) rooted phylogenetic tree re‐constructed using a panel of ~12,000 SNPs. Ae. mascarensis was used as an outgroup, and Aaa samples from New World and Asia were used to test the distinctiveness of Aaf and Aaa lineages. Bootstraps are presented on the nodes; values <70 are not shown