Chromosomal inversions, natural selection and adaptation in the malaria vector Anopheles funestus

Abstract

Chromosomal polymorphisms, such as inversions, are presumably involved in the rapid adaptation of populations to local environmental conditions. Reduced recombination between alternative arrangements in heterozygotes may protect sets of locally adapted genes, promoting ecological divergence and potentially leading to reproductive isolation and speciation. Through a comparative analysis of chromosomal inversions and microsatellite marker polymorphisms, we hereby present biological evidence that strengthens this view in the mosquito Anopheles funestus s.s, one of the most important and widespread malaria vectors in Africa. Specimens were collected across a wide range of geographical, ecological, and climatic conditions in Cameroon. We observed a sharp contrast between population structure measured at neutral microsatellite markers and at chromosomal inversions. Microsatellite data detected only a weak signal for population structuring among geographical zones (F(ST) < 0.013, P < 0.01). By contrast, strong differentiation among ecological zones was revealed by chromosomal inversions (F(ST) > 0.190, P < 0.01). Using standardized estimates of F(ST), we show that inversions behave at odds with neutral expectations strongly suggesting a role of environmental selection in shaping their distribution. We further demonstrate through canonical correspondence analysis that heterogeneity in eco-geographical variables measured at specimen sampling sites explained 89% of chromosomal variance in A. funestus. These results are in agreement with a role of chromosomal inversions in ecotypic adaptation in this species. We argue that this widespread mosquito represents an interesting model system for the study of chromosomal speciation mechanisms and should provide ample opportunity for comparative studies on the evolution of reproductive isolation and speciation in major human malaria vectors.

FIG. 1.

Sampling sites. Topographic Map of Cameroon showing the study area divided into four ecological zones (A–D) and villages sampled in each zone (dots). Dotted lines delimit biogeographic domains as defined in Olivry (1986). Elevation Source: Shuttle Radar Topography Mission, http://www2.jpl.nasa.gov/srtm

FIG. 2.

Neutrality tests. single-locus F_ST estimates among geographic populations of A. funestus in Cameroon, plotted against expected heterozygosity (Nei 1987). (A) Data from 16 microsatellites markers located inside (circles) and outside (triangles) common polymorphic chromosomal inversions. (B) Data form seven chromosomal inversion systems. In both panels, outlier loci are pointed by arrows and referred to by their names. Dashed lines and solid lines represent the 95% and 99% confidence limits under the hypothesis of neutrality of the loci, respectively.

FIG. 3.

Eco-geographical chromosome inversion distributions. CCA diagram showing the ordination of chromosomal inversions for each homozygote (standard or inverted) along the first two canonical axes (explaining 89.7% of variance). Open triangles represent STANDARD homokaryotes. Full triangles represent INVERTED homokaryotes. EGVs are passively plotted on the graph. Alt, altitude; temp, temperature; rain, rainfall; lat, latitude; long, longitude; WVP: water vapor pressure.