Complexities in the genetic structure of Anopheles gambiae populations in west Africa as revealed by microsatellite DNA analysis

Abstract

Chromosomal forms of Anopheles gambiae, given the informal designations Bamako, Mopti, and Savannah, have been recognized by the presence or absence of four paracentric inversions on chromosome 2. Studies of karyotype frequencies at sites where the forms occur in sympatry have led to the suggestion that these forms represent species. We conducted a study of the genetic structure of populations of An. gambiae from two villages in Mali, west Africa. Populations at each site were composed of the Bamako and Mopti forms and the sibling species, Anopheles arabiensis. Karyotypes were determined for each individual mosquito and genotypes at 21 microsatellite loci determined. A number of the microsatellites have been physically mapped to polytene chromosomes, making it possible to select loci based on their position relative to the inversions used to define forms. We found that the chromosomal forms differ at all loci on chromosome 2, but there were few differences for loci on other chromosomes. Geographic variation was small. Gene flow appears to vary among different regions within the genome, being lowest on chromosome 2, probably due to hitchhiking with the inversions. We conclude that the majority of observed genetic divergence between chromosomal forms can be explained by forces that need not involve reproductive isolation, although reproductive isolation is not ruled out. We found low levels of gene flow between the sibling species Anopheles gambiae and Anopheles arabiensis, similar to estimates based on observed frequencies of hybrid karyotypes in natural populations.

Figure 1

Pairwise gametic phase disequilibria for 21 microsatellite loci for pooled An. gambiae populations (above diagonal) and An. arabiensis (below diagonal). Black boxes with + sign indicate significant (0.01 level) linkage disequilibrium; white boxes with a − sign indicate lack of significant (0.01 level). Loci are grouped by linkage association, indicated at top and far left. 2R, right arm of chromosome 2; 2L, left arm of chromosome 2, etc.; ARRANG., chromosome 2R gene arrangements, treated as alleles for purposes of calculating gametic phase disequilibria.

Figure 2

Phenograms based on Unweighted pair-group method with arithmetic averaging of R_ST values to illustrate relationships among the An. gambiae chromosomal forms and An. arabiensis. Separate phenograms illustrate results for loci on all chromosomes and for loci on each chromosome separately. Bamako-B, Bamako form from the village of Banambani; Mopti-S, Mopti form from the village of Selenkenyi; etc. An “∗” indicates that two or more members of the joining operational taxonomic units differ statistically at the 0.01 level by an analysis of molecular variance (AMOVA) test for the loci on that chromosome combined. See text for further explanation.