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In the malaria vector Anopheles gambiae, alternative arrangements of chromosome 2 (2La and 2L+(a)) vary in relative frequency along clines of aridity, suggesting the action of natural selection on targets within the inversion. Our long term goal of detecting such targets depends in part on the level of genetic exchange between arrangements. Accordingly, we estimated recombination rates on 2L from the backcross progeny of 2La/+(a) heterokaryotypes and as a control, from 2L+(a) homokaryotypes. In homokaryotypes, the recombination rate was uniform at ~2.0 centimorgans per megabase (cM/Mb). In heterokaryotypes, recombination within the rearranged region was reduced to < 0.5 cM/Mb, with slightly higher but nevertheless reduced levels (< 1.0 cM/Mb) flanking the rearrangement. Yet, gene exchange was recorded between nearly all markers, including those very near the distal inversion breakpoint. These results suggest that reduced recombination is a necessary but not sufficient mechanism for genetic isolation between alternative arrangements, and that the targets of natural selection can be identified against the different chromosomal backgrounds.

Emerging species within the primary malaria vector Anopheles gambiae show different ecological preferences and significant prezygotic reproductive isolation. They are defined by fixed sequence differences in X-linked rDNA, but most previous studies have failed to detect large and significant differentiation between these taxa elsewhere in the genome, except at two other loci on the X chromosome near the rDNA locus. Hypothesizing that this pericentromeric region of the X chromosome may be accumulating differences faster than other regions of the genome, we explored the pattern and extent of differentiation between A. gambiae incipient species and a sibling species, A. arabiensis, from Burkina Faso, West Africa, at 17 microsatellite loci spanning the X chromosome. Interspecific differentiation was large and significant across the entire X chromosome. Among A. gambiae incipient species, we found some of the highest levels of differentiation recorded in a large region including eight independent loci near the centromere of the X chromosome. Outside of this region, no significant differentiation was detected. This pattern suggests that selection is playing a role in the emergence of A. gambiae incipient species. This process, associated with efficient exploitation of anthropogenic modifications to the environment, has public health implications as it fosters the spread of malaria transmission both spatially and temporally.

The M and S molecular forms of Anopheles gambiae are considered to be incipient species, despite residual gene exchange. Of the three small genome regions that are strongly differentiated between the molecular forms ("speciation islands"), two are located near centromeres, on the left arm of chromosome 2 and the X chromosome. To test the prediction of reduced recombination in these islands, we estimated recombination rates between microsatellite loci on the X chromosome using two M-form strains. Across most of the chromosome, recombination occurred at approximately 1 centimorgan per megabase (cM Mb(-1)), a value closely matching the genome-wide average estimated for A. gambiae and for other eukaryotes. Recombination was much higher at the telomeric end, > 7 cM Mb(-1). In the speciation island at the centromeric end, recombination was sharply reduced to approximately 0.2 cM Mb(-1), consistent with a role for reduced recombination in maintaining differentiation between nascent species despite gene flow.

The M and S molecular forms of Anopheles gambiae are undergoing speciation as they adapt to heterogeneities in the environment, spreading malaria in the process. We hypothesized that their divergence despite gene flow is facilitated by reduced recombination at the centromeric (proximal) end of the X chromosome. We sequenced introns from 22 X chromosome genes in M and S from two locations of West Africa where the forms are sympatric. Generally, in both forms nucleotide diversity was high distally, lower proximally, and very low nearest the centromere. Conversely, differentiation between the forms was virtually zero distally and very high proximally. Pairwise comparisons to a close relative, the sibling species Anopheles arabiensis , demonstrated uniformly high divergence regardless of position along the X chromosome, suggesting that this pattern is not purely mechanical. Instead, the pattern observed for M and S suggests the action of divergent natural selection countering gene flow only at the proximal end of the X chromosome, where recombination is reduced. Comparison of sites with fixed differences between M and S to the corresponding sites in A. arabiensis revealed that derived substitutions had been fixed in both forms, further supporting the hypothesis that both have been under selection. These derived substitutions are fixed in the two West African samples and in samples of S from western and coastal Kenya, suggesting that selection occurred before the forms expanded to their current ranges. Our findings are consistent with a role for suppressed genetic recombination in speciation of A. gambiae .

Background Alternative means of malaria control are urgently needed. Evaluating the effectiveness of measures that involve genetic manipulation of vector populations will be facilitated by identifying small, genetically isolated vector populations. The study was designed to use variation in microsatellite markers to look at genetic structure across four Lake Victoria islands and two surrounding mainland populations and for evidence of any restriction to free gene flow. Methods Four Islands (from 20–50 km apart) and two surrounding mainland populations (96 km apart) were studied. Samples of indoor resting adult mosquitoes, collected over two consecutive years, were genotyped at microsatellite loci distributed broadly throughout the genome and analysed for genetic structure, effective migration (Nem) and effective population size (Ne). Results Ne estimates showed island populations to consist of smaller demes compared to the mainland ones. Most populations were significantly differentiated geographically, and from one year to the other. Average geographic pair-wise F ST ranged from 0.014–0.105 and several pairs of populations had Ne m < 3. The loci showed broad heterogeneity at capturing or estimating population differences. Conclusion These island populations are significantly genetically differentiated. Differences reoccurred over the study period, between the two mainland populations and between each other. This appears to be the product of their separation by water, dynamics of small populations and local adaptation. With further characterisation these islands could become possible sites for applying measures evaluating effectiveness of control by genetic manipulation.