Academic journal article Genetics

Divergence with Gene Flow in Anopheles Funestus from the Sudan Savanna of Burkina Faso, West Africa

Academic journal article Genetics

Divergence with Gene Flow in Anopheles Funestus from the Sudan Savanna of Burkina Faso, West Africa

Article excerpt

ABSTRACT

Anopheles funestus is a major vector of malaria across Africa. Understanding its complex and nonequilibrium population genetic structure is an important challenge that must be overcome before vector populations can be successfully perturbed for malaria control. Here we examine the role of chromosomal inversions in structuring genetic variation and facilitating divergence in Burkina Faso, West Africa, where two incipient species (chromosomal forms) of A. funestus, defined principally by rearrangements of chromosome 3R, have been hypothesized. Sampling across an ~300-km east-west transect largely contained within the Sudan-Savanna ecoclimatic zone, we analyzed chromosomal inversions, 16 microsatellite loci distributed genomewide, and 834 bp of the mtDNA ND5 gene. Both molecular markers revealed high genetic diversity, nearly all of which was accounted for by within-population differences among individuals, owing to recent population expansion. Across the study area there was no correlation between genetic and geographic distance. Significant genetic differentiation found between chromosomal forms on the basis of microsatellites was not genomewide but could be explained by chromosome 3R alone on the basis of loci inside and near inversions. These data are not compatible with complete reproductive isolation but are consistent with differential introgression and sympatric divergence between the chromosomal forms, facilitated by chromosome 3R inversions.

MALARIA continues to claim over 1 million lives annually and remains the leading pathogenspecific cause of morbidity and mortality in children from tropical Africa (WORLD HEALTH ORGANIZATION 2003). Among its principal African vectors are two highly anthropophilic mosquito species, Anopheles gambiae and A. funestus, whose population genetic structure shows remarkable parallels (LEHMANN et al. 2003; MICHEL et al. 2005b). The tendency of both species to specialize on humans not only maintains a high malaria transmission intensity but also has shaped their population history. This is evidenced by very shallow population structure across Africa and signs of recent population expansion in response to human population growth triggered by the rise and spread of agriculture. The shallow and nonequilibrium population genetic structure of these mosquitoes represents a major challenge to understanding contemporary rates and patterns of gene flow but one that must be overcome if vector populations are to be successfully perturbed for malaria control (COETZEE and FONTENILLE 2004).

Against the backdrop of weak population genetic structure inferred from neutral molecular markers, nonrandom patterns of chromosomal inversion polymorphism in West Africa suggest an ongoing speciation process in both vectors, associated with environmental changes, including irrigation schemes for rice cultivation (DELLA TORRE et al. 2002). Although this phenomenon has been most extensively studied in A. gambiae (COLUZZI et al. 2002), karyotypic analysis of >5,000 A. funestus specimens also has revealed significant and stable departures from Hardy-Weinberg equilibrium due to heterokaryotype deficit and linkage disequilibrium between arrangements on independently assorting chromosome arms (COSTANTINI et al. 1999; GUELBEOGO et al. 2005). Equilibrium was restored under the hypothesis of two sympatric and morphologically indistinguishable but assortatively mating chromosomal forms designated Folonzo and Kiribina. Corresponding ecological and behavioral differences suggest that Kiribina is associated with rice cultivation and is less likely than Folonzo to rest indoors, feed on humans, or carry malaria parasites (COSTANTINI et al. 1999).

Owing to their role in suppressing recombination between alternative arrangements, chromosomal inversions may facilitate divergence in the face of gene flow between incompletely isolated populations (NOOR et al. 2001; RIESEBERG 2001; AYALA and COLUZZI 2005). …

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