Divergence With Gene Flow in Anopheles funestus From the Sudan Savanna of Burkina Faso, West Africa

Center for Tropical Disease Research and Training, Department of Biological Sciences, University of Notre Dame, Indiana 46556, USA.
Genetics (Impact Factor: 5.96). 08/2006; 173(3):1389-95. DOI: 10.1534/genetics.106.059667
Source: PubMed


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 approximately 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.

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    • "Secondly, neutral divergence within and around inversions should be increased relative to colinear parts of the genomes as a consequence of reduced gene flow. A signature of elevated divergence around inversion breakpoints has been found not only in the sister species D. pseudoobscura and D. persimilis, a classic model of speciation (Noor et al. 2007; Kulathinal et al. 2009), but also in mosquitoes (Besansky et al. 2003; Michel et al. 2006), sunflowers (Rieseberg et al. 1999), shrews (Yannic et al. 2009), and Heliconius butterflies (Joron et al. 2011). "
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    ABSTRACT: Models of speciation-with-gene-flow have shown that the reduction in recombination between alternative chromosome arrangements can facilitate the fixation of locally adaptive genes in the face of gene flow and contribute to speciation. However, it has proven frustratingly difficult to show empirically that inversions have reduced gene flow and arose during or shortly after the onset of species divergence rather than represent ancestral polymorphisms. Here we present an analysis of whole genome data from a pair of cactophilic fruit flies, Drosophila mojavensis and D. arizonae, which are reproductively isolated in the wild and differ by several large inversions on three chromosomes. We found an increase in divergence at rearranged compared to colinear chromosomes. Using the density of divergent sites in short sequence blocks we fit a series of explicit models of species divergence in which gene flow is restricted to an initial period after divergence and may differ between colinear and rearranged parts of the genome. These analyses show that D. mojavensis and D. arizonae have experienced post-divergence gene flow which ceased around 270 KY ago and was significantly reduced in chromosomes with fixed inversions. Moreover, we show that these inversions most likely originated around the time of of species divergence which is compatible with theoretical models of speciation with gene flow. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Full-text · Article · Mar 2015 · Evolution
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    • "Although direct evidence is lacking, the Folonzo form is associated with natural larval habitats such as marshes, while Kiribina is associated with larval habitats created by the practice of agriculture, notably rice fields. Molecular genetic studies using mtDNA and microsatellite markers revealed very slight but significant divergence between sympatric samples of Folonzo and Kiribina across Burkina Faso, although nuclear divergence was not genome-wide and could be explained by loci on chromosome 3R inside and outside inversions [23,24]. These data are suggestive of an incipient process of ecological divergence and lineage splitting, similar to, but less advanced than, that responsible for the divergence of An. coluzzii and An. "
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    ABSTRACT: In Burkina Faso, two chromosomal forms of the malaria vector Anopheles funestus, Folonzo and Kiribina, are distinguished by contrasting frequencies of shared polymorphic chromosomal inversions. Sympatric and synchronous populations of Folonzo and Kiribina mate assortatively, as indicated by a significant deficit of heterokaryotypes, and genetic associations among inversions on independently segregating chromosome arms. The present study aimed to assess, by intensive longitudinal sampling, whether sympatric Folonzo and Kiribina populations are characterized by behavioural differences in key malaria vectorial parameters. The study was conducted in two adjacent villages near Ouagadougou, in the dry savanna of central Burkina Faso. Mosquito adult resting behaviour of both forms was compared based on parallel indoor/outdoor collections across six breeding seasons; 8,235 fully karyotyped samples of half-gravid females were analysed in total. Additionally, indoor/outdoor human biting behaviour, host selection, and Plasmodium falciparum sporozoite rate was assessed and compared between chromosomal forms. The Kiribina form was numerically predominant in the area. However, the Folonzo form was significantly over-represented in indoor resting collections and showed stronger post-prandial endophily, while Kiribina predominated outdoors. Neither form was statistically distinguishable in human biting behaviour, and both were more likely to seek human blood meals indoors than outside. The human blood index and sporozoite rate were comparably high in both chromosomal forms in indoor collections (>89% and >8%, respectively). Both Kiribina and Folonzo chromosomal forms are formidable malaria vectors in Burkina Faso. However, the significantly greater tendency for the Kiribina form to rest outdoors despite its pronounced anthropophily suggests that uniform exposure of the overall An. funestus population to indoor-based vector control tools cannot be expected; Kiribina is more likely to evade indoor interventions and escape unharmed outdoors, reducing the efficacy of malaria control. Accordingly, more efficient methods to detect Kiribina and Folonzo, and a more complete understanding of their distribution and behaviour in Africa are advocated.
    Full-text · Article · Feb 2014 · Malaria Journal
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    • "In the study by Michel et al.[15], samples from East Africa had significantly lower average heterozygosity (0.455) and allelic richness (3.9) across all microsatellite loci, and lower mean mtDNA haplotype diversity (0.773) compared with the rest of Africa (0.606, 6.0 and 0.924 respectively). Other studies [16,35] have also reported two different subdivisions within An. funestus from the analysis of ND5. However, these proposed subdivisions were not correlated with the clades of Michel et al.[15]. "
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    ABSTRACT: Background Anopheles funestus s.s., one of the major malaria vectors in sub-Saharan Africa, belongs to a group of eleven African species that are morphologically similar at the adult stage, most of which do not transmit malaria. The population structure of An. funestus based on mitochondrial DNA data led to the description of two cryptic subdivisions, clade I widespread throughout Africa and clade II known only from Mozambique and Madagascar. In this study, we investigated five common members of the Anopheles funestus group in southern Africa in order to determine relationships within and between species. Methods A total of 155 specimens of An. funestus, An. parensis, An. vaneedeni, An. funestus-like and An. rivulorum from South Africa, Mozambique and Malawi were used for the study. The population genetic structure was assessed within and between populations using mitochondrial DNA. Results The phylogenetic trees revealed three main lineages: 1) An. rivulorum; 2) An. funestus-like clade I and An. parensis clade II; and 3) An. funestus clades I and II, An. funestus-like clade II, An. parensis clade I and An. vaneedeni clades I and II. Within An. funestus, 32 specimens from Mozambique consisted of 40.6% clade I and 59.4% clade II while all 21 individuals from Malawi were clade I. In the analysis of mitochondrial DNA sequences, there were 37 polymorphic sites and 9 fixed different nucleotides for ND5 and 21 polymorphic sites and 6 fixed different nucleotides for COI between the two An. funestus clades. The results for COI supported the ND5 analysis. Conclusion This is the first report comparing An. funestus group species including An. funestus clades I and II and the new species An. funestus-like. Anopheles funestus clade I is separated from the rest of the members of the An. funestus subgroup and An. funestus-like is distinctly distributed from the other species in this study. However, there were two clades for An. funestus-like, An. parensis and An. vaneedeni. Further investigations are needed to determine what these results mean in terms of the specific status of the clades within each taxon and whether this has any epidemiological implications for malaria transmission.
    Full-text · Article · Dec 2012 · Parasites & Vectors
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