Abstract
BackgroundGenomic differentiation between Anopheles gambiae and Anopheles coluzzii - the major malaria vectors in sub-Saharan Africa - is localized into large “islands” toward the centromeres of chromosome-X and the two autosomes. Linkage disequilibrium between these genomic islands was first detected between species-specific polymorphisms within ribosomal DNA genes (IGS-rDNA) on the X-chromosome and a single variant at position 702 of intron 1 (Int-1702) of the para Voltage-Gated Sodium Channel (VGSC) gene on chromosome arm 2 L. Intron-1 sequence data from West and Central Africa revealed two clearly distinct and species-specific haplogroups, each characterized by very low polymorphism, which has been attributed to a selective sweep. The aim of this study was to analyse Int-1 sequence diversity in A. gambiae and A. coluzzii populations from the Far-West of their range, in order to assess whether this selective-sweep signature could persist in a zone of high interspecific hybridization.MethodsA 531 bp region of VGSC Int-1 was sequenced in 21 A. coluzzii, 31 A. gambiae, and 12 hybrids from The Gambia and Guinea Bissau, located within the Far-West geographical region, and in 53 A. gambiae s.l. samples from the rest of the range.ResultsFar-West samples exhibit dramatic Int-1 polymorphism, far higher within each country than observed throughout the rest of the species range. Moreover, patterning of haplotypes within A. coluzzii confirms previous evidence of a macro-geographic subdivision into a West and a Central African genetic cluster, and reveals a possible genetic distinction of A. coluzzii populations from the Far-West.ConclusionsThe results suggest a relaxation of selective pressures acting across the VGSC gene region in the hybrid zone. Genetic differentiation in the Far-West could be attributable to a founder effect within A. coluzzii, with subsequent extensive gene flow with secondarily-colonizing A. gambiae, potentially yielding a novel insight on the dynamic processes impacting genetic divergence of these key malaria vectors.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-014-0522-1) contains supplementary material, which is available to authorized users.
Highlights
Genomic differentiation between Anopheles gambiae and Anopheles coluzzii - the major malaria vectors in sub-Saharan Africa - is localized into large “islands” toward the centromeres of chromosome-X and the two autosomes
The aim of this study was to investigate sequence diversity of the Int-1 region of the Voltage-Gated Sodium Channel (VGSC) in A. gambiae and A. coluzzii populations from the Far-West to assess whether the selective-sweep observed in the rest of the species range is maintained in the face of high interspecific gene flow
Anopheles gambiae sensu lato sample identification and kdr genotyping Anopheles gambiae s.l. specimens were identified as A. arabiensis, A. quadriannulatus, A. melas or A. merus using the method of Scott et al [24], and as A. coluzzii or A. gambiae s.s. by using both PCR-RFLP of the intergenic spacer (IGS) rDNA region [25] and the SINEPCR [26] methods
Summary
Genomic differentiation between Anopheles gambiae and Anopheles coluzzii - the major malaria vectors in sub-Saharan Africa - is localized into large “islands” toward the centromeres of chromosome-X and the two autosomes. These studies have revealed the existence of morphologically indistinguishable, but chromosomally/ genetically distinct species with very different roles as malaria vectors (A. gambiae sensu stricto, Anopheles arabiensis, Anopheles quadriannulatus, Anopheles amharicus, Anopheles melas, Anopheles merus, Anopheles bwambae) [5,6] In addition to these sibling species, which are isolated by both pre-and post-mating mechanisms, more recent studies have highlighted a further subdivision within the nominal species A. gambiae s.s., the most synanthropic and efficient malaria vector of the complex [7,8]. The two species are isolated only by (partially understood) pre-mating mechanisms and show limited genomic differentiation, which is localized most prominently in low-recombination pericentromeric regions of chromosome-X and of the two autosomes [10,11,12,13] These regions have been postulated to represent ‘genomic islands of speciation’, expanding in size by selection across linked loci connected to reproductive isolation, as predicted by ecological speciation with gene flow models [1,2]. In this putative secondary contact zone between the two species, high frequencies of hybrids are found and pronounced inter-specific differentiation is maintained only on the chromosome-X centromere [17,18,19,20,21]
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