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Remarkable diversity of intron-1 of the para voltage-gated sodium channel gene in an Anopheles gambiae/Anopheles coluzzii hybrid zone.

Santolamazza F, Caputo B, Nwakanma DC, Fanello C, Petrarca V, Conway DJ, Weetman D, Pinto J, Mancini E, della Torre A - Malar. J. (2015)

Bottom Line: Far-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.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.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Sanità Pubblica e Malattie Infettive, Istituto Pasteur-Fondazione Cenci-Bolognetti, Università "Sapienza", Piazzale Aldo Moro 5, Rome, 00185, Italy. emiliano.mancini@uniroma1.it.

ABSTRACT

Background: 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. 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.

Methods: A 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.

Results: Far-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.

Conclusions: The 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.

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Parsimony-based networks of genealogical relationships among VGSC Intron-1 haplotypes in theAnopheles gambiaecomplex. a) Network built with original data collected from all studied species of the A. gambiae complex, with the exception of Anopheles melas and Anopheles merus, whose haplotypes exceeded the 95% threshold of TCS connection limit. Haplotypes are represented by pies whose sizes are proportional to frequencies in the sample and coloured as follows: blue = Anopheles arabiensis (AR), red = Anopheles quadriannulatus (QD), violet = Anopheles coluzzii, green = Anopheles gambiae (haplotypes are named and numbered according to Gentile et al. [23]), yellow = private haplotypes from either Guinea Bissau (GU), The Gambia (GA), or from both Countries (GUGA); sequential codes are used to name A. coluzzii (i.e. M7, M8) and A. gambiae (S7-S10) novel haplotypes not exclusive to The Gambia and Guinea Bissau; M1, M3, M5, S1 and S7, which are not completely segregated between the two species in the Far-West and/or Rwanda, are shaded. Below: VGSC Int-1 network for M (A. coluzzii) and S (A. gambiae) molecular forms as in Gentile et al. [23]; b) and c) networks only including A. coluzzii, A. gambiae and hybrids haplotypes from The Gambia and Guinea Bissau, respectively. White squares report numbers of alleles for A. coluzzii (M), A. gambiae (S) and hybrids (MS) (identified based on SINE-PCR [26]) included in each haplotype.
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Fig2: Parsimony-based networks of genealogical relationships among VGSC Intron-1 haplotypes in theAnopheles gambiaecomplex. a) Network built with original data collected from all studied species of the A. gambiae complex, with the exception of Anopheles melas and Anopheles merus, whose haplotypes exceeded the 95% threshold of TCS connection limit. Haplotypes are represented by pies whose sizes are proportional to frequencies in the sample and coloured as follows: blue = Anopheles arabiensis (AR), red = Anopheles quadriannulatus (QD), violet = Anopheles coluzzii, green = Anopheles gambiae (haplotypes are named and numbered according to Gentile et al. [23]), yellow = private haplotypes from either Guinea Bissau (GU), The Gambia (GA), or from both Countries (GUGA); sequential codes are used to name A. coluzzii (i.e. M7, M8) and A. gambiae (S7-S10) novel haplotypes not exclusive to The Gambia and Guinea Bissau; M1, M3, M5, S1 and S7, which are not completely segregated between the two species in the Far-West and/or Rwanda, are shaded. Below: VGSC Int-1 network for M (A. coluzzii) and S (A. gambiae) molecular forms as in Gentile et al. [23]; b) and c) networks only including A. coluzzii, A. gambiae and hybrids haplotypes from The Gambia and Guinea Bissau, respectively. White squares report numbers of alleles for A. coluzzii (M), A. gambiae (S) and hybrids (MS) (identified based on SINE-PCR [26]) included in each haplotype.

Mentions: Variable sites among haplotypes, and their relationships among different members of the A. gambiae complex, are shown in Figure 1 and in Figure 2, respectively. All species are well-separated from each other and from A. coluzzii and A. gambiae (except for one A. arabiensis individual from Senegal sharing the S1-haplotype with A. gambiae). Interestingly, A. gambiae carries a C to T mutation at site 702 (hereafter Int-1702, in red in Figure 1) separating it from all other species. This mutation was already shown by Gentile et al. [23] to separate “S-molecular form-S1 (Int-1T)” from “M-form-M1 (Int-1C)” haplotypes and closely-related locale-specific variants. In the Gambian and Guinean samples, however, A. coluzzii-specific Int-1C haplotypes are also found in A. gambiae, but no A. gambiae-specific Int-1T haplotypes are found in A. coluzzii (Figures 2b and 2c; Additional file 2: Table S2). This result does not change if the species are identified using the IGS marker rather than by SINE-PCR, as presented so far.Figure 1


Remarkable diversity of intron-1 of the para voltage-gated sodium channel gene in an Anopheles gambiae/Anopheles coluzzii hybrid zone.

Santolamazza F, Caputo B, Nwakanma DC, Fanello C, Petrarca V, Conway DJ, Weetman D, Pinto J, Mancini E, della Torre A - Malar. J. (2015)

Parsimony-based networks of genealogical relationships among VGSC Intron-1 haplotypes in theAnopheles gambiaecomplex. a) Network built with original data collected from all studied species of the A. gambiae complex, with the exception of Anopheles melas and Anopheles merus, whose haplotypes exceeded the 95% threshold of TCS connection limit. Haplotypes are represented by pies whose sizes are proportional to frequencies in the sample and coloured as follows: blue = Anopheles arabiensis (AR), red = Anopheles quadriannulatus (QD), violet = Anopheles coluzzii, green = Anopheles gambiae (haplotypes are named and numbered according to Gentile et al. [23]), yellow = private haplotypes from either Guinea Bissau (GU), The Gambia (GA), or from both Countries (GUGA); sequential codes are used to name A. coluzzii (i.e. M7, M8) and A. gambiae (S7-S10) novel haplotypes not exclusive to The Gambia and Guinea Bissau; M1, M3, M5, S1 and S7, which are not completely segregated between the two species in the Far-West and/or Rwanda, are shaded. Below: VGSC Int-1 network for M (A. coluzzii) and S (A. gambiae) molecular forms as in Gentile et al. [23]; b) and c) networks only including A. coluzzii, A. gambiae and hybrids haplotypes from The Gambia and Guinea Bissau, respectively. White squares report numbers of alleles for A. coluzzii (M), A. gambiae (S) and hybrids (MS) (identified based on SINE-PCR [26]) included in each haplotype.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4308935&req=5

Fig2: Parsimony-based networks of genealogical relationships among VGSC Intron-1 haplotypes in theAnopheles gambiaecomplex. a) Network built with original data collected from all studied species of the A. gambiae complex, with the exception of Anopheles melas and Anopheles merus, whose haplotypes exceeded the 95% threshold of TCS connection limit. Haplotypes are represented by pies whose sizes are proportional to frequencies in the sample and coloured as follows: blue = Anopheles arabiensis (AR), red = Anopheles quadriannulatus (QD), violet = Anopheles coluzzii, green = Anopheles gambiae (haplotypes are named and numbered according to Gentile et al. [23]), yellow = private haplotypes from either Guinea Bissau (GU), The Gambia (GA), or from both Countries (GUGA); sequential codes are used to name A. coluzzii (i.e. M7, M8) and A. gambiae (S7-S10) novel haplotypes not exclusive to The Gambia and Guinea Bissau; M1, M3, M5, S1 and S7, which are not completely segregated between the two species in the Far-West and/or Rwanda, are shaded. Below: VGSC Int-1 network for M (A. coluzzii) and S (A. gambiae) molecular forms as in Gentile et al. [23]; b) and c) networks only including A. coluzzii, A. gambiae and hybrids haplotypes from The Gambia and Guinea Bissau, respectively. White squares report numbers of alleles for A. coluzzii (M), A. gambiae (S) and hybrids (MS) (identified based on SINE-PCR [26]) included in each haplotype.
Mentions: Variable sites among haplotypes, and their relationships among different members of the A. gambiae complex, are shown in Figure 1 and in Figure 2, respectively. All species are well-separated from each other and from A. coluzzii and A. gambiae (except for one A. arabiensis individual from Senegal sharing the S1-haplotype with A. gambiae). Interestingly, A. gambiae carries a C to T mutation at site 702 (hereafter Int-1702, in red in Figure 1) separating it from all other species. This mutation was already shown by Gentile et al. [23] to separate “S-molecular form-S1 (Int-1T)” from “M-form-M1 (Int-1C)” haplotypes and closely-related locale-specific variants. In the Gambian and Guinean samples, however, A. coluzzii-specific Int-1C haplotypes are also found in A. gambiae, but no A. gambiae-specific Int-1T haplotypes are found in A. coluzzii (Figures 2b and 2c; Additional file 2: Table S2). This result does not change if the species are identified using the IGS marker rather than by SINE-PCR, as presented so far.Figure 1

Bottom Line: Far-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.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.

View Article: PubMed Central - PubMed

Affiliation: Dipartimento di Sanità Pubblica e Malattie Infettive, Istituto Pasteur-Fondazione Cenci-Bolognetti, Università "Sapienza", Piazzale Aldo Moro 5, Rome, 00185, Italy. emiliano.mancini@uniroma1.it.

ABSTRACT

Background: 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. 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.

Methods: A 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.

Results: Far-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.

Conclusions: The 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.

Show MeSH
Related in: MedlinePlus