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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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VGSC intron-1 (Int-1) polymorphism within theAnopheles gambiaecomplex. Nucleotide alignments show variable positions among Int-1 haplotypes. Positions are numbered as in Gentile et al. [23] and site 702 (i.e. Int-1702) is highlighted in red. Haplotypes are named as follows: M1-M6 and S1-S6 = Anopheles coluzzii and A. gambiae haplotypes as in Gentile et al. [23]; M7-M8 and S7-S10 are novel A. coluzzii and A. gambiae haplotypes not exclusive to The Gambia and Guinea Bissau; GU, GA or GUGA = A. coluzzii and A. gambiae private haplotypes from either Guinea Bissau, The Gambia, or both Countries, respectively. AR1-AR4 = Anopheles arabiensis haplotypes; QD1-QD2 = Anopheles quadriannulatus haplotypes; MR1-MR3 = Anopheles merus haplotypes; ML1-ML2 = Anopheles melas haplotypes.
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Fig1: VGSC intron-1 (Int-1) polymorphism within theAnopheles gambiaecomplex. Nucleotide alignments show variable positions among Int-1 haplotypes. Positions are numbered as in Gentile et al. [23] and site 702 (i.e. Int-1702) is highlighted in red. Haplotypes are named as follows: M1-M6 and S1-S6 = Anopheles coluzzii and A. gambiae haplotypes as in Gentile et al. [23]; M7-M8 and S7-S10 are novel A. coluzzii and A. gambiae haplotypes not exclusive to The Gambia and Guinea Bissau; GU, GA or GUGA = A. coluzzii and A. gambiae private haplotypes from either Guinea Bissau, The Gambia, or both Countries, respectively. AR1-AR4 = Anopheles arabiensis haplotypes; QD1-QD2 = Anopheles quadriannulatus haplotypes; MR1-MR3 = Anopheles merus haplotypes; ML1-ML2 = Anopheles melas haplotypes.

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)

VGSC intron-1 (Int-1) polymorphism within theAnopheles gambiaecomplex. Nucleotide alignments show variable positions among Int-1 haplotypes. Positions are numbered as in Gentile et al. [23] and site 702 (i.e. Int-1702) is highlighted in red. Haplotypes are named as follows: M1-M6 and S1-S6 = Anopheles coluzzii and A. gambiae haplotypes as in Gentile et al. [23]; M7-M8 and S7-S10 are novel A. coluzzii and A. gambiae haplotypes not exclusive to The Gambia and Guinea Bissau; GU, GA or GUGA = A. coluzzii and A. gambiae private haplotypes from either Guinea Bissau, The Gambia, or both Countries, respectively. AR1-AR4 = Anopheles arabiensis haplotypes; QD1-QD2 = Anopheles quadriannulatus haplotypes; MR1-MR3 = Anopheles merus haplotypes; ML1-ML2 = Anopheles melas haplotypes.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: VGSC intron-1 (Int-1) polymorphism within theAnopheles gambiaecomplex. Nucleotide alignments show variable positions among Int-1 haplotypes. Positions are numbered as in Gentile et al. [23] and site 702 (i.e. Int-1702) is highlighted in red. Haplotypes are named as follows: M1-M6 and S1-S6 = Anopheles coluzzii and A. gambiae haplotypes as in Gentile et al. [23]; M7-M8 and S7-S10 are novel A. coluzzii and A. gambiae haplotypes not exclusive to The Gambia and Guinea Bissau; GU, GA or GUGA = A. coluzzii and A. gambiae private haplotypes from either Guinea Bissau, The Gambia, or both Countries, respectively. AR1-AR4 = Anopheles arabiensis haplotypes; QD1-QD2 = Anopheles quadriannulatus haplotypes; MR1-MR3 = Anopheles merus haplotypes; ML1-ML2 = Anopheles melas haplotypes.
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