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Large-scale selective sweep among Segregation Distorter chromosomes in African populations of Drosophila melanogaster.

Presgraves DC, Gérard PR, Cherukuri A, Lyttle TW - PLoS Genet. (2009)

Bottom Line: Fifty years of genetic, molecular, and theory work have made SD one of the best-characterized meiotic drive systems, but surprisingly the details of its evolutionary origins and population dynamics remain unclear.In this report, we show, first, that SD chromosomes occur in populations in sub-Saharan Africa, the ancestral range of D. melanogaster, at a similarly low frequency (approximately 2%), providing evidence for the robustness of its equilibrium frequency but raising doubts about the Mediterranean-origins hypothesis.Thus, despite a seemingly stable equilibrium frequency, SD chromosomes continue to evolve, to compete with one another, or evade suppressors in the genome.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Rochester, Rochester, NY, USA. dvnp@mail.rochester.edu

ABSTRACT
Segregation Distorter (SD) is a selfish, coadapted gene complex on chromosome 2 of Drosophila melanogaster that strongly distorts Mendelian transmission; heterozygous SD/SD(+) males sire almost exclusively SD-bearing progeny. Fifty years of genetic, molecular, and theory work have made SD one of the best-characterized meiotic drive systems, but surprisingly the details of its evolutionary origins and population dynamics remain unclear. Earlier analyses suggested that the SD system arose recently in the Mediterranean basin and then spread to a low, stable equilibrium frequency (1-5%) in most natural populations worldwide. In this report, we show, first, that SD chromosomes occur in populations in sub-Saharan Africa, the ancestral range of D. melanogaster, at a similarly low frequency (approximately 2%), providing evidence for the robustness of its equilibrium frequency but raising doubts about the Mediterranean-origins hypothesis. Second, our genetic analyses reveal two kinds of SD chromosomes in Africa: inversion-free SD chromosomes with little or no transmission advantage; and an African-endemic inversion-bearing SD chromosome, SD-Mal, with a perfect transmission advantage. Third, our population genetic analyses show that SD-Mal chromosomes swept across the African continent very recently, causing linkage disequilibrium and an absence of variability over 39% of the length of the second chromosome. Thus, despite a seemingly stable equilibrium frequency, SD chromosomes continue to evolve, to compete with one another, or evade suppressors in the genome.

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Variation in 12 Sd-RanGAP and 10 RanGAP sequences from African populations of D. melanogaster.Sd-RanGAP and RanGAP show four nucleotide differences and one indel difference. (N = nonsynonymous; S = synonymous; all other changes are noncoding.)
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pgen-1000463-g002: Variation in 12 Sd-RanGAP and 10 RanGAP sequences from African populations of D. melanogaster.Sd-RanGAP and RanGAP show four nucleotide differences and one indel difference. (N = nonsynonymous; S = synonymous; all other changes are noncoding.)

Mentions: After genetically extracting the SD chromosomes, we sequenced the ∼4.5-kb Sd-RanGAP sequence from all 12 as well as the homologous region of the parent gene, RanGAP, from 10 wildtype (non-SD) chromosomes sampled from Zimbabwe (see Methods). RanGAP and Sd-RanGAP show typical levels of silent divergence per site from the RanGAP homolog in the outgroup species, D. simulans, with Ksil = 0.0471 and 0.0478, respectively. Silent divergence between the duplicate genes, RanGAP and Sd-RanGAP, within D. melanogaster is more than an order of magnitude lower, Ksil = 0.0027 (see also ref. [37]). These findings confirm that Sd-RanGAP arose in D. melanogaster well after the split from D. simulans [29]. Using D. simulans RanGAP as an outgroup sequence, we polarized the substitutions between D. melanogaster RanGAP and Sd-RanGAP. Of five fixed differences between RanGAP and Sd-RanGAP, all were fixed in the common ancestor of the Sd-RanGAP sequences: three noncoding changes, one fixed 6-bp deletion, and a single nonsynonymous change (Figure 2). The first intron of RanGAP contains the gene, Hs2st, raising the possibility that some “silent” changes in one gene are not silent in the other. However, of the five fixed substitutions occurring in Sd-RanGAP, only four affect Hs2st: two are noncoding and two are synonymous.


Large-scale selective sweep among Segregation Distorter chromosomes in African populations of Drosophila melanogaster.

Presgraves DC, Gérard PR, Cherukuri A, Lyttle TW - PLoS Genet. (2009)

Variation in 12 Sd-RanGAP and 10 RanGAP sequences from African populations of D. melanogaster.Sd-RanGAP and RanGAP show four nucleotide differences and one indel difference. (N = nonsynonymous; S = synonymous; all other changes are noncoding.)
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2668186&req=5

pgen-1000463-g002: Variation in 12 Sd-RanGAP and 10 RanGAP sequences from African populations of D. melanogaster.Sd-RanGAP and RanGAP show four nucleotide differences and one indel difference. (N = nonsynonymous; S = synonymous; all other changes are noncoding.)
Mentions: After genetically extracting the SD chromosomes, we sequenced the ∼4.5-kb Sd-RanGAP sequence from all 12 as well as the homologous region of the parent gene, RanGAP, from 10 wildtype (non-SD) chromosomes sampled from Zimbabwe (see Methods). RanGAP and Sd-RanGAP show typical levels of silent divergence per site from the RanGAP homolog in the outgroup species, D. simulans, with Ksil = 0.0471 and 0.0478, respectively. Silent divergence between the duplicate genes, RanGAP and Sd-RanGAP, within D. melanogaster is more than an order of magnitude lower, Ksil = 0.0027 (see also ref. [37]). These findings confirm that Sd-RanGAP arose in D. melanogaster well after the split from D. simulans [29]. Using D. simulans RanGAP as an outgroup sequence, we polarized the substitutions between D. melanogaster RanGAP and Sd-RanGAP. Of five fixed differences between RanGAP and Sd-RanGAP, all were fixed in the common ancestor of the Sd-RanGAP sequences: three noncoding changes, one fixed 6-bp deletion, and a single nonsynonymous change (Figure 2). The first intron of RanGAP contains the gene, Hs2st, raising the possibility that some “silent” changes in one gene are not silent in the other. However, of the five fixed substitutions occurring in Sd-RanGAP, only four affect Hs2st: two are noncoding and two are synonymous.

Bottom Line: Fifty years of genetic, molecular, and theory work have made SD one of the best-characterized meiotic drive systems, but surprisingly the details of its evolutionary origins and population dynamics remain unclear.In this report, we show, first, that SD chromosomes occur in populations in sub-Saharan Africa, the ancestral range of D. melanogaster, at a similarly low frequency (approximately 2%), providing evidence for the robustness of its equilibrium frequency but raising doubts about the Mediterranean-origins hypothesis.Thus, despite a seemingly stable equilibrium frequency, SD chromosomes continue to evolve, to compete with one another, or evade suppressors in the genome.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Rochester, Rochester, NY, USA. dvnp@mail.rochester.edu

ABSTRACT
Segregation Distorter (SD) is a selfish, coadapted gene complex on chromosome 2 of Drosophila melanogaster that strongly distorts Mendelian transmission; heterozygous SD/SD(+) males sire almost exclusively SD-bearing progeny. Fifty years of genetic, molecular, and theory work have made SD one of the best-characterized meiotic drive systems, but surprisingly the details of its evolutionary origins and population dynamics remain unclear. Earlier analyses suggested that the SD system arose recently in the Mediterranean basin and then spread to a low, stable equilibrium frequency (1-5%) in most natural populations worldwide. In this report, we show, first, that SD chromosomes occur in populations in sub-Saharan Africa, the ancestral range of D. melanogaster, at a similarly low frequency (approximately 2%), providing evidence for the robustness of its equilibrium frequency but raising doubts about the Mediterranean-origins hypothesis. Second, our genetic analyses reveal two kinds of SD chromosomes in Africa: inversion-free SD chromosomes with little or no transmission advantage; and an African-endemic inversion-bearing SD chromosome, SD-Mal, with a perfect transmission advantage. Third, our population genetic analyses show that SD-Mal chromosomes swept across the African continent very recently, causing linkage disequilibrium and an absence of variability over 39% of the length of the second chromosome. Thus, despite a seemingly stable equilibrium frequency, SD chromosomes continue to evolve, to compete with one another, or evade suppressors in the genome.

Show MeSH
Related in: MedlinePlus