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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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Distribution of DNA sequence variation at Sd-RanGAP and eight non-coding regions in Africa.Sequences were sampled from 12 SD and 10 wildtype second chromosomes from African populations of D. melanogaster. The positions of the two overlapping inversions, In(2R)Mal, and the sequenced loci are shown on chromosome 2 (only part of 2L is shown). Sequence variants are arbitrarily coded: gray matches SD-GN09, white does not. The red box highlights the long, mutation-free haplotype that spans from Sd-RanGAP on 2L to locus G (55B) on 2R.
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pgen-1000463-g003: Distribution of DNA sequence variation at Sd-RanGAP and eight non-coding regions in Africa.Sequences were sampled from 12 SD and 10 wildtype second chromosomes from African populations of D. melanogaster. The positions of the two overlapping inversions, In(2R)Mal, and the sequenced loci are shown on chromosome 2 (only part of 2L is shown). Sequence variants are arbitrarily coded: gray matches SD-GN09, white does not. The red box highlights the long, mutation-free haplotype that spans from Sd-RanGAP on 2L to locus G (55B) on 2R.

Mentions: If the major African SD haplotype has indeed risen to high frequency due to positive selection or superior segregation distortion, then the haplotype structure may extend beyond the Sd-RanGAP region. To test this possibility, we sequenced eight noncoding regions across chromosome 2 from all 12 African SD chromosomes and from 10 wildtype chromosomes (Figure 3; Table 3). The amount and distribution of DNA sequence variation among wildtype chromosomes was typical for African D. melanogaster populations [27], with θ ranging from 0.0053 to 0.0137 and Tajima's D ranging from −1.630 to 0.445 (P = 0.045 for locus G, but ≥0.05 for other loci; Table 3). In addition, there is ample evidence for recombination in all but one of the loci (region E has an unusual lack of variability and a small number of haplotypes, though not significantly so; Table 3; Figure 3).


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)

Distribution of DNA sequence variation at Sd-RanGAP and eight non-coding regions in Africa.Sequences were sampled from 12 SD and 10 wildtype second chromosomes from African populations of D. melanogaster. The positions of the two overlapping inversions, In(2R)Mal, and the sequenced loci are shown on chromosome 2 (only part of 2L is shown). Sequence variants are arbitrarily coded: gray matches SD-GN09, white does not. The red box highlights the long, mutation-free haplotype that spans from Sd-RanGAP on 2L to locus G (55B) on 2R.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000463-g003: Distribution of DNA sequence variation at Sd-RanGAP and eight non-coding regions in Africa.Sequences were sampled from 12 SD and 10 wildtype second chromosomes from African populations of D. melanogaster. The positions of the two overlapping inversions, In(2R)Mal, and the sequenced loci are shown on chromosome 2 (only part of 2L is shown). Sequence variants are arbitrarily coded: gray matches SD-GN09, white does not. The red box highlights the long, mutation-free haplotype that spans from Sd-RanGAP on 2L to locus G (55B) on 2R.
Mentions: If the major African SD haplotype has indeed risen to high frequency due to positive selection or superior segregation distortion, then the haplotype structure may extend beyond the Sd-RanGAP region. To test this possibility, we sequenced eight noncoding regions across chromosome 2 from all 12 African SD chromosomes and from 10 wildtype chromosomes (Figure 3; Table 3). The amount and distribution of DNA sequence variation among wildtype chromosomes was typical for African D. melanogaster populations [27], with θ ranging from 0.0053 to 0.0137 and Tajima's D ranging from −1.630 to 0.445 (P = 0.045 for locus G, but ≥0.05 for other loci; Table 3). In addition, there is ample evidence for recombination in all but one of the loci (region E has an unusual lack of variability and a small number of haplotypes, though not significantly so; Table 3; Figure 3).

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