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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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Polytene chromosome squashes reveal two overlapping inversions on arm 2R of ten SD chromosomes.The In(2R)Mal arrangement is endemic in African populations and involves two inversions, In(2R)51B6–11;55E3–12 and In(2R)44F3–12;54E3–10.
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pgen-1000463-g004: Polytene chromosome squashes reveal two overlapping inversions on arm 2R of ten SD chromosomes.The In(2R)Mal arrangement is endemic in African populations and involves two inversions, In(2R)51B6–11;55E3–12 and In(2R)44F3–12;54E3–10.

Mentions: The magnitude of a selective sweep is determined by two key parameters: the local rate of recombination and the strength of selection driving the major haplotype to high frequency. The SD chromosomes carrying the major haplotype are unique in both respects. First, recombination is suppressed along much of the major SD haplotype. We cytogenetically characterized the 12 African SD chromosomes by crossing SD/SD or SD/CyO males to virgin cn bw females (which are homozygous for standard-arrangement second chromosomes) and examined polytene chromosome squashes from larval salivary glands. None of the African SD chromosomes possess the In(2R)NS inversion (52A2–52B1;56F9–56F13) found on most non-African SD chromosomes [2]. Indeed, SD-BN19 and SD-MD31 are inversion-free chromosomes (Table 2). The other ten SD chromosomes, however, possess a complex chromosomal arrangement on 2R (Table 2). The cytological order (40–44F/54E–55E/51BC–44F/54E–51BC/55E–60) shows that these SD chromosomes have recruited two overlapping inversions: In(2R)51BC;55E first, followed by In(2R)44F;54E (Figure 4). These inversion breakpoints match a previously identified, but rare, African endemic chromosomal arrangement found in Malawi [50], hereafter called In(2R)Mal. In addition to In(2R)Mal, four SD chromosomes (SD-KN20, SD-KY87, SD-ZK178, SD-ZK216) carry the cosmopolitan In(2L)t inversion (22D3–D6;34A8–A9; Table 2).


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)

Polytene chromosome squashes reveal two overlapping inversions on arm 2R of ten SD chromosomes.The In(2R)Mal arrangement is endemic in African populations and involves two inversions, In(2R)51B6–11;55E3–12 and In(2R)44F3–12;54E3–10.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000463-g004: Polytene chromosome squashes reveal two overlapping inversions on arm 2R of ten SD chromosomes.The In(2R)Mal arrangement is endemic in African populations and involves two inversions, In(2R)51B6–11;55E3–12 and In(2R)44F3–12;54E3–10.
Mentions: The magnitude of a selective sweep is determined by two key parameters: the local rate of recombination and the strength of selection driving the major haplotype to high frequency. The SD chromosomes carrying the major haplotype are unique in both respects. First, recombination is suppressed along much of the major SD haplotype. We cytogenetically characterized the 12 African SD chromosomes by crossing SD/SD or SD/CyO males to virgin cn bw females (which are homozygous for standard-arrangement second chromosomes) and examined polytene chromosome squashes from larval salivary glands. None of the African SD chromosomes possess the In(2R)NS inversion (52A2–52B1;56F9–56F13) found on most non-African SD chromosomes [2]. Indeed, SD-BN19 and SD-MD31 are inversion-free chromosomes (Table 2). The other ten SD chromosomes, however, possess a complex chromosomal arrangement on 2R (Table 2). The cytological order (40–44F/54E–55E/51BC–44F/54E–51BC/55E–60) shows that these SD chromosomes have recruited two overlapping inversions: In(2R)51BC;55E first, followed by In(2R)44F;54E (Figure 4). These inversion breakpoints match a previously identified, but rare, African endemic chromosomal arrangement found in Malawi [50], hereafter called In(2R)Mal. In addition to In(2R)Mal, four SD chromosomes (SD-KN20, SD-KY87, SD-ZK178, SD-ZK216) carry the cosmopolitan In(2L)t inversion (22D3–D6;34A8–A9; Table 2).

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