Limits...
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.

Show MeSH

Related in: MedlinePlus

A molecular screen for SD chromosomes.(A) Part of chromosome arm 2L and all of 2R are shown with the approximate cytological locations of SD loci. The centromere occurs at the transition between cytological divisions 40 and 41. (B) A three-primer assay was used to screen isofemale lines for the presence of the Sd-RanGAP duplication. There are two potential primer pairs: the F-R1 primer pair, a positive control, amplifies a 463-bp product from RanGAP; the F-R2 primer pair amplifies a 353-bp product from the proximal breakpoint of the Sd-RanGAP duplicate gene, if present. Note that the R2 primer anneals to the 5′ region of both RanGAP and Sd-RanGAP; for Sd-RanGAP, however, there is no corresponding forward primer. An example gel is shown: flies carrying Sd-RanGAP yield two amplicons (from Sd-RanGAP and RanGAP), whereas those lacking Sd-RanGAP produce only one (from RanGAP only).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2668186&req=5

pgen-1000463-g001: A molecular screen for SD chromosomes.(A) Part of chromosome arm 2L and all of 2R are shown with the approximate cytological locations of SD loci. The centromere occurs at the transition between cytological divisions 40 and 41. (B) A three-primer assay was used to screen isofemale lines for the presence of the Sd-RanGAP duplication. There are two potential primer pairs: the F-R1 primer pair, a positive control, amplifies a 463-bp product from RanGAP; the F-R2 primer pair amplifies a 353-bp product from the proximal breakpoint of the Sd-RanGAP duplicate gene, if present. Note that the R2 primer anneals to the 5′ region of both RanGAP and Sd-RanGAP; for Sd-RanGAP, however, there is no corresponding forward primer. An example gel is shown: flies carrying Sd-RanGAP yield two amplicons (from Sd-RanGAP and RanGAP), whereas those lacking Sd-RanGAP produce only one (from RanGAP only).

Mentions: The Segregation Distorter (SD) system of the fruitfly, Drosophila melanogaster, is a naturally occurring meiotic drive complex—instead of fair Mendelian transmission, heterozygous SD/SD+ males transmit SD chromosomes to most, if not all, progeny [1]–[8]. Full strength distortion is caused by three interacting loci clustered around the centromere of chromosome 2 (an autosome): the trans-acting Segregation distorter (Sd) locus; an upward modifier, Enhancer of SD (E(SD)); and a cis-acting distortion-insensitive allele at the target locus, Responder (Rspi). (By convention, Sd refers to the locus whereas SD refers to chromosomes assumed to carry the full complex of loci.) SD chromosomes are thus Sd E(SD) Rspi, whereas SD+ chromosomes, which lack the distorting Sd locus and usually carry sensitive alleles of Rsp, are Sd+ E(SD)+ Rsps (Figure 1A). During spermiogenesis in heterozygous SD/SD+ males, the sperm-specific histone transition required for proper chromatin packaging is disrupted in Rsps-bearing SD+ sperm, leaving functional Rspi-bearing SD sperm to monopolize fertilization [9]–[12]. For decades, the SD system has been a model in evolutionary genetics, not only for being selfish, propagating at the expense of its bearers, but as a coadapted gene complex whose fitness is determined by multiple epistatic interactors [5]–[7], [13]–[15].


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)

A molecular screen for SD chromosomes.(A) Part of chromosome arm 2L and all of 2R are shown with the approximate cytological locations of SD loci. The centromere occurs at the transition between cytological divisions 40 and 41. (B) A three-primer assay was used to screen isofemale lines for the presence of the Sd-RanGAP duplication. There are two potential primer pairs: the F-R1 primer pair, a positive control, amplifies a 463-bp product from RanGAP; the F-R2 primer pair amplifies a 353-bp product from the proximal breakpoint of the Sd-RanGAP duplicate gene, if present. Note that the R2 primer anneals to the 5′ region of both RanGAP and Sd-RanGAP; for Sd-RanGAP, however, there is no corresponding forward primer. An example gel is shown: flies carrying Sd-RanGAP yield two amplicons (from Sd-RanGAP and RanGAP), whereas those lacking Sd-RanGAP produce only one (from RanGAP only).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000463-g001: A molecular screen for SD chromosomes.(A) Part of chromosome arm 2L and all of 2R are shown with the approximate cytological locations of SD loci. The centromere occurs at the transition between cytological divisions 40 and 41. (B) A three-primer assay was used to screen isofemale lines for the presence of the Sd-RanGAP duplication. There are two potential primer pairs: the F-R1 primer pair, a positive control, amplifies a 463-bp product from RanGAP; the F-R2 primer pair amplifies a 353-bp product from the proximal breakpoint of the Sd-RanGAP duplicate gene, if present. Note that the R2 primer anneals to the 5′ region of both RanGAP and Sd-RanGAP; for Sd-RanGAP, however, there is no corresponding forward primer. An example gel is shown: flies carrying Sd-RanGAP yield two amplicons (from Sd-RanGAP and RanGAP), whereas those lacking Sd-RanGAP produce only one (from RanGAP only).
Mentions: The Segregation Distorter (SD) system of the fruitfly, Drosophila melanogaster, is a naturally occurring meiotic drive complex—instead of fair Mendelian transmission, heterozygous SD/SD+ males transmit SD chromosomes to most, if not all, progeny [1]–[8]. Full strength distortion is caused by three interacting loci clustered around the centromere of chromosome 2 (an autosome): the trans-acting Segregation distorter (Sd) locus; an upward modifier, Enhancer of SD (E(SD)); and a cis-acting distortion-insensitive allele at the target locus, Responder (Rspi). (By convention, Sd refers to the locus whereas SD refers to chromosomes assumed to carry the full complex of loci.) SD chromosomes are thus Sd E(SD) Rspi, whereas SD+ chromosomes, which lack the distorting Sd locus and usually carry sensitive alleles of Rsp, are Sd+ E(SD)+ Rsps (Figure 1A). During spermiogenesis in heterozygous SD/SD+ males, the sperm-specific histone transition required for proper chromatin packaging is disrupted in Rsps-bearing SD+ sperm, leaving functional Rspi-bearing SD sperm to monopolize fertilization [9]–[12]. For decades, the SD system has been a model in evolutionary genetics, not only for being selfish, propagating at the expense of its bearers, but as a coadapted gene complex whose fitness is determined by multiple epistatic interactors [5]–[7], [13]–[15].

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