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 (∼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.
Highlights
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 [1,2,3,4,5,6,7,8]
After genetically extracting the SD chromosomes, we sequenced the,4.5-kb Segregation distorter (Sd)-RanGAP sequence from all 12 as well as the homologous region of the parent gene, RanGAP, from 10 wildtype chromosomes sampled from Zimbabwe
The hitchhiking effects of selfish meiotic drive gene complexes have shaped patterns of DNA sequence variability in at least five other cases: four selfish X chromosome systems that drive in the male germline and a selfish autosomal centromere that drives in the female germline of the monkeyflower, Mimulus guttatus [61]
Summary
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 [1,2,3,4,5,6,7,8]. Full strength distortion is caused by three interacting loci clustered around the centromere of chromosome 2 (an autosome): the transacting 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). The clustering of SD loci around the centromere of chromosome 2, where crossing over is reduced, is unsurprising [15]. The paracentric inversions are thought to reduce crossing over between the centromeric SD elements and modifiers of distortion distributed across 2R, such as Modifier of SD (M(SD)), Stabilizer of SD (St(SD)), and possibly others [19,20,21,22]. SD chromosomes have evolved a complex of multiple, epistatically interacting loci with coadapted alleles whose linkage relationships are usually further tightened by one or more chromosomal inversions
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