Skip to main content
Genetics logoLink to Genetics
. 2002 Nov;162(3):1221–1231. doi: 10.1093/genetics/162.3.1221

Sex-ratio drive in Drosophila simulans: variation in segregation ratio of X chromosomes from a natural population.

Catherine Montchamp-Moreau 1, Michel Cazemajor 1
PMCID: PMC1462311  PMID: 12454068

Abstract

The sex-ratio trait that exists in a dozen Drosophila species is a case of naturally occurring X chromosome drive that causes males to produce female-biased progeny. Autosomal and Y polymorphism for suppressors are known to cause variation in drive expression, but the X chromosome polymorphism has never been thoroughly investigated. We characterized 41 X chromosomes from a natural population of Drosophila simulans that had been transferred to a suppressor-free genetic background. We found two clear-cut groups of chromosomes, sex-ratio and standard. The sex-ratio X chromosomes differed in their segregation ratio (81-96% females in the progeny), the less powerful drivers being less stable in their expression. A sib analysis, using a moderate driver, indicated that within-X variation in drive expression depended on genetic (autosomal) or epigenetic factors and that the age of the males also affected the trait. The other X chromosomes produced equal or roughly equal sex ratios, but again with significant variation. The continuous pattern of variation observed within both groups suggested that, in addition to a major sex-ratio gene, many X-linked loci of small effect modify the segregation ratio of this chromosome and are maintained in a polymorphic state. This was also supported by the frequency distribution of sex ratios produced by recombinant X chromosomes.

Full Text

The Full Text of this article is available as a PDF (154.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Carvalho A. B., Vaz S. C. Are Drosophila SR drive chromosomes always balanced? Heredity (Edinb) 1999 Sep;83(Pt 3):221–228. doi: 10.1038/sj.hdy.6886100. [DOI] [PubMed] [Google Scholar]
  2. Carvalho A. B., Vaz S. C., Klaczko L. B. Polymorphism for Y-linked suppressors of sex-ratio in two natural populations of Drosophila mediopunctata. Genetics. 1997 Jul;146(3):891–902. doi: 10.1093/genetics/146.3.891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Cazemajor M., Landré C., Montchamp-Moreau C. The sex-ratio trait in Drosophila simulans: genetic analysis of distortion and suppression. Genetics. 1997 Oct;147(2):635–642. doi: 10.1093/genetics/147.2.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clark A. G. Natural selection and Y-linked polymorphism. Genetics. 1987 Mar;115(3):569–577. doi: 10.1093/genetics/115.3.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Curtsinger J. W. Components of selection in X chromosome lines of Drosophila melanogaster: sex ratio modification by meiotic drive and viability selection. Genetics. 1984 Dec;108(4):941–952. doi: 10.1093/genetics/108.4.941. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dermitzakis E. T., Masly J. P., Waldrip H. M., Clark A. G. Non-Mendelian segregation of sex chromosomes in heterospecific Drosophila males. Genetics. 2000 Feb;154(2):687–694. doi: 10.1093/genetics/154.2.687. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Faulhaber S. H. An abnormal sex ratio in Drosophila simulans. Genetics. 1967 May;56(1):189–213. doi: 10.1093/genetics/56.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hamilton W. D. Extraordinary sex ratios. A sex-ratio theory for sex linkage and inbreeding has new implications in cytogenetics and entomology. Science. 1967 Apr 28;156(3774):477–488. doi: 10.1126/science.156.3774.477. [DOI] [PubMed] [Google Scholar]
  9. Hauschteck-Jungen E. Postmating reproductive isolation and modification of the 'sex ratio' trait in Drosophila subobscura induced by the sex chromosome gene arrangement A2+3+5+7. Genetica. 1990;83(1):31–44. doi: 10.1007/BF00774686. [DOI] [PubMed] [Google Scholar]
  10. Hiraizumi Y., Watanabe S. S. Aging effect on the phenomenon of segregation distortion in Drosophila melanogaster. Genetics. 1969 Sep;63(1):121–131. doi: 10.1093/genetics/63.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hurst L. D., Pomiankowski A. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena. Genetics. 1991 Aug;128(4):841–858. doi: 10.1093/genetics/128.4.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lyttle T. W. Experimental Population Genetics of Meiotic Drive Systems II. Accumulation of Genetic Modifiers of Segregation Distorter (SD) in Laboratory Populations. Genetics. 1979 Feb;91(2):339–357. doi: 10.1093/genetics/91.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Miklos G. L., Smith-White S. An analysis of the instability of segregation-distorter in Drosophila melanogaster. Genetics. 1971 Feb;67(2):305–317. doi: 10.1093/genetics/67.2.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Montchamp-Moreau C., Ginhoux V., Atlan A. The Y chromosomes of Drosophila simulans are highly polymorphic for their ability to suppress sex-ratio drive. Evolution. 2001 Apr;55(4):728–737. doi: 10.1554/0014-3820(2001)055[0728:tycods]2.0.co;2. [DOI] [PubMed] [Google Scholar]
  15. Stalker H D. The Genetic Systems Modifying Meiotic Drive in Drosophila Paramelanica. Genetics. 1961 Feb;46(2):177–202. doi: 10.1093/genetics/46.2.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Sturtevant A H, Dobzhansky T. Geographical Distribution and Cytology of "Sex Ratio" in Drosophila Pseudoobscura and Related Species. Genetics. 1936 Jul;21(4):473–490. doi: 10.1093/genetics/21.4.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Tao Y., Hartl D. L., Laurie C. C. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc Natl Acad Sci U S A. 2001 Oct 30;98(23):13183–13188. doi: 10.1073/pnas.231478798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Taylor Jesse E., Jaenike John. Sperm competition and the dynamics of X chromosome drive: stability and extinction. Genetics. 2002 Apr;160(4):1721–1731. doi: 10.1093/genetics/160.4.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Temin R. G. The independent distorting ability of the Enhancer of Segregation Distortion, E(SD), in Drosophila melanogaster. Genetics. 1991 Jun;128(2):339–356. doi: 10.1093/genetics/128.2.339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Voelker R. A. Preliminary characterization of "sex ratio" and rediscovery and reinterpretation of "male sex ratio" in Drosophila affinis. Genetics. 1972 Aug;71(4):597–606. doi: 10.1093/genetics/71.4.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wu C. I., Beckenbach A. T. Evidence for Extensive Genetic Differentiation between the Sex-Ratio and the Standard Arrangement of DROSOPHILA PSEUDOOBSCURA and D. PERSIMILIS and Identification of Hybrid Sterility Factors. Genetics. 1983 Sep;105(1):71–86. doi: 10.1093/genetics/105.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wu C. I. The fate of autosomal modifiers of the sex-ratio trait in drosophila and other sex-linked meiotic drive systems. Theor Popul Biol. 1983 Oct;24(2):107–120. doi: 10.1016/0040-5809(83)90035-7. [DOI] [PubMed] [Google Scholar]
  23. de Carvalho A. B., Klaczko L. B. Age and sex-ratio expression in Drosophila mediopunctata. Genetica. 1992;87(2):107–111. doi: 10.1007/BF00121000. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES