The sex-ratio trait and its evolution in Drosophila simulans: a comparative approach

  • D. Jutier
  • N. Derome
  • C. Montchamp-Moreau
Part of the Contemporary Issues in Genetics and Evolution book series (CIGE, volume 11)


Sex-ratio X chromosomes, which prevent the production of Y-bearing sperm, have been identified in a dozen Drosophila species covering a wide phylogenetic range. It has not yet been established whether the same ancestral genetic system underlies this type of meiotic drive across the genus, but the biological characteristics and the evolutionary history of species undoubtedly determine the fate of X-linked drivers. The intragenomic conflict they trigger contributes to geographical variation in D. simulans, which shows a sharp contrast between ancestralstock derived and recently introduced populations. In the former, sex-ratio X chromosomes are widespread and sometimes reach a high frequency, but they are inactivated by strong Y-linked and autosomal drive suppressors. In recently-introduced populations, sex-ratio X chromosomes are generally rare and suppressors are moderate or absent. We discuss how this pattern could be related to the recent geographical expansion of D. simulans, and consider possible reasons why sex-ratio drive apparently does not occur in D. melanogaster.

Key words

Drosophila simulans intragenomic conflicts meiotic drive sex chromosomes sex ratio 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Atlan, A., H. Merçot, C. Landre & C. Montchamp-Moreau, 1997. The sex-ratio trait in Drosophila simulans: geographical distribution of distortion and resistance. Evolution 51(6): 1886-1895.Google Scholar
  2. Atlan, A., C. Capillon, N. Derome, D. Couvet & C. Montchamp-Moreau, 2002. The evolution of autosoraal suppressors of sex-ratio drive in Drosophila simulans. Genetica (in press).Google Scholar
  3. Beckenbach, A., 1983. Fitness analysis of the’ sex-ratio polymorphism in experimental populations of Drosophila pseudoobscura. Am. Nat. 121: 630–648.Google Scholar
  4. 1.
    Beckenbach, A.T., 1996. Selection and the’ sex-ratio polymorphism in natural populations of Drosophila pseudoobscura. Evolution 50: 787–794.Google Scholar
  5. Capillon, C., 2000. Évolution du Système sex-ratio chez Drosophila simulans: gènètique et Cytologie. PhD Thesis, Universite Paris 6.Google Scholar
  6. Capillon, C. & A. Atlan, 1999. Evolution of driving X chromosomes and resistance factors in experimental populations of Drosophila simulans. Evolution 53: 506–517.Google Scholar
  7. 1.
    Carvalho, A.B. & L.B. Klaczko, 1993. Autosomal suppressors of sex-ratio in Drosophila mediopunctata. Heredity 71: 546–551.Google Scholar
  8. Carvalho, A.B. & L.B. Klaczko, 1994. Y-linked suppressors of the sex-ratio trait in Drosophila mediopunctata. Heredity 73: 573-579.Google Scholar
  9. Carvalho, A.B., A.A. Peixoto & L.B. Klaczko, 1989. Sex ratio in Drosophila mediopunctata. Heredity 62: 425 128.Google Scholar
  10. Carvalho, A.B., S.C. Vaz & L.B. Klaczko, 1997. Polymorphism for Y-linked suppressors of sex-ratio in two natural populations of Drosophila melanogaster. Genetics 146: 891–902.Google Scholar
  11. Cazemajor, M., 1999. Le Systeme sex-ratio de distorsion de ségrégation méiotique chez Drosophila simulans: gènètique et Cytologie. PhD Thesis, Université Paris 6.Google Scholar
  12. Cazemajor, M., C. Landre & C. Montchamp-Moreau, 1997. The sex-ratio trait in Drosophila simulans: genetic analysis of distortion and suppression. Genetics 147: 635–642.Google Scholar
  13. Cazemajor, M., D.Joly & C. Montchamp-Moreau, 2000. Sex-ratio meiotic drive in Drosophila simulans is related to equational nondisjunction of the Y chromosome. Genetics 154: 229–236.Google Scholar
  14. Chanter, A.O. & D.F. Owen, 1972. The inheritance and population genetics of sex ratio in the butterfly Acraea encedon. J. Zool. 166: 363–383. 1. Clark, A.G., 1987. Natural selection and Y-linked polymorphism. Genetics 115:569-577. 1. Cobbs, G., L. Jewell & L. Gordon, 1991. Male-sex-ratio trait in Drosophila pseudoobscura: frequency of autosomal aneuploid sperm. Genetics 127: 381–39Google Scholar
  15. Curtsinger, J.W. & M.W. Feldman, 1980. Experimental and theoretical analysis of the ’sex-Ratio ’ polymorphism in Drosophila pseudoobscura. Genetics 94: 4451Google Scholar
  16. de Magalhaes, L., I. Roveroni& S. Campos, 1985. Occurrence of the sex-ratio trait in natural populations of Drosophila simulans in Brazil. Bolm Fac. Filos. Cienc. S. Paulo 8: 449-456.Google Scholar
  17. Dermitzakis, E.T., J.P. Masly, H.M. Waldrip & A.G. Clark, 2000. Non-Mendelian segregation of sex chromosomes in heterospecific Drosophila males. Genetics 154(2): 687-694. 1. Edwards, A.W.F., 1961. The population genetics of’ sex-ratio’ in Drosophila pseudoobscura. Heredity 16: 291–30Google Scholar
  18. S., 1967. An abnormal sex ratio in Drosophila simulans. Genetics 56: 189–213.Google Scholar
  19. Fisher, R., 1930. The Genetical Theory of Natural Selection. Clarendon Press, Oxford.Google Scholar
  20. Fredga, K., A. Gropp, H. Winking & F. Frank, 1976. Fertile XX-and XY-type females in the wood lemming Myopus schisricolor. Nature 261: 225–227.Google Scholar
  21. Gershenson, S., 1928. A new sex-ratio abnormality in Drosophila obscura. Genetics 13: 488–507.Google Scholar
  22. Gileva, E.A., 1987. Meiotic drive in the sex chromosome system in the varying lemming Discrotonyx torquantua Pall (Rodentia, Microtinae). Heredity 59: 383–389.Google Scholar
  23. Hamblin, M.T. & M. Veuille, 1999. Population structure among african and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture. Genetics 153: 305–317.Google Scholar
  24. Hamilton, W.D., 1967. Extraordinary sex ratios. Science 156: 477-488.Google Scholar
  25. Hauschteck-Jungen, E., H. Jungen & M. Müller, 1972. Karyotyp und meiose bei wild-und sex ratio-mannchen von Drosophila subobscura. Revue Suisse Zool. 79: 297–305.Google Scholar
  26. Henahan, J. & G. Cobbs, 1983. Origin of X/O progeny from crosses of sex-ratio trait males of Drosophila pseudoobscura. J. Hered. 74: 145–148. 1. Hickey, W.A. & G.B.J. Craig, 1966. Genetic distortion of sex ratio in a mosquito, Aedes aegypti. Genetics 53(6): 1177-1196Google Scholar
  27. Horn, S.,1964. Drosophila simulans. New mutants report. D.I.S. 39: 80.Google Scholar
  28. Hurst, L.D., A. Atlan & B.O. Bengtsson, 1996. Genetic conflicts. Q. Rev. Biol. 71: 317–364. 1. Imhof, M., B. Harr, G. Brem & C. Schlotterer, 1998. Multiple mating in wild Drosophila melanogaster revisited by microsatellite analysis. Mol. Ecol. 7: 915-917Google Scholar
  29. Irvin, S.I., K.A. Wetterstrand, CM. Hutter & C. F. Aquadro, 1998. Genetic variation and differentiation at microsatellite loci in Drosophila simulans: evidence for founder effects in New World populations. Genetics 150: 777–790.Google Scholar
  30. Jaenike, J., 1996. Sex-Ratio meiotic drive in the Drosophila quinaria group. Am. Nat. 148: 237–254.CrossRefGoogle Scholar
  31. Jaenike, J., 1999. Suppression of sex-ratio meiotic drive and the maintenance of Y-chromosome polymorphism in Drosophila. Evolution 53: 164–174.Google Scholar
  32. Jaenike, J., 2001. Sex chromosome meiotic drive. Annu. Rev. Ecol. Syst. 32: 2519.CrossRefGoogle Scholar
  33. James, A. & J. Jaenike, 1990. ’sex ratio’ meiotic drive in Drosophila testacea. Genetics 126(3): 651-656.Google Scholar
  34. Jungen, H., 1968. ’sex ratio’ in natürlichen populationen von Drosophila subobscura. Arch. Jul. Klaus-Stift 43: 52–57. 1. Lachaise, D. & J.F. Silvain, 2004. How two Afrotropical endemics made two cosmopolitan human commensals: the Drosophila melanogaster-D. simulans palaeogeographic riddle. Genetica 120: 17–39. 1. Lachaise, D., M.L. Cariou, J. David, F. Lemeunier, L. Tsacas & M. Ashburner, 1988. Historical biogeography of the Drosophila melanogaster species subgroup, pp. 159-225 in Evolutionary Biology, Vol. 22, edited by M.K. Hecht, B. Wallace & G.T. Prance. New YGoogle Scholar
  35. Lande, R. & G.S. Wilkinson, 1999. Models of sex-ratio meiotic drive and sexual selection in stalk-eyed flies. Genet. Res. Camb. 74: 245–253.CrossRefGoogle Scholar
  36. Lyttle, T.,. Segregation distorters. Annu. Rev. Genet. 25: 511Google Scholar
  37. Lyttle, T.W., 1981. Experimental population genetics of meiotic drive systems. III. Neutralization of sex-ratio distortion in Drosophila through sex-chromosome aneuploidy. Genetics 98(2): 317–334.PubMedGoogle Scholar
  38. McKee, B.D., K. Wilhelm, C. Merrill & X. Ren, 1998. Male sterility and meiotic drive associated with sex chromosome rearrangements in Drosophila. Role of X-Y pairing. Genetics 149: 143–155.PubMedGoogle Scholar
  39. Merçot, H., A. Atlan, M. Jacques & C. Montchamp, 1995. Sex-ratio distortion in Drosophila simulans: co-occurrence of meiotic drive and suppressor of drive. J. Evol. Biol. 8: 283–300.CrossRefGoogle Scholar
  40. Montchamp-Moreau, C. & M. Cazemajor, 2002. Sex-ratio drive in Drosophila simulans: variation in segregation ratio of X chromosomes from a natural population. Genetics (in press).Google Scholar
  41. Montchamp-Moreau, C, V. Ginhoux & A. Atlan, 2001. The Y chromosome of Drosophila simulans are highly polymorphic for their ability to suppress sex-ratio drive. Evolution 55: 728–737.PubMedCrossRefGoogle Scholar
  42. Novitski, E., W.J. Peacock & J. Engel, 1965. Cytological basis of ’sex-ratio’ in Drosophila pseudoobscura. Science 25: 516-577. 1. Ochando, M.D., A. Reyes & F.J. Ayala, 1996. Multiple paternity in two natural populations (orchard and vineyard) of Drosophila. PNAS93: 11769–11773.Google Scholar
  43. Policansky, D. & B. Dempsey, 1978. Modifiers and’ sex ratio’ in Drosophila pseudoobscura. Evolution 32: 922–924. 1. Presgraves, D.C., E. Severance & G.S. Wilkinson, 1997. Sex chromosome meiotic drive in stalk-eyed flies. Genetics 147: 1169-1180. 1. Ramamurthy, G., M. Alfert & C. Stern, 1980. Ultrastructural studies on spermatogenesis in a sex-ratio-mutant strain of Drosophila simulans. Am. J. Anat. 157: 205–21CrossRefGoogle Scholar
  44. Segarra, C. & M. Aguade, 1992. Molecular organization of the X chromosome in different species of the obscura group of Drosophila. Genetics 130: 513–521. 1. Smith, D.A.S., 1975. All-female broods in the polymorphic butterfly Danaus chrysippus and their ecological significance. Heredity 34: 363–37PubMedGoogle Scholar
  45. Stalker, H.D., 1961. The genetic system modifying meiotic drive in Drosophila paramelanica. Genetics 46: 177–202.PubMedGoogle Scholar
  46. Sturtevant, A.H. & T. Dobzhansky, 1936. Geographical distribution and cytology of’ sex-ratio’ in Drosophila pseudoobscura and related species. Genetics 21: 473–490.PubMedGoogle Scholar
  47. Sweeney, T.L. & R. Baar, 1978. Sex ratio distortion caused by meiotic drive in a mosquito, Culex pipiens L. Genetics 88: 427146.Google Scholar
  48. Tao, Y, D.L. Haiti & C.C. Laurie, 2001. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. PNAS 98: 13183–13188.PubMedCrossRefGoogle Scholar
  49. Taylor, D.R., 1994. The genetic basis of sex ratio in Silene alba. Genetics 136: 641–651. 1. Voelker, R.A., 1972. Preliminary characterization of’ sex ratio’ and rediscovery and reinterpretation of ‘male sex ratio in Drosophila affinis. Genetics 71: 597–606. 1. Voelker, R.A. & K. Kojima, 1971. Fertility and fitness of X0 males in Drosophila I. Qualitative study. Evolution 25: 119–128.PubMedGoogle Scholar
  50. Wallace, B., 1948. Studies on’ sex-ratio’ in Drosophila pseudoobscura. I. Selection and ’sex-ratio’. Evolution 2: 189–217. 1. Wu, C.-I., 1983a. Virility deficiency and the sex-ratio trait in Drosophila pseudoobscura. I. Sperm displacement and sexual selection. Genetics 105: 651–662. 1. Wu, C.-I., 1983b. Virility deficiency and the sex-ratio trait in Drosophila pseudoobscura. II. Multiple mating and overall virility selection. Genetics 105: 663–679.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2004

Authors and Affiliations

  • D. Jutier
    • 1
  • N. Derome
    • 1
    • 2
  • C. Montchamp-Moreau
    • 1
  1. 1.Laboratoire Populations Génétique et ÉvolutionCNRS Gif-sur-YvetteParis VIFrance
  2. 2.École Pratique des Hautes Études, Laboratoire d’ÉcologieUniversitéParis VIFrance

Personalised recommendations