Genetica

, Volume 116, Issue 2–3, pp 225–237 | Cite as

Genetics of Sexual Isolation Based on Courtship Song between Two Sympatric Species: Drosophila Ananassae and D. Pallidosa

  • Hirokazu Yamada
  • Muneo Matsuda
  • Yuzuru Oguma
Article

Abstract

Sexual isolation has been considered one of the primary causes of speciation and its genetic study has the potential to reveal the genetics of speciation. In Drosophila, the importance of courtship songs in sexual isolation between closely related species has been well investigated, but studies analysing the genetic basis of the difference in the courtship songs associated with sexual isolation are less well documented. Drosophila ananassae and Drosophila pallidosa are useful for studies of sexual isolation, because of their sympatric distribution and absence of postmating isolation. Courtship songs are known to play a crucial role in sexual isolation between these two species, and the female discrimination behaviour against the courting male has been revealed to be controlled by a very narrow region on the second chromosome. In this study we investigated the genetic basis controlling the song differences associated with their sexual isolation, using intact and wingless males with chromosomes substituted between species. The results obtained from F1 hybrid males between these species indicate the dominance of the song characters favoured by D. pallidosa females. In addition, the results obtained from backcross F2 males indicate that chromosome 2 had a major effect on the control of the song characters associated with sexual isolation.

chromosomal substitution courtship song Drosophila ananassae Drosophila pallidosa genetic analysis sexual isolation speciation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bennet-Clark, H.C. & A.W. Ewing, 1969. Pulse interval as a critical parameter in the courtship song of Drosophila melanogaster. Anim. Behav. 17: 755–759.Google Scholar
  2. Bock, I.R. & M.R. Wheeler, 1972. The Drosophila melanogaster species group. Univ. Tex. Publ. 7213: 1–102.Google Scholar
  3. Cabot, E.L., A.W. Davis, N.A. Johnson & C.I. Wu, 1994. Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics 137: 175–189.Google Scholar
  4. Charlesworth, B., J.A. Coyne & N.H. Barton, 1987. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130: 113–146.Google Scholar
  5. Cobb, M. & J.-F. Ferveur, 1996. Evolution and genetic control of mate recognition and stimulation in Drosophila. Behav. Proc. 35: 35–54.Google Scholar
  6. Cowling, D.E. & B. Burnet, 1981. Courtship songs and genetic control of their acoustic characteristics in sibling species of Drosophila melanogaster subgroup. Anim. Behav. 29: 924–935.Google Scholar
  7. Coyne, J., 1996. Genetics of sexual isolation in male hybrids of Drosophila simulans and D. mauritiana. Genet. Res. Camb. 68: 211–220.Google Scholar
  8. Crossley, S., 1986. Courtship sounds and behaviour in the four species of the Drosophila bipectinata complex. Anim. Behav. 34: 1146–1159.Google Scholar
  9. Davis, A.W. & C.I. Wu, 1996. The broom of sorcerer's apprentice: the fine structure of a chromosomal region causing reproductive isolation between two sibling species of Drosophila. Genetics 143: 1287–1298.Google Scholar
  10. Davis, A.W., E.G. Noonburg & C.I. Wu, 1994. Evidence for complex genetic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clades. Genetics 137: 191–199.Google Scholar
  11. Doi, M., T. Nemoto, H. Nakanishi, Y. Kuwahara & Y. Oguma, 1997. Behavioral response of males to major sex pheromone component, (Z,Z)-5,25-hentriacontadiene, of Drosophila ananassae females. J. Chem. Ecol. 23: 2067–2078.Google Scholar
  12. Doi, M., M. Matsuda, M. Tomaru, H. Matsubayashi & Y. Oguma, 2001. A locus for female discrimination behavior causing sexual isolation in Drosophila. Proc. Natl. Acad. Sci. USA 98: 6714–6719.Google Scholar
  13. Ehrman, L., 1961. The genetics of sexual isolation in Drosophila paulistrum. Genetics 46: 1025–1038.Google Scholar
  14. Ewing, A.W., 1969. The genetic basis of sound production in Drosophila pseudoobscura and D. persimilis. Anim. Behav. 17: 555–560.Google Scholar
  15. Ewing, A.W., 1983. Functional aspects of Drosophila courtship. Biol. Rev. 58: 275–292.Google Scholar
  16. Ewing, A.W. & H.C. Bennet-Clark, 1968. The courtship songs of Drosophila. Behaviour 31: 288–301.Google Scholar
  17. Ewing, A.W. & J.A. Miyan, 1986. Sexual selection, sexual isolation and the evolution of song in the Drosophila repleta group of species. Anim. Behav. 34: 421–429.Google Scholar
  18. Futch, D.G., 1966. III. A study of speciation in South Pacific population of Drosophila ananassae. Univ. Tex. Publ. 6615: 79–120.Google Scholar
  19. Futch, D.G., 1973. On the ethological differentiation of Drosophila ananassae and Drosophila pallidosa in Samoa. Evolution 27: 456–467.Google Scholar
  20. Hall, J.C., 1994. The mating of a fly. Science 264: 1702–1714.Google Scholar
  21. Hoikkala, A., S. Paallysaho, J. Aspi & J. Lumme, 2000. Localization of genes affecting species differences in male courtship song between Drosophila virilis and D. littoralis. Genet. Res. Camb. 75: 37–45.Google Scholar
  22. Isoherranen, E., J. Aspi & A. Hoikkala, 1999. Variation and consistency of female preference for simulated courtship songs in Drosophila virilis. Anim. Behav. 57: 619–625.Google Scholar
  23. Kyriacou, C.P. & J.C. Hall, 1980. Circadian rhythm mutations in Drosophila melanogaster affect short-term fluctuations in the male's courtship song. Proc. Natl. Acad. Sci. USA 77: 6729–6733.Google Scholar
  24. Kyriacou, C.P. & J.C. Hall, 1982. The function of courtship song rhythms in Drosophila. Anim. Behav. 30: 794–801.Google Scholar
  25. Neems, R.M., K. Dooher, R.K. Butlin & B. Shorrocks, 1997. Differences in male courtship song among the species of the quinaria group of Drosophila. J. Insect. Behav. 10: 237–246.Google Scholar
  26. Nemoto, T., M. Doi, K. Oshio, H. Matsubayashi, Y. Oguma, T. Suzuki & Y. Kuwahara, 1994. (Z,Z)-5,27-tritriacontadiene: major sex pheromone of Drosophila pallidosa (Diptera: Drosophilidae). J. Chem. Ecol. 20: 3029–3037.Google Scholar
  27. Noor, M.A.F., 1997. Genetics of sexual isolation and courtship dysfunction in male hybrids of Drosophila pseudoobscura and Drosophila persimilis. Evolution 51: 809–815.Google Scholar
  28. Noor, M.A.F. & C.F. Aquadro, 1998. Courtship songs of Drosophila pseudoobscura and D. persimilis: analysis of variation. Anim. Behav. 56: 115–125.Google Scholar
  29. Oguma, Y., 1993. Sexual Behavior (Chapter 10), pp. 199–207 in Drosophila ananassae: Genetical and Biological Aspects, edited by Tobari. Jap. Sci. Soc. Press.Google Scholar
  30. Palopoli, M.F. & C.I. Wu, 1994. Genetics of hybrid male sterility between Drosophila sibling species: a complex web of epistasis if revealed in interspecific studies. Genetics 138: 329–341.Google Scholar
  31. Pugh, A.R. & M. Ritchie, 1996. Polygenic control of a mating signal in Drosophila. Heredity 77: 378–382.Google Scholar
  32. Ritchie, M.G. & Phillips, S.D.F., 1998. The Genetics of Sexual Isolation, pp. 291–308 in Endless Forms-Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, New York.Google Scholar
  33. Ritchie, M.G., R.M. Townhill & A. Hoikkala, 1998. Female preference for fly song: playback experiments confirm the targets of sexual selection. Anim. Behav. 56: 713–717.Google Scholar
  34. Spieth, H.T., 1966. V. Mating behavior of D. ananassae and ananassae-like flies from the Pacific. Univ. Tex. Publ. 6615: 133–145.Google Scholar
  35. Stone, W.S., M.R. Wheeler, F.D. Wilson, V.L. Gerstenberg & H. Yang, 1966. I. Genetic studies of natural population of Drosophila II. Pacific island populations. Univ. Tex. Publ. 6615: 1–36.Google Scholar
  36. Tobari, Y.N., 1993. Drosophila ananassae: Genetical and Biological Aspects. Jap. Sci. Soc. Press.Google Scholar
  37. Tomaru, M. & Y. Oguma, 1994a. Differences in courtship song in the species of the Drosophila auraria complex. Anim. Behav. 47: 133–140.Google Scholar
  38. Tomaru, M. & Y. Oguma, 1994b. Genetic basis and evolution of species-specific courtship song in the Drosophila auraria complex. Genet. Res. Camb. 63: 11–17.Google Scholar
  39. Tomaru, M., H. Matsubayashi & Y. Oguma, 1995. Heterospecific inter-pulse intervals of courtship song elicit female rejection in Drosophila biauraria. Anim. Behav. 50: 905–914.Google Scholar
  40. Williams, M.A., A.G. Blouin & M.A.F. Noor, 2001. Courtship songs of Drosophila pseudoobscura and D. persimilis. II. Genetics of species differences. Heredity 86: 68–77.Google Scholar
  41. Yamada, H., T. Sakai, M. Tomaru, M. Doi, M. Matsuda & Y. Oguma, 2002. Search for species-specific mating signal in courtship songs of sympatric sibling species, Drosophila ananassae and D. pallidosa. Genes Genet. Syst. 77: 97–106.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Hirokazu Yamada
    • 1
  • Muneo Matsuda
    • 2
  • Yuzuru Oguma
    • 1
  1. 1.Institute of Biological SciencesUniversity of TsukubaTsukuba, IbarakiJapan
  2. 2.Department of Biology, School of MedicineKyorin UniversityJapan

Personalised recommendations