Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 1997 Nov;147(3):1191–1201. doi: 10.1093/genetics/147.3.1191

Incipient Speciation by Sexual Isolation in Drosophila Melanogaster: Extensive Genetic Divergence without Reinforcement

H Hollocher 1, C T Ting 1, M L Wu 1, C I Wu 1
PMCID: PMC1208243  PMID: 9383062

Abstract

The collection of Drosophila melanogaster from Zimbabwe and nearby regions (the Z-type) yield females who would not mate with the cosmopolitan D. melanogaster males (the M-type). To dissect the genetic basis of this sexual isolation, we constructed 16 whole-chromosome substitution lines between two standard Z-and M-lines. The results were as follows: (1) All substitution lines appear normal in viability and fertility in both sexes, indicating no strong postmating isolation. (2) The genes for the behaviors are mapped to all three major chromosomes with the same ranking and comparable magnitude of effects for both sexes: III > II >> X >/= 0 (III, II and X designate the effects of the three chromosomes). The results suggest less evolution on the X than on autosomes at loci of sexual behavior. (3) The genes for ``Z-maleness'' are many and somewhat redundant. Whole-chromosome effects for Z-maleness appear nearly additive and show little dominance. (4) In contrast, ``Z-femaleness'' has less redundancy as partial genotypes never exhibit full phenotypic effects. Epistatic interactions and incomplete dominance can sometimes be detected. (5) The extensive genetic divergence underlying sexual isolation has evolved in the absence of detectable reduction in hybrid fitnesses. Sexual selection has apparently been a driving force of multiple facets of speciation at the nascent stage without reinforcement.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. Begun D. J., Aquadro C. F. African and North American populations of Drosophila melanogaster are very different at the DNA level. Nature. 1993 Oct 7;365(6446):548–550. doi: 10.1038/365548a0. [DOI] [PubMed] [Google Scholar]
  2. Begun D. J., Aquadro C. F. Evolution at the tip and base of the X chromosome in an African population of Drosophila melanogaster. Mol Biol Evol. 1995 May;12(3):382–390. doi: 10.1093/oxfordjournals.molbev.a040213. [DOI] [PubMed] [Google Scholar]
  3. Cabot E. L., Davis A. W., Johnson N. A., Wu C. I. Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics. 1994 May;137(1):175–189. doi: 10.1093/genetics/137.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Coyne J. A., Charlesworth B. Genetic analysis of X-linked sterility in hybrids between three sibling species of Drosophila. Heredity (Edinb) 1989 Feb;62(Pt 1):97–106. doi: 10.1038/hdy.1989.13. [DOI] [PubMed] [Google Scholar]
  5. Coyne J. A. Genetics and speciation. Nature. 1992 Feb 6;355(6360):511–515. doi: 10.1038/355511a0. [DOI] [PubMed] [Google Scholar]
  6. Coyne J. A. Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5464–5468. doi: 10.1073/pnas.86.14.5464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davis A. W., Noonburg E. G., Wu C. I. Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade. Genetics. 1994 May;137(1):191–199. doi: 10.1093/genetics/137.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Davis A. W., Wu C. I. The broom of the sorcerer's apprentice: the fine structure of a chromosomal region causing reproductive isolation between two sibling species of Drosophila. Genetics. 1996 Jul;143(3):1287–1298. doi: 10.1093/genetics/143.3.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dobzhansky T. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics. 1936 Mar;21(2):113–135. doi: 10.1093/genetics/21.2.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. EHRMAN L. The genetics of sexual isolation in Drosophila paulistorum. Genetics. 1961 Aug;46:1025–1038. doi: 10.1093/genetics/46.8.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hollocher H., Wu C. I. The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics. 1996 Jul;143(3):1243–1255. doi: 10.1093/genetics/143.3.1243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hutter P., Roote J., Ashburner M. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics. 1990 Apr;124(4):909–920. doi: 10.1093/genetics/124.4.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Iwasa Y., Pomiankowski A. Continual change in mate preferences. Nature. 1995 Oct 5;377(6548):420–422. doi: 10.1038/377420a0. [DOI] [PubMed] [Google Scholar]
  14. Johnson N. A., Perez D. E., Cabot E. L., Hollocher H., Wu C. I. A test of reciprocal X-Y interactions as a cause of hybrid sterility in Drosophila. Nature. 1992 Aug 27;358(6389):751–753. doi: 10.1038/358751a0. [DOI] [PubMed] [Google Scholar]
  15. Kim B. K., Watanabe T. K., Kitagawa O. Evolutionary genetics of the Drosophila montium subgroup. I. Reproductive isolations and the phylogeny. Jpn J Genet. 1989 Jun;64(3):177–190. doi: 10.1266/jjg.64.177. [DOI] [PubMed] [Google Scholar]
  16. Krebs R. A. Courtship behavior and control of reproductive isolation in Drosophila mojavensis: genetic analysis of population hybrids. Behav Genet. 1990 Jul;20(4):535–543. doi: 10.1007/BF01067718. [DOI] [PubMed] [Google Scholar]
  17. Lande R. Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3721–3725. doi: 10.1073/pnas.78.6.3721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Naveira H. F. Location of X-linked polygenic effects causing sterility in male hybrids of Drosophila simulans and D. mauritiana. Heredity (Edinb) 1992 Mar;68(Pt 3):211–217. doi: 10.1038/hdy.1992.34. [DOI] [PubMed] [Google Scholar]
  19. Palopoli M. F., Wu C. I. Genetics of hybrid male sterility between drosophila sibling species: a complex web of epistasis is revealed in interspecific studies. Genetics. 1994 Oct;138(2):329–341. doi: 10.1093/genetics/138.2.329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pantazidis A. C., Galanopoulos V. K., Zouros E. An autosomal factor from Drosophila arizonae restores normal spermatogenesis in Drosophila mojavensis males carrying the D. arizonae Y chromosome. Genetics. 1993 May;134(1):309–318. doi: 10.1093/genetics/134.1.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Perez D. E., Wu C. I. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics. 1995 May;140(1):201–206. doi: 10.1093/genetics/140.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Perez D. E., Wu C. I., Johnson N. A., Wu M. L. Genetics of reproductive isolation in the Drosophila simulans clade: DNA marker-assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics. 1993 May;134(1):261–275. doi: 10.1093/genetics/134.1.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rice W. R. Sexually antagonistic genes: experimental evidence. Science. 1992 Jun 5;256(5062):1436–1439. doi: 10.1126/science.1604317. [DOI] [PubMed] [Google Scholar]
  24. Tan C. C. Genetics of Sexual Isolation between DROSOPHILA PSEUDOOBSCURA and DROSOPHILA PERSIMILIS. Genetics. 1946 Nov;31(6):558–573. doi: 10.1093/genetics/31.6.558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. True J. R., Weir B. S., Laurie C. C. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics. 1996 Mar;142(3):819–837. doi: 10.1093/genetics/142.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Wu C. I., Hollocher H., Begun D. J., Aquadro C. F., Xu Y., Wu M. L. Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2519–2523. doi: 10.1073/pnas.92.7.2519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wu C. I., Palopoli M. F. Genetics of postmating reproductive isolation in animals. Annu Rev Genet. 1994;28:283–308. doi: 10.1146/annurev.ge.28.120194.001435. [DOI] [PubMed] [Google Scholar]
  29. Zouros E. Advances in the genetics of reproductive isolation in Drosophila. Genome. 1989;31(1):211–220. doi: 10.1139/g89-036. [DOI] [PubMed] [Google Scholar]
  30. Zouros E. The chromosomal basis of sexual isolation in two sibling species of Drosophila: D. arizonensis and D. mojavensis. Genetics. 1981 Mar-Apr;97(3-4):703–718. doi: 10.1093/genetics/97.3-4.703. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES