Skip to main content
Genetics logoLink to Genetics
. 1995 May;140(1):389–402. doi: 10.1093/genetics/140.1.389

The Dominance Theory of Haldane's Rule

M Turelli 1, H A Orr 1
PMCID: PMC1206564  PMID: 7635302

Abstract

``HALDANE's rule'' states that, if species hybrids of one sex only are inviable or sterile, the afflicted sex is much more likely to be heterogametic (XY) than homogametic (XX). We show that most or all of the phenomena associated with HALDANE's rule can be explained by the simple hypothesis that alleles decreasing hybrid fitness are partially recessive. Under this hypothesis, the XY sex suffers more than the XX because X-linked alleles causing postzygotic isolation tend to have greater cumulative effects when hemizygous than when heterozygous, even though the XX sex carries twice as many such alleles. The dominance hypothesis can also account for the ``large X effect,'' the disproportionate effect of the X chromosome on hybrid inviability/sterility. In addition, the dominance theory is consistent with: the long temporal lag between the evolution of heterogametic and homogametic postzygotic isolation, the frequency of exceptions to HALDANE's rule, puzzling Drosophila experiments in which ``unbalanced'' hybrid females, who carry two X chromosomes from the same species, remain fertile whereas F(1) hybrid males are sterile, and the absence of cases of HALDANE's rule for hybrid inviability in mammals. We discuss several novel predictions that could lead to rejection of the dominance theory.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. 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]
  2. Coyne J. A. Genetics and speciation. Nature. 1992 Feb 6;355(6360):511–515. doi: 10.1038/355511a0. [DOI] [PubMed] [Google Scholar]
  3. Coyne J. A. The genetic basis of Haldane's rule. 1985 Apr 25-May 1Nature. 314(6013):736–738. doi: 10.1038/314736a0. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Garcia-Bellido A., Robbins L. G. Viability of Female Germ-Line Cells Homozygous for Zygotic Lethals in DROSOPHILA MELANOGASTER. Genetics. 1983 Feb;103(2):235–247. doi: 10.1093/genetics/103.2.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Grant S. G., Chapman V. M. Mechanisms of X-chromosome regulation. Annu Rev Genet. 1988;22:199–233. doi: 10.1146/annurev.ge.22.120188.001215. [DOI] [PubMed] [Google Scholar]
  7. Johnson N. A., Hollocher H., Noonburg E., Wu C. I. The effects of interspecific Y chromosome replacements on hybrid sterility within the Drosophila simulans clade. Genetics. 1993 Oct;135(2):443–453. doi: 10.1093/genetics/135.2.443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kacser H., Burns J. A. The molecular basis of dominance. Genetics. 1981 Mar-Apr;97(3-4):639–666. doi: 10.1093/genetics/97.3-4.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kondrashov A. S. Deleterious mutations and the evolution of sexual reproduction. Nature. 1988 Dec 1;336(6198):435–440. doi: 10.1038/336435a0. [DOI] [PubMed] [Google Scholar]
  10. Kratzer P. G., Chapman V. M. X chromosome reactivation in oocytes of Mus caroli. Proc Natl Acad Sci U S A. 1981 May;78(5):3093–3097. doi: 10.1073/pnas.78.5.3093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Migeon B. R., Moser H. W., Moser A. B., Axelman J., Sillence D., Norum R. A. Adrenoleukodystrophy: evidence for X linkage, inactivation, and selection favoring the mutant allele in heterozygous cells. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5066–5070. doi: 10.1073/pnas.78.8.5066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Migeon B. R. X-chromosome inactivation: molecular mechanisms and genetic consequences. Trends Genet. 1994 Jul;10(7):230–235. doi: 10.1016/0168-9525(94)90169-4. [DOI] [PubMed] [Google Scholar]
  13. Ripoll P. Behavior of somatic cells homozygous for zygotic lethals in Drosophila melanogaster. Genetics. 1977 Jun;86(2 Pt 1):357–376. [PMC free article] [PubMed] [Google Scholar]
  14. Simmons M. J., Crow J. F. Mutations affecting fitness in Drosophila populations. Annu Rev Genet. 1977;11:49–78. doi: 10.1146/annurev.ge.11.120177.000405. [DOI] [PubMed] [Google Scholar]
  15. Takagi N. Differentiation of X chromosomes in early female mouse embryos. Exp Cell Res. 1974 May;86(1):127–135. doi: 10.1016/0014-4827(74)90657-0. [DOI] [PubMed] [Google Scholar]
  16. 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]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES