The Dominance Theory of HALDANE's Rule

INVESTIGATIONS

The Dominance Theory of HALDANE's Rule

M. Turelli and H. A. Orr
Section of Evolution and Ecology and Center for Population Biology, University of California, Davis, California 95616

``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.

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				M. Turelli and L. C. Moyle Asymmetric Postmating Isolation: Darwin's Corollary to Haldane's Rule Genetics, June 1, 2007; 176(2): 1059 - 1088. [Abstract] [Full Text] [PDF]

				A. S. Chang and M. A. F. Noor The Genetics of Hybrid Male Sterility Between the Allopatric Species Pair Drosophila persimilis and D. pseudoobscura bogotana: Dominant Sterility Alleles in Collinear Autosomal Regions Genetics, May 1, 2007; 176(1): 343 - 349. [Abstract] [Full Text] [PDF]

				A. Geraldes, N. Ferrand, and M. W. Nachman Contrasting Patterns of Introgression at X-Linked Loci Across the Hybrid Zone Between Subspecies of the European Rabbit (Oryctolagus cuniculus) Genetics, June 1, 2006; 173(2): 919 - 933. [Abstract] [Full Text] [PDF]

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				J. K. Kelly Epistasis in Monkeyflowers Genetics, December 1, 2005; 171(4): 1917 - 1931. [Abstract] [Full Text] [PDF]

				B. Fernandez, A. Garcia-Dorado, and A. Caballero The Effect of Antagonistic Pleiotropy on the Estimation of the Average Coefficient of Dominance of Deleterious Mutations Genetics, December 1, 2005; 171(4): 2097 - 2112. [Abstract] [Full Text] [PDF]

				L. C. Moyle and E. B. Graham Genetics of Hybrid Incompatibility Between Lycopersicon esculentum and L. hirsutum Genetics, January 1, 2005; 169(1): 355 - 373. [Abstract] [Full Text] [PDF]

				C. E. Linn Jr., H. R. Dambroski, J. L. Feder, S. H. Berlocher, S. Nojima, and W. L. Roelofs Postzygotic isolating factor in sympatric speciation in Rhagoletis flies: Reduced response of hybrids to parental host-fruit odors PNAS, December 21, 2004; 101(51): 17753 - 17758. [Abstract] [Full Text] [PDF]

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				D. C. Presgraves A Fine-Scale Genetic Analysis of Hybrid Incompatibilities in Drosophila Genetics, March 1, 2003; 163(3): 955 - 972. [Abstract] [Full Text] [PDF]

				H.-W. Deng, G. Gao, and J.-L. Li Estimation of Deleterious Genomic Mutation Parameters in Natural Populations by Accounting for Variable Mutation Effects Across Loci Genetics, November 1, 2002; 162(3): 1487 - 1500. [Abstract] [Full Text] [PDF]

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				N. A. Johnson Sixty Years After "Isolating Mechanisms, Evolution and Temperature": Muller's Legacy Genetics, July 1, 2002; 161(3): 939 - 944. [Full Text] [PDF]

				H. A. Orr and S. Irving Complex Epistasis and the Genetic Basis of Hybrid Sterility in the Drosophila pseudoobscura Bogota-USA Hybridization Genetics, July 1, 2001; 158(3): 1089 - 1100. [Abstract] [Full Text] [PDF]

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				R. R. Snook, S. Y. Cleland, M. F. Wolfner, and T. L. Karr Offsetting Effects of Wolbachia Infection and Heat Shock on Sperm Production in Drosophila simulans: Analyses of Fecundity, Fertility and Accessory Gland Proteins Genetics, May 1, 2000; 155(1): 167 - 178. [Abstract] [Full Text]

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				M. Turelli and H. A. Orr Dominance, Epistasis and the Genetics of Postzygotic Isolation Genetics, April 1, 2000; 154(4): 1663 - 1679. [Abstract] [Full Text]

				D. A. Barbash, J. Roote, and M. Ashburner The Drosophila melanogaster Hybrid male rescue Gene Causes Inviability in Male and Female Species Hybrids Genetics, April 1, 2000; 154(4): 1747 - 1771. [Abstract] [Full Text]

				M. Kirkpatrick and M. R. Servedio The Reinforcement of Mating Preferences on an Island Genetics, February 1, 1999; 151(2): 865 - 884. [Abstract] [Full Text]

				J. A. Coyne, S. Simeonidis, and P. Rooney Relative Paucity of Genes Causing Inviability in Hybrids Between Drosophila melanogaster and D. simulans Genetics, November 1, 1998; 150(3): 1091 - 1103. [Abstract] [Full Text]

				D. C. Presgraves and H. A. Orr Haldane's Rule in Taxa Lacking a Hemizygous X Science, October 30, 1998; 282(5390): 952 - 954. [Abstract] [Full Text]