• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Dec 1997; 147(4): 1799–1815.
PMCID: PMC1208347

Haldane's Rule and X-Chromosome Size in Drosophila

Abstract

The ``dominance theory'' of HALDANE's rule postulates that hybrids of the heterogametic sex are more likely to be inviable or sterile than the homogametic sex because some of the epistatic incompatibilities contributing to postzygotic isolation behave as X-linked partial recessives. When this is true, pairs of taxa with relatively large X chromosomes should require less divergence time, on average, to produce HALDANE's rule than pairs with smaller Xs. Similarly, if the dominance theory is correct and if the X chromosome evolves at a similar rate to the autosomes, the size of the X should not influence the rate at which homogametic hybrids become inviable or sterile. We use Drosophila data to examine both of these predictions. As expected under the dominance theory, pairs of taxa with large X chromosomes (~40% of the nuclear genome) show HALDANE's rule for sterility at significantly smaller genetic distances than pairs with smaller X chromosomes (~20% of the genome). As also predicted, the genetic distances between taxa that exhibit female inviability/sterility show no differences between ``large X'' vs. ``small X'' pairs. We present some simple mathematical models to relate these data to the dominance theory and alternative hypotheses involving faster evolution of the X vs. the autosomes and/or faster evolution of incompatibilities that produce male-specific vs. female-specific sterility. Although the data agree qualitatively with the predictions of the dominance theory, they depart significantly from the quantitative predictions of simple models of the dominance theory and the other hypotheses considered. These departures probably stem from the many simplifying assumptions needed to tractably model epistatic incompatibilities and to analyze heterogeneous data from many taxa.

Full Text

The Full Text of this article is available as a PDF (1.8M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Ayala FJ, Tracey ML. Enzyme variability in the Drosophila willistoni group. 8. Genetic differentiation and reproduction isolation between tow subspecies. J Hered. 1973 May-Jun;64(3):120–124. [PubMed]
  • Bone JR, Kuroda MI. Dosage compensation regulatory proteins and the evolution of sex chromosomes in Drosophila. Genetics. 1996 Oct;144(2):705–713. [PMC free article] [PubMed]
  • Choudhary M, Singh RS. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. III. Variations in Genetic Structure and Their Causes between Drosophila melanogaster and Its Sibling Species Drosophila simulans. Genetics. 1987 Dec;117(4):697–710. [PMC free article] [PubMed]
  • Choudhary M, Coulthart MB, Singh RS. A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VI. Patterns and processes of genic divergence between D. melanogaster and its sibling species, Drosophila simulans. Genetics. 1992 Apr;130(4):843–853. [PMC free article] [PubMed]
  • Coyne JA. 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. [PMC free article] [PubMed]
  • Coyne JA. Genetics and speciation. Nature. 1992 Feb 6;355(6360):511–515. [PubMed]
  • Davis AW, Wu CI. 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. [PMC free article] [PubMed]
  • Dobzhansky T, Ehrman L, Kastritsis PA. Ethological isolation between sympatric and allopatric species of the Obscura group of Drosophila. Anim Behav. 1968 Feb;16(1):79–87. [PubMed]
  • Heikkinen E, Lumme J. Sterility of male and female hybrids of Drosophila virilis and Drosophila lummei. Heredity (Edinb) 1991 Aug;67(Pt 1):1–11. [PubMed]
  • Khadem M, Krimbas CB. Studies of the species barrier between Drosophila subobscura and D. madeirensis. I. The genetics of male hybrid sterility. Heredity (Edinb) 1991 Oct;67(Pt 2):157–165. [PubMed]
  • Kim BK, Watanabe TK, Kitagawa O. Evolutionary genetics of the Drosophila montium subgroup. I. Reproductive isolations and the phylogeny. Jpn J Genet. 1989 Jun;64(3):177–190. [PubMed]
  • Moriyama EN, Powell JR. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. [PubMed]
  • Orr HA. Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics. 1987 Aug;116(4):555–563. [PMC free article] [PubMed]
  • Orr HA. Mapping and characterization of a 'speciation gene' in Drosophila. Genet Res. 1992 Apr;59(2):73–80. [PubMed]
  • Orr HA. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics. 1995 Apr;139(4):1805–1813. [PMC free article] [PubMed]
  • Orr HA, Turelli M. Dominance and Haldane's rule. Genetics. 1996 May;143(1):613–616. [PMC free article] [PubMed]
  • Orr HA, Madden LD, Coyne JA, Goodwin R, Hawley RS. The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics. 1997 Apr;145(4):1031–1040. [PMC free article] [PubMed]
  • Sawamura K. Maternal effect as a cause of exceptions for Haldane's rule. Genetics. 1996 May;143(1):609–611. [PMC free article] [PubMed]
  • Simmons MJ, Crow JF. Mutations affecting fitness in Drosophila populations. Annu Rev Genet. 1977;11:49–78. [PubMed]
  • Sturtevant AH, Novitski E. The Homologies of the Chromosome Elements in the Genus Drosophila. Genetics. 1941 Sep;26(5):517–541. [PMC free article] [PubMed]
  • True JR, Weir BS, Laurie CC. 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. [PMC free article] [PubMed]
  • Turelli M, Orr HA. The dominance theory of Haldane's rule. Genetics. 1995 May;140(1):389–402. [PMC free article] [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...