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. 2000 Apr;154(4):1663–1679. doi: 10.1093/genetics/154.4.1663

Dominance, epistasis and the genetics of postzygotic isolation.

M Turelli 1, H A Orr 1
PMCID: PMC1461023  PMID: 10747061

Abstract

The sterility and inviability of species hybrids can be explained by between-locus "Dobzhansky-Muller" incompatibilities: alleles that are fit on their "normal" genetic backgrounds sometimes lower fitness when brought together in hybrids. We present a model of two-locus incompatibilities that distinguishes among three types of hybrid interactions: those between heterozygous loci (H(0)), those between a heterozygous and a homozygous (or hemizygous) locus (H(1)), and those between homozygous loci (H(2)). We predict the relative fitnesses of hybrid genotypes by calculating the expected numbers of each type of incompatibility. We use this model to study Haldane's rule and the large effect of X chromosomes on postzygotic isolation. We show that the severity of H(0) vs. H(1) incompatibilities is key to understanding Haldane's rule, while the severity of H(1) vs. H(2) incompatibilities must also be considered to explain large X effects. Large X effects are not inevitable in backcross analyses but rather-like Haldane's rule-may often reflect the recessivity of alleles causing postzygotic isolation. We also consider incompatibilities involving the Y (or W) chromosome and maternal effects. Such incompatibilities are common in Drosophila species crosses, and their consequences in male- vs. female-heterogametic taxa may explain the pattern of exceptions to Haldane's rule.

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Selected References

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  1. Carvajal A. R., Gandarela M. R., Naveira H. F. A three-locus system of interspecific incompatibility underlies male inviability in hybrids between Drosophila buzzatii and D. koepferae. Genetica. 1996 Jul;98(1):1–19. doi: 10.1007/BF00120214. [DOI] [PubMed] [Google Scholar]
  2. Charlesworth B. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet Res. 1990 Jun;55(3):199–221. doi: 10.1017/s0016672300025532. [DOI] [PubMed] [Google Scholar]
  3. Civetta A., Singh R. S. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol. 1995 Dec;41(6):1085–1095. doi: 10.1007/BF00173190. [DOI] [PubMed] [Google Scholar]
  4. Coyne J. A., Orr H. A. The evolutionary genetics of speciation. Philos Trans R Soc Lond B Biol Sci. 1998 Feb 28;353(1366):287–305. doi: 10.1098/rstb.1998.0210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coyne J. A., Simeonidis S., Rooney P. Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans. Genetics. 1998 Nov;150(3):1091–1103. doi: 10.1093/genetics/150.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. 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]
  7. Falileeva L. I., Mitrofanov V. G. Genomnaia nesovmestimost' u gibridov Drosophila virilis X Drosophila lummei Hackman. Genetika. 1997 Apr;33(4):458–463. [PubMed] [Google Scholar]
  8. 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. doi: 10.1038/hdy.1991.58. [DOI] [PubMed] [Google Scholar]
  9. Heikkinen E., Lumme J. The Y chromosomes of Drosophila lummei and D. novamexicana differ in fertility factors. Heredity (Edinb) 1998 Nov;81(Pt 5):505–513. doi: 10.1046/j.1365-2540.1998.00422.x. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Hutter P. Genetics of hybrid inviability in Drosophila. Adv Genet. 1997;36:157–185. doi: 10.1016/s0065-2660(08)60309-0. [DOI] [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. 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]
  14. Lamnissou K., Loukas M., Zouros E. Incompatibilities between Y chromosome and autosomes are responsible for male hybrid sterility in crosses between Drosophila virilis and Drosophila texana. Heredity (Edinb) 1996 Jun;76(Pt 6):603–609. doi: 10.1038/hdy.1996.86. [DOI] [PubMed] [Google Scholar]
  15. Laurie C. C. The weaker sex is heterogametic: 75 years of Haldane's rule. Genetics. 1997 Nov;147(3):937–951. doi: 10.1093/genetics/147.3.937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Marín I. Genetic architecture of autosome-mediated hybrid male sterility in Drosophila. Genetics. 1996 Apr;142(4):1169–1180. doi: 10.1093/genetics/142.4.1169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Naveira H., Fontdevila A. The Evolutionary History of DROSOPHILA BUZZATII. Xii. the Genetic Basis of Sterility in Hybrids between D. BUZZATII and Its Sibling D. SERIDO from Argentina. Genetics. 1986 Nov;114(3):841–857. doi: 10.1093/genetics/114.3.841. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Orr H. A., Coyne J. A. The genetics of postzygotic isolation in the Drosophila virilis group. Genetics. 1989 Mar;121(3):527–537. doi: 10.1093/genetics/121.3.527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Orr H. A. Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics. 1987 Aug;116(4):555–563. doi: 10.1093/genetics/116.4.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Orr H. A. Haldane's rule has multiple genetic causes. Nature. 1993 Feb 11;361(6412):532–533. doi: 10.1038/361532a0. [DOI] [PubMed] [Google Scholar]
  21. Orr H. A. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics. 1995 Apr;139(4):1805–1813. doi: 10.1093/genetics/139.4.1805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Paterson A. H., Damon S., Hewitt J. D., Zamir D., Rabinowitch H. D., Lincoln S. E., Lander E. S., Tanksley S. D. Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments. Genetics. 1991 Jan;127(1):181–197. doi: 10.1093/genetics/127.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Presgraves D. C., Orr H. A. Haldane's rule in taxa lacking a hemizygous X. Science. 1998 Oct 30;282(5390):952–954. doi: 10.1126/science.282.5390.952. [DOI] [PubMed] [Google Scholar]
  25. Sawamura K. Maternal effect as a cause of exceptions for Haldane's rule. Genetics. 1996 May;143(1):609–611. doi: 10.1093/genetics/143.1.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sawamura K., Taira T., Watanabe T. K. Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics. 1993 Feb;133(2):299–305. doi: 10.1093/genetics/133.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Suzuki M. G., Shimada T., Kobayashi M. Bm kettin, homologue of the Drosophila kettin gene, is located on the Z chromosome in Bombyx mori and is not dosage compensated. Heredity (Edinb) 1999 Feb;82(Pt 2):170–179. doi: 10.1038/sj.hdy.6884570. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Turelli M., Begun D. J. Haldane's rule and X-chromosome size in Drosophila. Genetics. 1997 Dec;147(4):1799–1815. doi: 10.1093/genetics/147.4.1799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Turelli M., Orr H. A. The dominance theory of Haldane's rule. Genetics. 1995 May;140(1):389–402. doi: 10.1093/genetics/140.1.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Turelli M. The causes of Haldane's rule. Science. 1998 Oct 30;282(5390):889–891. doi: 10.1126/science.282.5390.889. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. 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]

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