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PMID: 10747061 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Dominance, epistasis and the genetics of postzygotic isolation.

Genetics ·Vol. 154 ·No. 4 ·2000-04-00 ·Pages 1663-79

Turelli M, Orr HA

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.

MeSH Terms
Animals Drosophila/embryology,genetics Epistasis, Genetic Female Heterozygote Homozygote Hybridization, Genetic Male Models, Genetic Species Specificity Zygote
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Turelli M
Section of Evolution and Ecology and Center for Population Biology, University of California, Davis 95616, USA. [email protected]
Orr H A
References (33)
33 references, click to expand
  1. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids.
    Genetics. 1936 Mar;21(2):113-35 PMID: 17246786
  2. 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):1085-95 PMID: 8587107
  3. Mendelian factors underlying quantitative traits in tomato: comparison across species, generations, and environments.
    Genetics. 1991 Jan;127(1):181-97 PMID: 1673106
  4. 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):841-57 PMID: 17246354
  5. A genetic basis for the inviability of hybrids between sibling species of Drosophila.
    Genetics. 1990 Apr;124(4):909-20 PMID: 2108905
  6. The evolutionary genetics of speciation.
    Philos Trans R Soc Lond B Biol Sci. 1998 Feb 28;353(1366):287-305 PMID: 9533126
  7. The effects of interspecific Y chromosome replacements on hybrid sterility within the Drosophila simulans clade.
    Genetics. 1993 Oct;135(2):443-53 PMID: 8244006
  8. 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 PMID: 8436276
  9. Haldane's rule in taxa lacking a hemizygous X.
    Science. 1998 Oct 30;282(5390):952-4 PMID: 9794768
  10. Sterility of male and female hybrids of Drosophila virilis and Drosophila lummei.
    Heredity (Edinb). 1991 Aug;67 ( Pt 1):1-11 PMID: 1917547
  11. The Y chromosomes of Drosophila lummei and D. novamexicana differ in fertility factors.
    Heredity (Edinb). 1998 Nov;81 ( Pt 5):505-13 PMID: 9881450
  12. 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):819-37 PMID: 8849890
  13. Haldane's rule has multiple genetic causes.
    Nature. 1993 Feb 11;361(6412):532-3 PMID: 8429905
  14. The population genetics of speciation: the evolution of hybrid incompatibilities.
    Genetics. 1995 Apr;139(4):1805-13 PMID: 7789779
  15. The causes of Haldane's rule.
    Science. 1998 Oct 30;282(5390):889-91 PMID: 9841436
  16. 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 PMID: 8765678
  17. The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects.
    Genetics. 1996 Jul;143(3):1243-55 PMID: 8807297
  18. Genetic architecture of autosome-mediated hybrid male sterility in Drosophila.
    Genetics. 1996 Apr;142(4):1169-80 PMID: 8846896
  19. The dominance theory of Haldane's rule.
    Genetics. 1995 May;140(1):389-402 PMID: 7635302
  20. 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):603-9 PMID: 8801221
  21. 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):170-9 PMID: 10328683
  22. Haldane's rule and X-chromosome size in Drosophila.
    Genetics. 1997 Dec;147(4):1799-815 PMID: 9409837
  23. The weaker sex is heterogametic: 75 years of Haldane's rule.
    Genetics. 1997 Nov;147(3):937-51 PMID: 9383043
  24. An autosomal factor from Drosophila arizonae restores normal spermatogenesis in Drosophila mojavensis males carrying the D. arizonae Y chromosome.
    Genetics. 1993 May;134(1):309-18 PMID: 8514139
  25. Maternal effect as a cause of exceptions for Haldane's rule.
    Genetics. 1996 May;143(1):609-11 PMID: 8722809
  26. Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis.
    Genetics. 1987 Aug;116(4):555-63 PMID: 3623079
  27. [Genomic incompatibility in Drosophila virilis Sturt. X Drosophila lummei Hackman hybrids].
    Genetika. 1997 Apr;33(4):458-63 PMID: 9206663
  28. Genetics of postmating reproductive isolation in animals.
    Annu Rev Genet. 1994;28:283-308 PMID: 7893128
  29. 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 PMID: 17246158
  30. Mutation-selection balance and the evolutionary advantage of sex and recombination.
    Genet Res. 1990 Jun;55(3):199-221 PMID: 2394378
  31. Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans.
    Genetics. 1998 Nov;150(3):1091-103 PMID: 9799261
  32. The genetics of postzygotic isolation in the Drosophila virilis group.
    Genetics. 1989 Mar;121(3):527-37 PMID: 2714637
  33. Genetics of hybrid inviability in Drosophila.
    Adv Genet. 1997;36:157-85 PMID: 9348655
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2000-04-00
Pages
1663-79
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1461023
Subset
IM
Grants
NIGMS NIH HHS · GM51932 · United States
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