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PMID: 18514967 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Sex chromosomes and speciation in Drosophila.

Trends in genetics : TIG ·Vol. 24 ·No. 7 ·2008-07-00 ·Pages 336-43

Presgraves DC

Abstract

Two empirical rules suggest that sex chromosomes play a special role in speciation. The first is Haldane's rule - the preferential sterility and inviability of species hybrids of the heterogametic (XY) sex. The second is the disproportionately large effect of the X chromosome in genetic analyses of hybrid sterility. Whereas the causes of Haldane's rule are well established, the causes of the 'large X-effect' have remained controversial. New genetic analyses in Drosophila confirm that the X is a hotspot for hybrid male sterility factors, providing a proximate explanation for the large X-effect. Several other new findings -- on faster X evolution, X chromosome meiotic drive and the regulation of the X chromosome in the male-germline -- provide plausible evolutionary explanations for the large X-effect.

MeSH Terms
Animals Drosophila/genetics Evolution, Molecular Genetic Speciation Infertility Male Sex Chromosomes/genetics X Chromosome/genetics
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Presgraves Daven C
Department of Biology, University of Rochester, Rochester, NY 14627, USA. [email protected] <[email protected]>
References (65)
65 references, click to expand
  1. Patterns of postzygotic isolation in Lepidoptera.
    Evolution. 2002 Jun;56(6):1168-83 PMID: 12144018
  2. A test for faster X evolution in Drosophila.
    Mol Biol Evol. 2002 Oct;19(10):1816-9 PMID: 12270910
  3. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans.
    PLoS Biol. 2007 Nov 6;5(11):e310 PMID: 17988176
  4. 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
  5. Using comparative genomic data to test for fast-X evolution.
    Evolution. 2004 Mar;58(3):656-60 PMID: 15119449
  6. On the relative roles of faster-X evolution and dominance in the establishment of intrinsic postzygotic isolating barriers.
    Genetica. 2003 May;118(1):41-50 PMID: 12733663
  7. Histone H3 lysine 9 acetylation pattern suggests that X and B chromosomes are silenced during entire male meiosis in a grasshopper.
    Cytogenet Genome Res. 2007;119(1-2):135-42 PMID: 18160793
  8. Meiotic segregation and male recombination in interspecific hybrids of Drosophila.
    Genetics. 1986 Oct;114(2):485-94 PMID: 3021573
  9. Pervasive and largely lineage-specific adaptive protein evolution in the dosage compensation complex of Drosophila melanogaster.
    Genetics. 2007 Nov;177(3):1959-62 PMID: 18039888
  10. Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages.
    Mol Biol Evol. 2007 Jan;24(1):137-45 PMID: 17032727
  11. Paucity of genes on the Drosophila X chromosome showing male-biased expression.
    Science. 2003 Jan 31;299(5607):697-700 PMID: 12511656
  12. The population genetics of the origin and divergence of the Drosophila simulans complex species.
    Genetics. 2000 Dec;156(4):1913-31 PMID: 11102384
  13. Gene transposition as a cause of hybrid sterility in Drosophila.
    Science. 2006 Sep 8;313(5792):1448-50 PMID: 16960009
  14. Contrasting the efficacy of selection on the X and autosomes in Drosophila.
    Mol Biol Evol. 2008 Feb;25(2):454-67 PMID: 18083702
  15. FURTHER EVIDENCE AGAINST MEIOTIC-DRIVE MODELS OF HYBRID STERILITY.
    Evolution. 1993 Apr;47(2):685-687 PMID: 28568727
  16. Speciation genes.
    Curr Opin Genet Dev. 2004 Dec;14(6):675-9 PMID: 15531163
  17. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila.
    Science. 2006 Nov 24;314(5803):1292-5 PMID: 17124320
  18. An analysis of maleless and histone H4 acetylation in Drosophila melanogaster spermatogenesis.
    Mech Dev. 1998 Feb;71(1-2):107-17 PMID: 9507080
  19. Meiotic sex chromosome inactivation.
    Development. 2007 May;134(10):1823-31 PMID: 17329371
  20. DIVERGENCE OF MEIOTIC DRIVE-SUPPRESSION SYSTEMS AS AN EXPLANATION FOR SEX-BIASED HYBRID STERILITY AND INVIABILITY.
    Evolution. 1991 Mar;45(2):262-267 PMID: 28567880
  21. GENETICS OF STERILITY IN HYBRIDS BETWEEN TWO SUBSPECIES OF DROSOPHILA.
    Evolution. 1989 Jan;43(1):180-189 PMID: 28568487
  22. Meiotic pairing constraints and the activity of sex chromosomes.
    J Theor Biol. 1988 Jul 8;133(1):23-36 PMID: 3226141
  23. Dominance, epistasis and the genetics of postzygotic isolation.
    Genetics. 2000 Apr;154(4):1663-79 PMID: 10747061
  24. Evolution on the X chromosome: unusual patterns and processes.
    Nat Rev Genet. 2006 Aug;7(8):645-53 PMID: 16847464
  25. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes.
    Genetics. 2003 Aug;164(4):1383-97 PMID: 12930747
  26. Sex-ratio segregation distortion associated with reproductive isolation in Drosophila.
    Proc Natl Acad Sci U S A. 2001 Nov 6;98(23):13183-8 PMID: 11687638
  27. Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus.
    PLoS Biol. 2004 Jun;2(6):e142 PMID: 15208709
  28. Sex chromosomes, recombination, and chromatin conformation.
    Chromosoma. 1993 Jan;102(2):71-80 PMID: 8432196
  29. A rapidly evolving homeobox at the site of a hybrid sterility gene.
    Science. 1998 Nov 20;282(5393):1501-4 PMID: 9822383
  30. Causes of sex ratio bias may account for unisexual sterility in hybrids: a new explanation of Haldane's rule and related phenomena.
    Genetics. 1991 Aug;128(4):841-58 PMID: 1916248
  31. The genetic basis of Haldane's rule.
    Nature. 1985 Apr 25-May 1;314(6013):736-8 PMID: 3921852
  32. X-chromosome inactivation during spermatogenesis is regulated by an Xist/Tsix-independent mechanism in the mouse.
    Genesis. 2002 Dec;34(4):257-66 PMID: 12434336
  33. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila.
    Nature. 2003 Jun 12;423(6941):715-9 PMID: 12802326
  34. Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome.
    Mol Biol Evol. 2002 Jun;19(6):918-25 PMID: 12032248
  35. Genes and speciation.
    Nat Rev Genet. 2004 Feb;5(2):114-22 PMID: 14735122
  36. Excess of amino acid substitutions relative to polymorphism between X-linked duplications in Drosophila melanogaster.
    Mol Biol Evol. 2005 Feb;22(2):273-84 PMID: 15483321
  37. Species-specific positive selection of the male-specific lethal complex that participates in dosage compensation in Drosophila.
    Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15412-7 PMID: 17878295
  38. Genome-wide patterns of expression in Drosophila pure species and hybrid males.
    Mol Biol Evol. 2003 Jul;20(7):1070-6 PMID: 12777520
  39. Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution.
    Genome Res. 2005 Jan;15(1):1-18 PMID: 15632085
  40. A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter.
    PLoS Biol. 2007 Nov 6;5(11):e293 PMID: 17988173
  41. The evolution of F1 postzygotic incompatibilities in birds.
    Evolution. 2002 Oct;56(10):2083-9 PMID: 12449494
  42. Asymmetric postmating isolation: Darwin's corollary to Haldane's rule.
    Genetics. 2007 Jun;176(2):1059-88 PMID: 17435235
  43. Sex chromosomes and speciation.
    Proc Biol Sci. 1991 Mar 22;243(1308):203-8 PMID: 1675798
  44. The evolution of sex-biased genes and sex-biased gene expression.
    Nat Rev Genet. 2007 Sep;8(9):689-98 PMID: 17680007
  45. Dosage compensation: the beginning and end of generalization.
    Nat Rev Genet. 2007 Jan;8(1):47-57 PMID: 17173057
  46. A sex-ratio meiotic drive system in Drosophila simulans. I: an autosomal suppressor.
    PLoS Biol. 2007 Nov 6;5(11):e292 PMID: 17988172
  47. A genomic comparison of faster-sex, faster-X, and faster-male evolution between Drosophila melanogaster and Drosophila pseudoobscura.
    J Mol Evol. 2006 Jun;62(6):693-700 PMID: 16612543
  48. Segregation distorters.
    Annu Rev Genet. 1991;25:511-57 PMID: 1812815
  49. Sex chromosome silencing in the marsupial male germ line.
    Proc Natl Acad Sci U S A. 2007 Jun 5;104(23):9730-5 PMID: 17535928
  50. The role of X-chromosome inactivation during spermatogenesis (Drosophila-allocycly-chromosome evolution-male sterility-dosage compensation).
    Proc Natl Acad Sci U S A. 1972 Jan;69(1):182-6 PMID: 4621547
  51. X chromosomes and autosomes evolve at similar rates in Drosophila: no evidence for faster-X protein evolution.
    Genome Res. 2006 Apr;16(4):498-504 PMID: 16520459
  52. 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
  53. Genetics and speciation.
    Nature. 1992 Feb 6;355(6360):511-5 PMID: 1741030
  54. Demasculinization of X chromosomes in the Drosophila genus.
    Nature. 2007 Nov 8;450(7167):238-41 PMID: 17994090
  55. Global analysis of X-chromosome dosage compensation.
    J Biol. 2006;5(1):3 PMID: 16507155
  56. Evolution of postmating reproductive isolation: the composite nature of Haldane's rule and its genetic bases.
    Am Nat. 1993 Aug;142(2):187-212 PMID: 19425975
  57. The weaker sex is heterogametic: 75 years of Haldane's rule.
    Genetics. 1997 Nov;147(3):937-51 PMID: 9383043
  58. 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
  59. Speciation in Drosophila: from phenotypes to molecules.
    J Hered. 2007 Mar-Apr;98(2):103-10 PMID: 17194791
  60. X-chromosome silencing in the germline of C. elegans.
    Development. 2002 Jan;129(2):479-92 PMID: 11807039
  61. An empirical test of the meiotic drive models of hybrid sterility: sex-ratio data from hybrids between Drosophila simulans and Drosophila sechellia.
    Genetics. 1992 Mar;130(3):507-11 PMID: 1551573
  62. Recombination enhances protein adaptation in Drosophila melanogaster.
    Curr Biol. 2005 Sep 20;15(18):1651-6 PMID: 16169487
  63. Hybrid sterility in the mouse.
    Trends Genet. 1996 Oct;12(10):412-7 PMID: 8909138
  64. Adaptive protein evolution of X-linked and autosomal genes in Drosophila: implications for faster-X hypotheses.
    Mol Biol Evol. 2007 Nov;24(11):2566-72 PMID: 17884828
  65. Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura.
    Genetics. 2005 Feb;169(2):671-82 PMID: 15654115
Article Info
Journal
Trends in genetics : TIG
Abbr.
Trends Genet
ISSN
0168-9525
DOI
10.1016/j.tig.2008.04.007
Email
[email protected]
Published
2008-07-00
Pages
336-43
Language
English
Region
England
NLM ID
8507085
PMCID
PMC2819171
Subset
IM
Grants
NIGMS NIH HHS · R01 GM079543 · United States
NIGMS NIH HHS · R01 GM079543-02 · United States
NIGMS NIH HHS · GM 79543 · United States
External Links
PubMed source DOI: 10.1016/j.tig.2008.04.007 PMC Full Text View journal details
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