High-resolution genome-wide dissection of the two rules of speciation in Drosophila

PLoS Biology

Volumn 5, Issue 9, 2007, Pages 1890-1898

  Masly, John P ^a,b   Presgraves, Daven C ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; AUTOSOMAL INHERITANCE; CHROMOSOME; CONTROLLED STUDY; DISSECTION; DOMINANT GENE; DROSOPHILA; DROSOPHILA MAURITIANA; DROSOPHILA SECHELLIA; FEMALE; GENETIC INCOMPATIBILITY; GENOME; HYBRID; INTROGRESSION; MALE; MALE STERILITY; NONHUMAN; RECESSIVE GENE; X CHROMOSOME LINKAGE; ANIMAL; GENETICS; SPECIES DIFFERENTIATION; X CHROMOSOME;

DROSOPHILA MAURITIANA; DROSOPHILA SECHELLIA;

ANIMALS; CHROMOSOMES; DROSOPHILA; GENETIC SPECIATION; GENOME; MALE; X CHROMOSOME;

EID: 34548694295     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0050243     Document Type: Article

References (88)

1. Dobzhansky T (1937) Genetics and the origin of species. New York: Columbia University Press. 364 p.
2. Mayr E (1942) Systematics and the origin of species. New York: Columbia University Press. 334 p.
3. Muller HJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6: 71-125.
4. Coyne JA, Orr HA (2004) Speciation. Sunderland (Massachusetts): Sinauer Associates. 545 p.
5. Coyne JA, Orr HA (1989) Two rules of speciation. In: Otte D, Endler J, editors. Speciation and its consequences. Sunderland (Massachusetts): Sinauer Associates. pp. 180-207.
6. Haldane JBS (1922) Sex ratio and unisexual sterility in animal hybrids. J Genet 12: 101-109.
7. Coyne JA (1992) Genetics and speciation. Nature 355: 511-515.
8. Wu CI, Davis AW (1993) Evolution of postmating reproductive isolation: The composite nature of Haldane's rule and its genetic bases. Am Nat 142: 187-212.
9. Laurie CC (1997) The weaker sex is heterogametic: 75 years of Haldane's rule. Genetics 147: 937-951.
10. Orr HA (1997) Haldane's rule. Ann Rev Ecol Syst 28: 195-218.
11. Presgraves DC (2002) Patterns of poszygotic isolation in Lepidoptera. Evolution 56: 1168-1183.
12. 1 post-zygotic incompatibilities in birds. Evolution 56: 2083-2089.
13. Muller HJ (1940) Bearing of the Drosophila work on systematics In: Huxley JS, editor. The new systematics. Oxford (United Kingdom): Clarendon Press. pp. 185-268.
14. Orr HA (1993) A mathematical model of Haldane's rule. Evolution 47: 1606-1611.
15. Turelli M, Orr HA (1995) The dominance theory of Haldane's rule. Genetics 140: 389-402.
16. Turelli M, Orr HA (2000) Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154: 1663-1679.
17. Muller HJ, Pontecorvo G (1942) Recessive genes causing interspecific sterility and other disharmonies between Drosophila melanogaster and simulans. Genetics 27: 157.
18. Orr HA (1992) Mapping and characterization of a 'speciation gene' in Drosophila. Genet Res 59: 73-80.
19. Davis AW, Noonburg EG, Wu CI (1994) Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade. Genetics 137: 191-199.
20. Breeuwer JAJ, Werren JH (1995) Hybrid breakdown between two haplodiploid species: The role of nuclear and cytoplasmic genes. Evolution 49: 705-717.
21. True JR, Weir BS, Laurie CC (1996) A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142: 819-837.
22. Hollocher H, Wu CI (1996) The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics 143: 1243-1255.
23. Coyne JA, Simeonidis S, Rooney P (1998) Relative paucity of gene causing hybrid inviability in hybrids between Drosophila melanogaster and D. simulans. Genetics 150: 1091-1103.
24. Sawamura K, Davis AW, Wu CI (2000) Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc Nat Acad Sci U S A 97: 2652-2655.
25. Presgraves DC (2003) A fine scale analysis of hybrid incompatibilities in Drosophila. Genetics 163: 955-972.
26. Tao Y, Chen S, Hartl DL, Laurie CC (2003) 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 164: 1383-1397.
27. Masly JP, Jones CD, Noor MAF, Locke J, Orr HA (2006) Gene transposition as a cause of hybrid sterility in Drosophila. Science 313: 1448-1450.
28. Turelli M, Begun DJ (1997) Haldane's rule and X-chromosome size in Drosophila. Genetics 147: 1799-1815.
29. Presgraves DC, Orr HA (1998) Haldane's rule in taxa lacking a hemizygous X. Science 282: 952-954.
30. Wu CI, Johnson NA, Palopoli MF (1996) Haldane's rule and its legacy: Why are there so many sterile males? Trends Ecol Evol 11: 281-284.
31. Tao Y, Hartl DL (2003) Genetic dissection of hybrid incompatibilities between Drosophila simulans and Drosophila mauritiana. III. Heterogeneous accumulation of hybrid incompatibilities, degree of dominance and implications for Haldane's rule. Evolution 57: 2580-2598.
32. 1 hybrids between Drosophila pseudoobscura and D. persimilis. BMC Evol Biol 2: 16.
33. Michalak P, Noor MAF (2003) Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol Biol Evol 20: 1070-1076.
34. Ranz JM, Namgyal K, Gibson G, Hartl DL (2004) Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. Genome Res 14: 373-379.
35. Charlesworth B, Coyne JA, Barton NH (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113-146.
36. Betancourt AJ, Presgraves DC, Swanson W (2002) A test for faster X evolution in Drosophila. Mol Biol Evol 19: 1816-1819.
37. Thornton K, Bachtrog D, Andolfatto P (2006) X chromosomes and autosomes evolve at similar rates in Drosophila: No evidence for faster-X protein evolution. Genome Res 16: 498-504.
38. Frank SH (1991) Divergence of meiotic drive suppression systems as an explanation for sex-biased hybrid sterility and inviability. Evolution 45: 262-267.
39. Hurst LD, Powmiankowski A (1991) Causes of sex-ratio bias may account for unisexuality in hybrids: A new explanation of Haldane's rule and related phenomena. Genetics 128: 841-858.
40. Malik HS, Henikoff S (2001) Adaptive evolution of Cid, a centromere-specific histone in Drosophila. Genetics 157: 1293-1298.
41. Tao Y, Hartl DL, Laurie CC (2001) Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc Nat Acad Sci U S A 98: 13183-13188.
42. Henikoff S, Ahmad K, Malik HS (2001) The centromere paradox: Stable inheritance with rapidly evolving DNA. Science 293: 1098-1102.
43. Turelli M, Moyle LC (2007) Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176: 1059-1088.
44. Orr HA (1993) Haldane's rule has multiples genetic causes. Nature 361: 532-533.
45. Crow JF (1942) Cross fertility and isolating mechanisms in the Drosophila mulleri group. Univ Texas Pub 4228: 53-67.
46. Patterson JT, Griffen RK (1944) The genetic mechanism underlying species isolation. Univ Texas Pub 4445: 212-223.
47. Detlefsen JA (1914) Genetic studies on a cavy species cross. Carnegie Inst Wash Pub 205: 1-134.
48. Dobzhansky T (1936) Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21: 113-135.
49. Sturtevant AH, Novitski E (1941) Sterility in crosses of geographical races of Drosophila micromelanica. Proc Nat Acad Sci U S A 27: 392-394.
50. Dobzhansky T (1974) Genetic analysis of hybrid sterility within the species Drosophila pseudoobscura. Hereditas 77: 81-88.
51. Grula JW, Taylor OR (1980) Some characteristics of hybrids derived from the sulfur butterflies Colias eurytheme and C. philodice: Phenotypic effects of the X-chromosome. Evolution 34: 673-687.
52. Curtis CF (1982) The mechanism of hybrid male sterility from crosses in the in Anopheles gambiae and Glossina morsitans complexes. In: Steiner WMF, editor. Recent developments of insect disease vectors. New York: Stipes Publishing. pp. 290-312.
53. Coyne JA, Kreitman M (1984) Evolutionary genetics of two sibling species, Drosophila simulans and D. sechellia. Evolution 40: 673-691.
54. Coyne JA (1985) Genetic studies of three sibling species of Drosophila with relationship to theories of speciation. Genet Res 46: 169-192.
55. Naveira H, Fontdevila A (1986) 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 114: 841-857.
56. Orr HA (1987) Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics 116: 555-563.
57. Zouros E, Lofdahl K, Martin PA (1988) Male hybrid sterility in Drosophila: Interactions between autosomes and sex chromosomes in crosses of D. mohavensis and D. arizonensis. Evolution 42: 1321-1331.
58. Coyne JA, Orr HA (1997) "Patterns of speciation in Drosophila" revisited. Evolution 51: 295-303.
59. Hagen RH, Scriber JM (1989) Sex-linked diapause, color, and allozyme loci in Papilio glaucus: Linkage analysis and significance in a hybrid zone. J Hered 80: 179-185.
60. Tucker PK, Sage RD, Warner J, Wilson AC, Eicher EM (1992) Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution 46: 1146-1163.
61. Dod B, Jermiin LS, Boursot P, Chapman VH, Nielsen JT, et al. (1993) Counterselection on sex chromosomes in the Mus musculus European hybrid zone. J Evol Biol 6: 529-546.
62. Machado CA, Kliman RM, Markert JA, Hey J (2002) Inferring the history of speciation from multilocus DNA sequence data: The case of Drosophila pseudoobscura and close relatives. Mol Biol Evol 19: 472-488.
63. Saetre GP, Borge T, Lindroos K, Haavbie J, Sheldon BC, et al. (2003) Sex chromosome evolution and speciation in flycatchers. Proc R Soc Lond B Biol Sci 270: 53-59.
64. Paysuer BA, Krenz JG, Nachman MW (2004) Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mouse. Evolution 58: 2064-2078.
65. Naveira HF (1992) Location of X-linked polygenic effects causing sterility in male hybrids of Drosophila simulans and D. mauritiana. Heredity 68: 211-217.
66. Perez DE, Wu CI, Johnson NA, Wu ML (1993) Genetics of reproductive isolation in the Drosophila simulans clade: DNA-marker assisted mapping and characterization of a hybrid-male sterility gene, Odysseus (Ods). Genetics 134: 261-275.
67. Cabot EL, Davis AW, Johnson NA, Wu CI (1994) Genetics of reproductive isolation in the Drosophila simulans clade: Complex epistasis underlying hybrid male sterility. Genetics 137: 175-189.
68. Perez DE, Wu CI (1995) Further characterization of the Odysseus locus of hybrid sterility in Drosophila: One gene is not enough. Genetics 140: 201-206.
69. Davis AW, Wu CI (1996) The broom of the sorcerer's apprentice: The fine structure of a chromosomal region causing reproductive isolation between two sibling species of Drosophila. Genetics 143: 1287-1298.
70. Kliman RM, Andolfatto P, Coyne JA, Depaulis F, Kreitman M, et al. (2000) The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156: 1913-1931.
71. Coyne JA (1989) Mutation rates in hybrids between sibling species of Drosophila. Heredity 63: 155-162.
72. Lindsley DL, Tokuyasu KT (1980) Spermatogenesis. In: Ashburner M, Wright TRF, editors. The genetics and biology of Drosophila, Volume 2d. New York: Academic Press. pp. 225-294.
73. Cooley L, Berg C, Spradling A (1988) Controlling P element insertional mutagenesis. Trends Genet 4: 254-258.
74. True JR, Mercer JM, Laurie CC (1996) Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics 142: 507-523.
75. Coyne JA, Berry A (1994) Effects of the fourth chromosome on the sterility of hybrids between Drosophila simulans and its relatives. J Hered 85: 224-227.
76. Coyne JA, Rux J, David JR (1991) Genetics of morphological differences and hybrid sterility between Drosophila sechellia and its relatives. Genet Res 57: 113-122.
77. Lindsley DL, Lifschytz E (1972) The genetic control of spermatogenesis in Drosophila. In: Beatty RA, Gluecksohn-Waelsch S, editors. Proceedings of the International Symposium on the Genetics of the Spermatozoon. Copenhagen: Bogtrykkeriet Forum. pp. 203-221.
78. Parisi M, Nuttall R, Naiman D, Bouffard G, Malley J, et al. (2003) Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299: 697-700.
79. Bauer VL, Aquadro CF (1997) Rates of DNA sequence evolution are not sex-biased in Drosophila melanogaster and D. simulans. Mol Biol Evol 14: 1252-1257.
80. Orr HA (1995) The population genetics of speciation: The evolution of hybrid incompatibilities. Genetics 139: 1805-1813.
81. Hauschteck-Jungen E (1990) Postmating reproductive isolation and modification of the 'sex ratio' trait in Drosophila subobscura induced by the sex chromosome gene arrangement A2+3+5+7. Genetica 83: 31-44.
82. Orr HA, Irving S (2005) Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169: 671-682.
83. Jaenike J (2001) Sex chromosome meiotic drive. Ann Rev Ecol Syst 32: 25-49.
84. Lucchesi JC (1998) Dosage compensation in flies and worms: The ups and downs of X-chromosome regulation. Curr Opin Genet Dev 8: 179-184.
85. Orr HA (1989) Does postzygotic isolation result from improper dosage compensation? Genetics 122: 891-894.
86. Gupta V, Parisi M, Sturgill D, Nuttall R, Doctolero M, et al. (2006) Global analysis of X-chromsome dosage compensation. J Biol 5: 3.
87. Lifschytz E, Lindsley DL (1972) The role of X-chromosome inactivation during spermatogenesis. Proc Nat Acad Sci U S A 69: 182-186.
88. Benson G (1999) Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acid Res 27: 573-580.