The Drosophila melanogaster Hybrid male rescue gene causes inviability in male and female species hybrids

Genetics

Volumn 154, Issue 4, 2000, Pages 1747-1771

  Barbash, Daniel A ^a   Roote, John ^a   Ashburner, Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; DROSOPHILA MELANOGASTER; FEMALE; FEMALE STERILITY; GENE MAPPING; GENE MUTATION; HYBRIDIZATION; LETHALITY; MALE; MALE STERILITY; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE; TEMPERATURE SENSITIVITY;

ANIMALS; DROSOPHILA MELANOGASTER; FEMALE; GENE DELETION; GENE DUPLICATION; GENES, DOMINANT; GENES, LETHAL; HEAT; HYBRIDIZATION, GENETIC; MALE; SPECIES SPECIFICITY;

DROSOPHILA MAURITIANA; DROSOPHILA MELANOGASTER; DROSOPHILA SECHELLIA; DROSOPHILA SIMULANS; MELANOGASTER;

EID: 0034036460     PISSN: 00166731     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (67)

1. ARTAVANIS-TSAKONAS, S., M. D. RAND and R. J. LAKE, 1999 Notch signaling: cell fate control and signal integration in development. Science 284: 770-776.
2. ASHBURNER, M., 1989 Drosophila: A Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. BAINBRIDGE, S. P., and M. BOWNES, 1981 Staging the metamorphosis of Drosophila melanogaster. J. Embryol. Exp. Morphol. 66: 57-80.
4. BIDDLE, R. L., 1932 The bristles of hybrids between Drosophila melanogaster and Drosophila simulans. Genetics 17: 153-174.
5. CACCONE, A., E. N. MORIYAMA, J. M. GLEASON, L. NIGRO and J. R. POWELL, 1996 A molecular phylogeny for the Drosophila melanogaster subgroup and the problem of polymorphism data. Mol. Biol. Evol. 13: 1224-1232.
6. CARVAJAL, A. R., M. R. GANDARELA and H. F. NAVEIRA, 1996 A three-locus system of interspecific incompatibility underlies male instability in hybrids between Drosophila buzzalii and D. koepferae. Genetica 98: 1-19.
7. COYNE, J. A., 1983 Genetic basis of differences in genital morphology among three sibling species of Drosophila. Evolution 37: 1101-1118.
8. COYNE, J. A., 1985 The genetic basis of Haldane's rule. Nature 314: 736-738.
9. COYNE, J. A., 1992 Genetics and speciation. Nature 355: 511-515.
10. COYNE, J. A., and H. A. ORR, 1998 The evolutionary genetics of speciation. Phil. Trans. R. Soc. Lond. Ser. B 353: 287-305.
11. COYNE, J. A., S. SIMEONIDIS and P. ROONEY, 1998 Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans. Genetics 150: 1091-1103.
12. DAVIS, A. W., J. ROOTE, T. MORLEY, K. SAWAMURA, S. HERRMANN et al., 1996 Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature 380: 157-159.
13. DOBZHANSKY, T., 1937 Genetics and the Origin of Species. Columbia University Press, New York.
14. FLYBASE, 1999 The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res. 27: 85-88 (available from http://flybase.bio.indiana.edu).
15. FREEMAN, M., 1998 Complexity of EGF receptor signalling revealed in Drosophila. Curr. Opin. Genet. Dev. 8: 407-411.
16. HALDANE, J. B. S., 1922 Sex ratio and unisexual sterility in hybrid animals. J. Genetics 12: 101-109.
17. HOLLOCHER, H., and C.-I. WU, 1996 Genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. Genetics 143: 1243-1255.
18. HUTTER, P., 1997 Genetics of hybrid inviability in Drosophila. Adv. Genet. 36: 157-185.
19. HUTTER, P., and M. ASHBURNER, 1987 Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327: 331-333.
20. HUTTER, P., and F. KARCH, 1994 Molecular analysis of a candidate gene for the reproductive isolation between sibling species of Drosophila. Experientia 50: 749-762.
21. HUTTER, P., J. ROOTE and M. ASHBURNER, 1990 A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics 124: 909-920.
22. JOLY, D., C. BAZIN, L.-W. ZENG and R. S. SINGH, 1997 Genetic basis of sperm and testis length differences and epistatic effect on hybrid inviability and sperm motility between Drosophila simulans and D. sechellia. Heredity 78: 354-362.
23. KERKIS, J., 1933a Development of gonads in hybrids between Drosophila melanogaster and Drosophila simulans. J. Exp. Zool. 66: 477-509.
24. KERKIS, J., 1933b Einfluss der Temperatur auf die Entwicklung der Hybriden von Drosophila melanogaster X Drosophila simulans. Wilhelm Roux' Arch. Entwicklungsmech. Org. 130: 1-10.
25. LACHAISE, D., J. R. DAVID, F. LEMEUNIER, L. TSACAS and M. ASHBURNER, 1986 The reproductive relationships of Drosophila sechellia with Drosophila mauritiana, Drosophila simulans and Drosophila melanogaster from the Afrotropical region. Evolution 40: 262-271.
26. LAURIE, C. C., 1997 The weaker sex is heterogametic: 75 years of Haldane's rule. Genetics 147: 937-951.
27. LEE, W. H., 1978 Temperature sensitive viability of hybrids between Drosophila melanogaster and D. simulans. Jpn. J. Genet. 53: 339-344.
28. LEMEUNIER, F., J. DAVID, L. TSACAS and M. ASHBURNER, 1986 The melanogaster species group, pp. 147-256 in The Genetics and Biology of Drosophila, Vol. 3e, edited by M. ASHBURNER, H. L. CARSON and J. N. THOMPSON. Academic Press, London.
29. LINDSLEY, D. L., and G. G. ZIMM, 1992 The Genome of Drosophila melanogaster. Academic Press, San Diego.
30. MASIDE, X. R., J. P. BARRAL and H. F. NAVEIRA, 1998 Hidden effects of Xchromosome introgressions on spermatogenesis in Drosophila simulans X D. mauritiana hybrids unveiled by interactions among minor genetic factors. Genetics 150: 745-754.
31. MAYR, E., 1942 Systematics and the Origins of Species. Columbia University Press, New York.
32. MULLER, H. J., 1940 Bearings of the 'Drosophila' work on systematics., pp. 185-268 in The New Systematics, edited by J. HUXLEY. The Clarendon Press, Oxford.
33. MULLER, H. J., 1942 Isolating mechanisms, evolution and temperature. Biol. Symp. 6: 71-125.
34. ORR, H. A., 1993a Haldane's rule has multiple genetic causes. Nature 361: 532-533.
35. ORR, H. A., 1993b A mathematical model of Haldane's rule. Evolution 47: 1606-1611.
36. ORR, H. A., 1996 The unexpected recovery of hybrids in a Drosophila species cross: a genetic analysis. Genet. Res. 67: 11-18.
37. ORR, H. A., 1997 Haldane's rule. Annu. Rev. Ecol. Syst. 28: 195-218.
38. ORR, H. A., 1999 Does hybrid lethality depend on sex or genotype? Genetics 152: 1767-1769.
39. ORR, H. A., L. D. MADDEN, J. A. COYNE, R. GOODWIN and R. S. HAWLEY, 1997 The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics 145: 1031-1040.
40. PONTECORVO, G., 1943 Viability interactions between chromosomes of Drosophila melanogaster and Drosophila simulans. J. Genet. 45: 51-66.
41. PRESGRAVES, D. C., and H. A. ORR, 1998 Haldane's rule in taxa lacking a hemizygous X. Science 282: 952-954.
42. PROVINE, W. B., 1991 Alfred Henry Sturtevant and crosses between Drosophila melanogaster and Drosophila simulans. Genetics 129: 1-5.
43. SAWAMURA, K., 2000 Genetics of hybrid inviability and sterility in Drosophila: the D. melanogaster-D. simulans case. Plant Species Biol. (in press).
44. SAWAMURA, K., and M.-T. YAMAMOTO, 1993 Cytogenetical localization of Zygotic hybrid rescue (Zhr), a Drosophila melanogaster gene that rescues interspecific hybrids from embryonic lethality. Mol. Gen. Genet. 239: 441-449.
45. SAWAMURA, R., T. TAIRA and T. K. WATANABE, 1993a Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybris rescue (mhr) gene of Drosophila simulans. Genetics 133: 299-305.
46. SAWAMURA, K., T. K. WATANABE and M.-T. YAMAMOTO, 1993b Hybrid lethal systems in the Drosophila melanogaster species complex. Genetica 88: 175-185.
47. SAWAMURA, K., M.-T. YAMAMOTO and T. K. WATANABE, 1993c Hybrid lethal systems in the Drosophila melanogaster species complex. II. The Zygotic hybrid rescue (Zhr) gene of Drosophila melanogaster. Genetics 133: 307-313.
48. SECOMBE, J., J. PISPA, R. SAINT and H. RICHARDSON, 1998 Analysis of a Drosophila cyclin E hypomorphic mutation suggests a novel role for cyclin E in cell proliferation control during eye imaginal disc development. Genetics 149: 1867-1882.
49. STURTEVANT, A. H., 1919 A new species closely resembling Drosophila melanogaster. Psyche 26: 153-155.
50. STURTEVANT, A. H., 1920 Genetic studies of Drosophila simulans. I. Introduction: hybrids with Drosophila melanogaster. Genetics 5: 488-500.
51. STURTEVANT, A. H., 1929 The genetics of Drosophila simulans. Carnegie Inst. Washington Publ. 399: 1-62.
52. STURTEVANT, A. H., and G. W. BEADLE, 1936 The relations of inversions in the X chromosome of Drosophila melanogaster to crossing over and disjunction. Genetics 21: 554-604.
53. TAKAMURA, T., and T. K. WATANABE, 1980 Further studies on the Lethal hybrid rescue (Lhr) gene of Drosophila simulans. Jpn. J. Genet. 55: 405-408.
54. TAKANO, T. S., 1998 Loss of notum macrochaetae as an interspecific hybrid anomaly between Drosophila melanogaster and D. simulans. Genetics 149: 1435-1450.
55. TING, C.-T., S.-C. TSAUR, M.-L. WU and C.-I. WU, 1998 A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282: 1501-1504.
56. TRUE, J. R., B. S. WEIR and C. C. LAURIE, 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.
57. TURELLI, M., and D. J. BEGUN, 1997 Haldane's rule and X-chromosome size in Drosophila. Genetics 147: 1799-1815.
58. TURELLI, M., and H. A. ORR, 1995 The dominance theory of Haldane's rule. Genetics 140: 389-402.
59. WADE, M. J., N. A. JOHNSON, R. JONES, V. SIGUEL and M. MCNAUGHTON, 1997 Genetic variation segregating in natural populations of Tribolium castaneum affecting traits observed in hybrids with T. freemani. Genetics 147: 1235-1247.
60. WATANABE, T. K., 1979 A gene that rescues the lethal hybrids between Drosophila melanogaster and Drosophila simulans. Jpn. J. Genet. 54: 325-331.
61. WATANABE, T. K., W. H. LEE, Y. INOUE and M. KAWANISHI, 1977 Genetic variation of the hybrid crossability between Drosophila melanogaster and D. simulans. Jpn. J. Genet. 52: 1-8.
62. WHITE-COOPER, H., M. CARMENA, C. GONZALEZ and D. M. GLOVER, 1996 Mutations in new cell cycle genes that fail to complement a multiply mutant third chromosome of Drosophila. Genetics 144: 1097-1111.
63. WU, C.-I., and A. W. DAVIS, 1993 Evolution of postmating reproductive isolation: the composite nature of Haldane's rule and its genetic bases. Am. Nat. 142: 187-212.
64. WU, C.-I., and M. F. PALOPOLI, 1994 Genetics of postmating reproductive isolation in animals. Annu. Rev. Genet. 27: 282-308.
65. WU, C.-I., N. A. JOHNSON and M. F. PALOPOLI, 1996 Haldane's rule and its legacy: Why are there so many sterile males? Trends Ecol. Evol. 11: 281-284.
66. YAMAMOTO, M.-T., 1992 Inviability of hybrids belween D. melanogaster and D. simulans results from the absence of simulans X not the presence of simulans Y chromosome. Genetica 87: 151-158.
67. ZHANG, Y. Q., J. ROOTE, S. BROGNA, A. W. DAVIS, D. A. BARBASH et al., 1999 stress sensitive B encodes an adenine nucleotide translocase in Drosophila melanogaster. Genetics 153: 891-903.