Variable post-zygotic isolation in Drosophila melanogaster/D. simulans hybrids

Journal of Evolutionary Biology

Volumn 27, Issue 8, 2014, Pages 1691-1705

  Matute, D R ^a   Gavin Smyth, J ^a   Liu, G ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Hybrid inviability; Hybrid sterility; Post zygotic isolation

Indexed keywords

DIVERGENCE; FLY; GENETIC ANALYSIS; GENETIC VARIATION; HYBRID; HYBRIDIZATION; MUTATION; PHENOTYPE; POLYMORPHISM; REPRODUCTIVE ISOLATION;

DROSOPHILA MELANOGASTER; DROSOPHILA SECHELLIA; DROSOPHILA SIMULANS;

4',6 DIAMIDINO 2 PHENYLINDOLE; DROSOPHILA PROTEIN; HYBRID MALE RESCUE PROTEIN, DROSOPHILA; INDOLE DERIVATIVE; LHR PROTEIN, DROSOPHILA;

ANATOMY AND HISTOLOGY; ANIMAL; CROSS BREEDING; CYTOLOGY; DNA SEQUENCE; DROSOPHILA MELANOGASTER; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; GERM CELL; HYBRIDIZATION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OVARY; POPULATION GENETICS; REPRODUCTIVE ISOLATION;

ANIMALS; BASE SEQUENCE; CROSSES, GENETIC; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS, POPULATION; GENOTYPE; GERM CELLS; HYBRIDIZATION, GENETIC; INDOLES; MOLECULAR SEQUENCE DATA; OVARY; POLYMORPHISM, GENETIC; REPRODUCTIVE ISOLATION; SEQUENCE ANALYSIS, DNA;

EID: 84904425050     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12422     Document Type: Article

References (89)

1. Aruna, S., Flores, H.A. & Barbash, D.A. 2009. Reduced fertility of Drosophila melanogaster Hybrid male rescue (Hmr) mutant females is partially complemented by Hmr orthologs from sibling species. Genetics 181: 1437-1450.
2. Barbash, D.A. 2007. Nup96-dependent hybrid lethality occurs in a subset of species from the simulans clade of Drosophila. Genetics 176: 543-552.
3. Barbash, D.A. & Ashburner, M. 2003. A novel system of fertility rescue in Drosophila hybrids reveals a link between hybrid lethality and female sterility. Genetics 163: 217-226.
4. Barbash, D.A., Roote, J. & Ashburner, M. 2000. The Drosophila melanogaster hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154: 1747-1771.
5. Barbash, D.A., Awadalla, P. & Tarone, A.M. 2004. Functional divergence caused by ancient positive selection of a Drosophila hybrid incompatibility locus. PLoS Biol. 2: e142.
6. Begun, D.J., Holloway, A.K., Stevens, K., Hillier, L.W., Poh, Y.-P., Hahn, M. et al. 2007. Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans. PLoS Biol. 5: e310.
7. Brideau, N.J., Flores, H.A., Wang, J., Maheshwari, S., Wang, X. & Barbash, D.A. 2006. Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314: 1292-1295.
8. Capy, P. & Gibert, P. 2004. Drosophila melanogaster, Drosophila simulans: so similar yet so different. Genetica 120: 5-16.
9. Chandler, C.H., Chari, S. & Dworkin, I. 2013. Does your gene need a background check? How genetic background impacts the analysis of mutations, genes, and evolution. Trends Genet. 29: 358-366.
10. Chari, S. & Dworkin, I. 2013. The conditional nature of genetic interactions: the consequences of wild-type backgrounds on mutational interactions in a genome-wide modifier screen. PLoS Genet. 9: e1003661.
11. Coyne, J.A. & Orr, H.A. 2004. Speciation. Sinauer Associates, Sunderland, MA.
12. Coyne, J.A., Simeonidis, S. & Rooney, P. 1998. Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans. Genetics 150: 1091-1103.
13. Cutter, A.D. 2012. The polymorphic prelude to Bateson-Dobzhansky-Muller incompatibilities. Trends Ecol. Evol. 27: 209-218.
14. David, J.R., Lemeunier, F., Tsacas, L. & Yassin, A. 2007. The historical discovery of the nine species in the Drosophila melanogaster species subgroup. Genetics 177: 1969-1973.
15. Davis, A.W., Roote, J., Morley, T., Sawamura, K., Herrmann, S. & Ashburner, M. 1996. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature 380: 157-159.
16. Demuth, J.P. & Wade, M.J. 2005. On the theoretical and empirical framework for studying genetic interactions within and among species. Am. Nat. 165: 524-536.
17. Dobzhansky, T. 1937. Genetics and the Origin of Species. Columbia University Press, New York.
18. Dworkin, I., Kennerly, E., Tack, D., Hutchinson, J., Brown, J., Mahaffey, J. et al. 2009. Genomic consequences of background effects on scalloped mutant expressivity in the wing of Drosophila melanogaster. Genetics 181: 1065-1076.
19. Ferree, P.M. & Barbash, D.A. 2009. Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol. 7: e1000234.
20. Fierst, J.L. & Hansen, T.F. 2010. Genetic architecture and post-zygotic reproductive isolation: Bateson-Dobzhansky-Muller incompatibilities in a polygenic model. Evolution 64: 675-693.
21. Fitzpatrick, B.M. 2008. Hybrid dysfunction: population genetic and quantitative genetic perspectives. Am. Nat. 171: 491-498.
22. Gérard, P.R. & Presgraves, D.C. 2012. Abundant genetic variability in Drosophila simulans for hybrid female lethality in interspecific crosses to D. melanogaster. Genet. Res. (Camb) 94: 1-7.
23. Giraudoux, P. & Giraudoux, M.P. 2013. R package 'pgirmess'. URL http://cran.r-project.org/web/packages/pgirmess/index.html.
24. Good, J.M., Handel, M.A. & Nachman, M.W. 2008. Asymmetry and polymorphism of hybrid male sterility during the early stages of speciation in house mice. Evolution 62: 50-65.
25. Granadino, B., Penalva, L.O.F. & Sánchez, L. 1996. Indirect evidence of alteration in the expression of the rDNA genes in interspecific hybrids between Drosophila melanogaster and Drosophila simulans. Mol. Gen. Genet. 250: 89-96.
26. Hayashi, T.I. & Kawata, M. 2002. How genes causing unfit hybrid evolve within population?: a review for models of postzygotic isolation. Popul. Ecol. 43: 179-188.
27. Hayashi, T.I. & Kawata, M. 2006. Impact of ancestral populations on postzygotic isolation in allopatric speciation. Popul. Ecol. 48: 121-130.
28. Hutter, P. & Ashburner, M. 1987. Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327: 331-333.
29. Hutter, P., Roote, J. & Ashburner, M. 1990. A genetic basis for the inviability of hybrids between sibling species of Drosophila. Genetics 124: 909-920.
30. Lachaise, D. & Silvain, J.-F. 2004. How two Afrotropical endemics made two cosmopolitan human commensals from Africa: the Drosophila melanogaster-D. simulans riddle. Genetica 120: 17-39.
31. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H. et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
32. Leffler, E.M., Bullaughey, K., Matute, D.R., Meyer, W., Segurel, L., Venkat, A. et al. 2012. revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol. 10: e1001388.
33. Legrand, D., Tenaillon, M.I., Matyot, P., Gerlach, J., Lachaise, D. & Cariou, M.L. 2009. Species-wide genetic variation and demographic history of Drosophila sechellia, a species lacking population structure. Genetics 182: 1197-1206.
34. Lemeunier, F., David, J., Tsacas, L. & Ashburner, M. 1986. The melanogaster species group. In: The Genetics and Biology of Drosophila, Vol. 3e. (M. Ashburner, H.L. Carson & J. Thompson, eds), pp. 147-256. Academic Press, London and New York.
35. López-Fernández, H. & Bolnick, D.I. 2007. Is partial hybrid viability due to incomplete penetrance are parents heterozygous for Dobzhansky-Muller incompatibilities? PLoS ONE 2: e1294.
36. Lynch, M. 1991. The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 45: 622-629.
37. Lynch, M. & Force, A. 2000. Gene duplication and the origin of interspecific genomic incompatibility. Am. Nat. 156: 590-605.
38. Mackay, T.F.C., Richards, S., Stone, E.A., Barbadilla, A., Ayroles, J.F., Zhu, D.H. et al. 2012. The Drosophila melanogaster genetic reference panel. Nature 482: 173-178.
39. Maheshwari, S. & Barbash, D.A. 2011. The genetics of hybrid incompatibilities. Annu. Rev. Genet. 45: 331-355.
40. Maheshwari, S. & Barbash, D.A. 2012. An indel polymorphism in the hybrid incompatibility gene Lethal hybrid rescue of Drosophila is functionally relevant. Genetics 192: 683-691.
41. Markow, T. & O'Grady, P.M. 2006. Drosophila: A Guide to Species Identification and Use. Academic Press, London, UK.
42. Masly, J.P., Jones, C.D., Noor, M.A.F. & Orr, H.A. 2006. Gene transposition as a cause of hybrid sterility. Science 313: 1448-1450.
43. Meiklejohn, C.D., Holmbeck, M.A., Siddiq, M.A., Abt, D.N., Rand, D.M. & Montooth, K.L. 2013. An incompatibility between a mitochondrial tRNA and its nuclear-encoded tRNA synthetase compromises development and fitness in Drosophila. PLoS Genet. 9: e1003238.
44. Montooth, K.L., Meiklejohn, C.D., Abt, D. & Rand, D.M. 2010. Mitochondrial-nuclear epistasis affects fitness within species but does not contribute to incompatibilities between species in Drosophila. Evolution 64: 3364-3379.
45. Moyle, L.C., Muir, C.D., Han, M.V. & Hahn, M.W. 2010. The contributions of gene movement to the "two rules of speciation". Evolution 64: 1541-1557.
46. Muller, H.J. 1942. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6: 71-125.
47. Nolte, V., Weigel, D. & Schlötterer, C. 2008. The impact of shared ancestral variation on hybrid male lethality-a 16 codon indel in the Drosophila simulans Lhr gene. J. Evol. Biol. 21: 551-555.
48. Nosil, P. 2012. Ecological Speciation. Oxford University Press, Oxford.
49. Nosil, P. & Schluter, D. 2011. The genes underlying the process of speciation. Trends Ecol. Evol. 26: 160-167.
50. Orgogozo, V. & Stern, D.L. 2009. How different are recently diverged species?: more than 150 phenotypic differences have been reported for the Drosophila melanogaster species subgroup. Fly (Austin) 3: 117.
51. Orr, H.A. 1995. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805-1813.
52. Orr, H.A. & Irving, S. 2001. Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics 158: 1089-1100.
53. Orr, H.A., Madden, L.D., Coyne, J.A., Goodwin, R. & Hawley, R.S. 1997. The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics 145: 1031-1040.
54. Orr, H.A., Masly, J.P. & Phadnis, N. 2007. Speciation in Drosophila: from phenotypes to molecules. J. Hered. 98: 103-110.
55. Perez, D.E. & Wu, C.I. 1995. Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough. Genetics 140: 201-206.
56. Presgraves, D.C. 2003. A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163: 955-972.
57. Presgraves, D.C., Balagopalan, L., Abmayr, S.M. & Orr, H.A. 2003. Adaptive evolution drives divergence of a hybrid inviability gene in Drosophila. Nature 423: 715-719.
58. R Development Core Team. 2005. R: A Language and Environment for Statistical Computing, Reference Index Version 2.2.1. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.
59. Raff, E.C., Popodi, E.M., Sly, B.J., Turner, F.R., Villinski, J.T. & Raff, R.A. 1999. A novel ontogenetic pathway in hybrid embryos between species with different modes of development. Development 126: 1937-1945.
60. Ràmia, M., Librado, P., Casillas, S., Rozas, J. & Barbadilla, A. 2012. PopDrowser: the population Drosophila browser. Bioinformatics 28: 595-596.
61. Reed, L.K. & Markow, T.A. 2004. Early events in speciation: polymorphism for hybrid male sterility in Drosophila mojavensis. Proc. Natl. Acad. Sci. USA 101: 9009-9012.
62. Reed, L.K., La Flamme, B.A. & Markow, T.A. 2008. Genetic architecture of hybrid male sterility in Drosophila: analysis of intraspecies variation for interspecies isolation. PLoS ONE 3: e3076.
63. Sanchez, L. & Dübendorfer, A. 1983. Development of imaginal discs from lethal hybrids between Drosophila melanogaster and Drosophila mauritiana. Wilhelm Roux. Arch. Dev. Biol. 192: 48-50.
64. Sawamura, K. & Tomaru, M. 2002. Biology of reproductive isolation in Drosophila: toward a better understanding of speciation. Popul. Ecol. 44: 0209-0219.
65. Sawamura, K. & Yamamoto, M. 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.
66. Sawamura, K. & Yamamoto, M.T. 1997. Characterization of a reproductive isolation gene, zygotic hybrid rescue, of Drosophila melanogaster by using minichromosomes. Heredity 79: 97-103.
67. Sawamura, K., Taira, T. & Watanabe, T.K. 1993a. Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics 133: 299-305.
68. Sawamura, K., Yamamoto, M.T. & Watanabe, T.K. 1993b. Hybrid lethal systems in the Drosophila melanogaster species complex. II. The Zygotic hybrid rescue (Zhr) gene of Drosophila melanogaster. Genetics 133: 307-313.
69. Sawamura, K., Davis, A.W. & Wu, C.I. 2000. Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 97: 2652-2655.
70. Sawamura, K., Roote, J., Wu, C.-I. & Yamamoto, M.T. 2004. Genetic complexity underlying hybrid male sterility in Drosophila. Genetics 166: 789-796.
71. Sawamura, K., Maehara, K., Mashino, S., Kagesawa, T., Kajiwara-Matsuno, K., Takahashi, A. et al. 2010. Introgression of Drosophila simulans nuclear pore protein 160 in Drosophila melanogaster alone does not cause inviability but does cause female sterility. Genetics 186: 669-676.
72. Schluter, D. 2009. Evidence for ecological speciation and its alternative. Science 323: 737-741.
73. Scopece, G., Lexer, C., Widmer, A. & Cozzolino, S. 2010. Polymorphism of postmating reproductive isolation within plant species. Taxon 59: 367-374.
74. Shirata, M., Araye, Q., Maehara, K., Enya, S., Takano-Shimizu, T. & Sawamura, K. 2014. Allelic asymmetry of the Lethal hybrid rescue (Lhr) gene expression in the hybrid between Drosophila melanogaster and D. simulans: confirmation by using genetic variations of D. melanogaster. Genetica 142: 43-48.
75. Sturtevart, A.H. 1920. Genetic studies of Drosophila simulans. I. Introduction. Hybrids with Drosophila melanogaster. Genetics 5: 488-500.
76. Tamura, K., Subramanian, S. & Kumar, S. 2004. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol. Biol. Evol. 21: 36-44.
77. Tang, S. & Presgraves, D.C. 2009. Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323: 779-782.
78. Tao, Y. & Hartl, D.L. 2003. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. III. Heterogeneous accumulation of hybrid incompatibilities, degree of dominance, and implications for Haldane's rule. Evolution 57: 2580-2598.
79. Thomae, A.W., Schade, G.O., Padeken, J., Borath, M., Vetter, I., Kremmer, E. et al. 2013. A pair of centromeric proteins mediates reproductive isolation in Drosophila species. Dev. Cell 27: 412-424.
80. Tsacas, L. & Bächli, G. 1981. Drosophila sechellia, n. sp., huitième espèce du sous-groupe melanogaster des Iles Seychelles (Diptera, Drosophilidae). Rev. Fr. Entomol. 3: 146-150.
81. Tsacas, L. & David, J. 1974. Drosophila mauritiana n. sp. du groupe melanogaster de l'île Maurice. Bull. Soc. Entomol. Fr. 79: 42-46.
82. Turelli, M. & Orr, H.A. 2000. Dominance, epistasis and the genetics of postzygotic isolation. Genetics 2000: 1663-1679.
83. Wade, M.J. & Johnson, W.A. 1994. Reproductive isolation between two species of flour beetles, Tribolium castaneum and T. freemani: variation within and among geographical populations of T. castaneum. Heredity 72: 155-162.
84. Wade, M.J., Johnson, N.A. & Wardle, G. 1994. Analysis of autosomal polygenic variation for the expression of Haldane's rule in flour beetles. Genetics 138: 791-799.
85. Wade, M.J., Johnson, N.A., Jones, R., Siguel, V. & McNaughton, M. 1997. Genetic variation segregating in natural populations of Tribolium castaneum affecting traits observed in hybrids with T. freemani. Genetics 147: 1235-1247.
86. Warnes, G. & Leisch, F. 2005. Genetics: Population Genetics. R package version, 1(0). Available at http://ftp.ussg.iu.edu/CRAN/bin/macosx/mavericks/contrib/3.1/genetics_1.3.8.1.tgz.
87. Watanabe, T.K. 1979. A gene that rescues the lethal hybrids between Drosophila melanogaster and Drosophila simulans. Jpn. J. Genet. 54: 325-331.
88. Watanabe, T.K., Lee, W.H., Inoue, Y. & Kawanishi, M. 1977. Genetic variation of the hybrid crossability between Drosophila melanogaster and D. simulans. Jpn. J. Genet. 52: 1-8.
89. Whiteman, H.H. & Semlitsch, R.D. 2005. Asymmetric reproductive isolation among polymorphic salamanders. Biol. J. Linn. Soc. 86: 265-281.