Cytonuclear genic incompatibilities cause increased mortality in male F2 hybrids of Nasonia giraulti and N. vitripennis

Genetics

Volumn 178, Issue 1, 2008, Pages 413-426

  Niehuis, Oliver ^a   Judson, Andrea K ^a   Gadau, Jürgen ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHROMOSOME SIZE; DNA HYBRIDIZATION; EMBRYO DEVELOPMENT; GENE MAPPING; GENETIC LINKAGE; GENETIC VARIABILITY; MALE; MORTALITY; NASONIA GIRAULTI; NASONIA VITRIPENNIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; WASP;

ALLELES; ANIMALS; CELL NUCLEUS; CHROMOSOME MAPPING; CHROMOSOMES; GENETIC MARKERS; GENOME, INSECT; HYBRIDIZATION, GENETIC; LINKAGE DISEQUILIBRIUM; MALE; MOLECULAR SEQUENCE DATA; MORTALITY; WASPS;

NASONIA; NASONIA GIRAULTI; NASONIA VITRIPENNIS;

EID: 40849106880     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.080523     Document Type: Article

References (104)

1. BARBASH, D. A., D. F. SIINO, A. M. TARONE and J. ROOTE, 2003 A rapidly evolving MYB-related protein causes species isolation in Drosophila. Proc. Natl. Acad. Sci. USA 100: 5302-5307.
2. BEUKEBOOM, L. W., and C. DESPLAN, 2003 Nasonia. Curr. Biol. 13: R860.
3. BLIER, P. U., F. DUFRESNE and R. S. BURTON, 2001 Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation. Trends Genet. 17: 400-406.
4. BOORE, J. L., 1999 Animal mitochondrial genomes. Nucleic Acids Res. 27: 1767-1780.
5. BORDENSTEIN, S. R., and J. H. WERREN, 1999 Effects of A and B Wolbachia and host genotype on interspecies cytoplasmic incompatibility in Nasonia. Genetics 148: 1833-1844.
6. BORDENSTEIN, S. R., M. D. DRAPEAU and J. H. WERREN, 2000 Intraspecific variation in sexual isolation in the jewel wasp Nasonia. Evolution 54: 567-573.
7. BORDENSTEIN, S. R., F. P. O'HARA and J. H. WERREN, 2001 Wolbachia-induced bidirectional incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409: 707-710.
8. BREEUWER, J. A. J., and J. H. WERREN, 1990 Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346: 558-560.
9. BREEUWER, J. A. J., and J. H. WERREN, 1993 Cytoplasmic incompatibility and bacterial density in Nasonia vitripennis. Genetics 135: 565-574.
10. BREEUWER, J. A. J., and J. H. WERREN, 1995 Hybrid breakdown between two haplodiploid species: the role of nuclear and cytoplasmic genes. Evolution 49: 705-717.
11. BREEUWER, J. A. J., R. STOUTHAMER, S. M. BARNS, D. A. PELLETIER, W. G. WEISBURG et al., 1992 Phylogeny of cytoplasmic incompatibility micro-organisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences. Insect Mol. Biol. 1: 25-36.
12. BRIDEAU, N. J., H. FLORES, J. WANG, S. MAHESHWARI, X. WANG et al., 2006 Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314: 1292-1295.
13. 2 hybrids: consequences of rapid mitochondrial DNA evolution in allopatric populations. Am. Nat. 168: S14-S24.
14. CABOT, E. L., A. W. DAVIS, N. A. JOHNSON and C.-I WU, 1994 Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility. Genetics 137: 175-189.
15. CAMPBELL, B. C., J. D. STEFFEN-CAMPBELL and J. H. WERREN, 1993 Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an rDNA internal transcribed spacer (ITS2). Insect Mol. Biol. 2: 225-237.
16. CAZEMAJOR, M., C. LANDRÉ and C. MONTCHAMP-MOREAU, 1997 The sex-ratio trait in Drosophila simulans: genetic analysis of distortion and suppression. Genetics 147: 635-642.
17. CHAKRAVARTI, A., L. K. LASHER and J. E. REEFER, 1991 A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128: 175-182.
18. COMAI, L., K. YOUNG, B. J. TILL, S. H. REYNOLDS, E. A. GREENE et al., 2004 Efficient discovery of DNA polymorphisms in natural populations by Ecotilling. Plant J. 37: 778-786.
19. COYNE, J. A., and H. A. ORR, 2004 Speciation. Sinauer Associates, Sunderland, MA.
20. DARLING, D. C., and J. H. WERREN, 1990 Biosystematics of Nasonia (Hymenoptera: Pteromalidae): two new species reared from birds' nests in North America. Ann. Entomol. Soc. Am. 83: 352-370.
21. DELNERI, D., I. COLSON, S. GRAMMENOUDI, I. N. ROBERTS, E. J. LOUIS et al., 2003 Engineering evolution to study speciation in yeast. Nature 422: 68-72.
22. DOBZHANSKY, T., 1934 Studies on hybrid sterility. I. Spermatogenesis in pure and hybrid Drosophila pseudoobscura. Z. Zellforsch. Mikrosk. Anat. 21: 169-221.
23. DOBZHANSKY, T., 1975 Analysis of incipient reproductive isolation within a species of Drosophila. Proc. Natl. Acad. Sci. USA 72: 3638-3641.
24. DRAPEAU, M. D., and J. H. WERREN, 1999 Differences in mating behavior and sex ratio between three sibling species of Nasonia. Evol. Ecol. Res. 1: 223-239.
25. ELLISON, C. K., and R. S. BURTON, 2006 Disruption of mitochondrial function in interpopulation hybrids of Tigriopus californicus. Evolution 60: 1382-1391.
26. FISHMANN, L., and J. H. WILLIS, 2005 A novel meiotic drive locus almost completely distorts segregation in Mimulus (Monkey-flower) hybrids. Genetics 169: 347-353.
27. FISHMANN, L., and J. H. WILLIS, 2006 A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60: 1372-1381.
28. FISHMANN, L., A. J. KELLY, E. MORGAN and J. H. WILLIS, 2001 A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics 159: 1701-1716.
29. GADAU, J., J. H. WERREN and R. E. PAGE, 1999 Mapping of hybrid incompatibility loci in Nasonia. Genetics 153: 1731-1741.
30. GADAU, J., J. H. WERREN and R. E. PAGE, 2002 The genetic basis of the interspecific differences in wing size in Nasonia (Hymenoptera; Pteromalidae): major quantitative trait loci and epistasis. Genetics 161: 673-684.
31. GADAU, J., O. NIEHUIS, A. PEIRE, J. H. WERREN, E. BAUDRY et al., 2008 The jewel wasp Nasonia, pp. 27-41 in Genome Mapping and Genomics in Animals. IV. Insects, edited by C. KOLE and W. HUNTER. Springer-Verlag, Berlin/Heidelberg, Germany, New York.
32. GANETSKY, B., 1977 On the components of segregation distortion in Drosophila melanogaster. Genetics 86: 321-355.
33. HALDANE, J. B. S., 1919 The combination of linkage values, and the calculation of distances between the loci of linked factors. J. Genet. 8: 299-309.
34. HALL, M. C., and J. H. WILLIS, 2005 Transmission ratio distortion in intraspecific hybrids of Mimulus guttatus: implications for genomic divergence. Genetics 170: 375-386.
35. HALL, T. A., 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95-98.
36. HARRISON, J. S., and R. S. BURTON, 2006 Tracing hybrid incompatibilities to single amino acid substitutions. Mol. Biol. Evol. 23: 559-564.
37. HARTER, H. L., H. J. KHAMIS and R. E. LAMB, 1984 Modified Kolmogorov-Smirnov tests for goodness of fit. Comm. Stat. Simul. Comp. 13: 293-323.
38. HURST, L. D., 1993 A model for the mechanism of transmission ratio distortion and for t-associated hybrid sterility. Proc. R. Soc. Lond. Ser. B Biol. Sci. 253: 83-91.
39. HURST, G. D. D., and J. H. WERREN, 2001 The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2: 597-606.
40. HUTTER, P., 1997 Genetics of hybrid inviability in Drosophila. Adv. Genet. 36: 157-185.
41. HUTTER, P., 2002 X-linked small GTPase linked and OXPHOS genes are candidates for the genetic basis of hybrid incompatibility in Drosophila. Dev. Genes Evol. 212: 504-512.
42. HUTTER, P., 2007 Rapidly evolving Rab GTPase paralogs and reproductive isolation in Drosophila. Adv. Genet. 58: 1-23.
43. JOHNSON, N. A., 2000 Gene interactions and the origin of species, pp. 197-212 in Endless Forms: Species and Speciation, edited by D. HOWARD and S. BERLOCHER. Oxford University Press, Oxford.
44. KHAMIS, H. J., 1990 The delta-corrected Kolmogorov-Smirnov test for goodness of fit. J. Stat. Plan. Inference 24: 317-335.
45. KHAMIS, H. J., 1993 A comparative study of the delta-corrected Kolmogorov-Smirnov test. J. Appl. Stat. 20: 401-421.
46. KOROL, A. B., I. A. PREYGEL and Y. I. NYUTIN, 1989 Quasi-linkage in tomato: formal analysis. Genetika 25: 2225-2233.
47. KOSAMBI, D. D., 1944 The estimation of map distances from recombination values. Ann. Eugen. 12: 172-175.
48. LANGE, K., and M. BOEHNKE, 1982 How many polymorphic genes will it take to span the human genome? Am. J. Hum. Genet. 34: 842-845.
49. LAVINE, M., and M. J. SCHERVISH, 1999 Bayes factors: what they are and what they are not. Am. Stat. 53: 119-122.
50. LEWONTIN, R. C., 1974 The Genetic Basis of Evolutionary Change. Columbia University Press, New York.
51. LILLIEFORS, H. W., 1967 On the Kolmogorov-Smirnov test for normality with mean and variance unknown. J. Am. Stat. Assoc. 62: 399-402.
52. LIU, B. H, 1998 Statistical Genomics: Linkage, Mapping, and QTL Analysis. CRC Press, Boca Raton, FL.
53. LORIEUX, M., B. GOFFINET, X. PERRIER, D. GONZÁLEZ DE LEÓN and C. LANAUD, 1995a Maximum likelihood models for mapping genetic markers showing segregation distortion. 1. Backcross populations. Theor. Appl. Genet. 90: 73-80.
54. 2-populations. Theor. Appl. Genet. 90: 81-89.
55. LYNCH, M., B. KOSKELLA and S. SCHAACK, 2006 Mutation pressure and the evolution of organelle genomic architecture. Science 311: 1727-1730.
56. LYTTLE, T. W., 1991 Segregation distorters. Annu. Rev. Genet. 25: 511-557.
57. MALITSCHEK, B., D. FORNZLER and M. SCHARTL, 1995 Melanoma formation in Xiphophorus: a model system for the role of receptor tyrosine kinases in tumorigenesis. BioEssays 17: 1017-1023.
58. MERÇOT, H., A. ATLAN, M. JACQUES and C. MONTCHAMP-MOREAU, 1995 Sex-ratio distortion in Drosophila simulans: co-occurrence of a meiotic drive and a suppressor of drive. J. Evol. Biol. 8: 283-300.
59. MERRILL, C., L. BAYRAKTAROGLU, A. KUSANO and B. GANETZKY, 1999 Truncated RanGAP encoded by the Segregation distorter locus of Drosophila. Science 283: 1742-1745.
60. MESTER, D. I., Y. I. RONIN, D. MINKOV, E. NEVO and A. B. KOROL, 2003a Constructing large-scale genetic maps using an evolutionary strategy algorithm. Genetics 165: 2269-2282.
61. MESTER, D. I., Y. I. RONIN, Y. HU, J. PENG, E. NEVO et al., 2003b Efficient multipoint mapping: making use of dominant repulsion-phase markers. Theor. Appl. Genet. 107: 1102-1112.
62. MESTER, D. I., Y. I. RONIN, E. NEVO and A. B. KOROL, 2004 Fast and high precision algorithms for optimization in large-scale genomic problems. Comput. Biol. Chem. 28: 281-290.
63. MISHMAR, D., and M. GERSHONI, 2007 Treating speciation processes as complex traits. Nat. Rev. Genet. 8:.
64. MONTCHAMP-MOREAU, C., and D. JOLY, 1997 Abnormal spermiogenesis is associated with the X-linked sex-ratio trait in Drosophila simulans. Heredity 79: 24-30.
65. MOYLE, L. C., and E. B. GRAHAM, 2006 Genome-wide associations between hybrid sterility QTL and marker transmission ratio distortion. Mol. Biol. Evol. 23: 973-980.
66. MULLER, J. H., 1939 Reversibility in evolution considered from the standpoint of genetics. Biol. Rev. Camb. Philos. Soc. 14: 261-280.
67. MULLER, J. H., 1940 Bearing of the Drosophila work on systematics, pp. 185-268 in The New Systematics, edited by J. S. HUXLEY. Clarendon Press, Oxford.
68. MULLER, J. H., 1942 Isolating mechanisms, evolution, and temperature. Biol. Symp. 6: 71-125.
69. NIEHUIS, O., A. K. JUDSON, J. H. WERREN, W. B. HUNTER, P. M. DANG et al., 2007 Species diagnostic single-nucleotide polymorphism and sequence-tagged site markers for the parasitic wasp genus Nasonia (Hymenoptera: Pteromalidae). J. Econ. Entomol. 100: 1033-1036.
70. ORR, A., 1995 The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805-1813.
71. ORR, A., 2005 The genetic basis of reproductive isolation: insights from Drosophila. Proc. Natl. Acad. Sci. USA 102: 6522-6526.
72. ORR, H. A., and S. IRVING, 2001 Complex epistasis and the genetic basis of hybrid sterility in the Drosophila pseudoobscura Bogota-USA hybridization. Genetics 158: 1089-1100.
73. ORR, H. A., and S. IRVING, 2005 Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169: 671-682.
74. ORR, A., J. P. MASLY and D. C. PRESGRAVES, 2004 Speciation genes. Curr. Opin. Genet. Dev. 14: 675-679.
75. PARDO-MANUEL DE VILLENA, F., E. DE LA CASA EPERÓN, T. L. BRISCOE and C. SAPIENZA, 2000 A genetic test to determine the origin of maternal transmission ratio distortion: meiotic drive at the mouse Om locus. Genetics 154: 333-342.
76. PENG, J. H., A. B. KOROL, T. FAHIMA, M. S. RÖDER, Y. I. RONIN et al., 2000 Molecular genetic maps in wild emmer wheat, Triticum dicoccoides: genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Res. 10: 1509-1531.
77. PIETSCH, C., 2005 The genetics of species differences within the genus Nasonia Ashmead 1904 (Hymenoptera: Pteromalidae). D. Nat. Sci. Thesis, University of Würzburg, Würzburg, Germany.
78. PIETSCH, C., K. RÜTTEN and J. GADAU, 2004 Eleven microsatellite markers in Nasonia, Ashmead 1904 (Hymenoptera; Pteromalidae). Mol. Ecol. Notes 4: 43-45.
79. PRESGRAVES, D. C., L. BALAGOPALAN, S. M. ABMAYR and H. A. ORR, 2003 Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423: 715-719.
80. RAND, D. M., R. A. HANEY and A. J. FRY, 2004 Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19: 645-653.
81. RAWSON, P. A., and R. S. BURTON, 2002 Functional coadaptation between cytochrome c and cytochrome c oxidase within allopatric populations of a marine copepod. Proc. Natl. Acad. Sci. USA 99: 12955-12958.
82. RÜTTEN, K., C. PIETSCH, K. OLEK, M. NEUSSER, L. W. BEUKEBOOM et al., 2004 Chromosomal anchoring of linkage groups and identification of wing size QTL markers and FISH probes derived from microdissected chromosomes in Nasonia (Pteromalidae: Hymenoptera). Cytogenet. Genome Res. 105: 126-133.
83. SACKTON, T. B., R. A. HANEY and D. M. RAND, 2003 Cytonuclear coadaptation in Drosophila: disruption of cytochrome c oxidase activity in backcross genotypes. Evolution 57: 2315-2325.
84. SAWAMURA, K., Y. TOMIMURA, H. SATO, H. YAMADA, M. MATSUDA et al., 2006 Establishing interspecific mosaic genome lines between Drosophila ananassae and Drosophila pallidosa by means of parthenogenesis. Genet. Res. 88: 1-11.
85. SCHARTL, A., N. DIMITRIJEVIC and M. SCHARTL, 1994 Evolutionary origin and molecular biology of the melanoma-inducing oncogene of Xiphophorus. Pigment Cell Res. 7: 428-432.
86. SILVER, L. M., 1993 The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 9: 250-254.
87. SKINNER, S. W., and J. H. WERREN, 1980 The genetics of sex determination in Nasonia vitripennis (Hymenoptera, Pteromalidae). Genetics 94: s98.
88. STEBBINS, G. L., 1950 Variation and Evolution in Plants. Columbia University Press, New York.
89. TAO, Y., and D. L. HARTL, 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.
90. TAO, Y., D. L. HARTL and C. C. LAURIE, 2001 Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc. Natl. Acad. Sci. USA 98: 13183-13188.
91. 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.
92. TURELLI, M., and L. C. MOYLE, 2007 Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176: 1059-1088.
93. VELTHUIS, B.-J., W. YANG, T. VAN OPIJNEN and J. H. WERREN, 2005 Genetics of female mate discrimination of heterospecific males in Nasonia (Hymenoptera, Pteromalidae). Anim. Behav. 69: 1107-1120.
94. VOGL, C., and S. XU, 2000 Multipoint mapping of viability and segregation distorting loci using molecular markers. Genetics 155: 1439-1447.
95. WERREN, J. H., 1997 Biology of Wolbachia. Annu. Rev. Entomol. 42: 587-609.
96. WERREN, J. H., 1998 Wolbachia and speciation, pp. 245-260 in Endless Forms: Species and Speciation, edited by D. HOWARD and S. BERLOCHER. Oxford University Press, Oxford.
97. WESTON, R. F., I. QURESHI and J. H. WERREN, 1999 Genetics of a wing size difference between two Nasonia species. J. Evol. Biol. 12: 586-595.
98. WHITING, A. R., 1967 The biology of the parasitic wasp Mormoniella vitripennis [= Nasonia brevicornis] (Walker). Q. Rev. Biol. 42: 333-406.
99. WILFERT, L., J. GADAU and P. SCHMID- HEMPEL, 2007 The genetic architecture of immune defense and reproduction in male Bombus terrestris bumblebees. Evolution 61: 804-815.
100. WILLETT, C. S., 2006 Deleterious epistatic interactions between electron transport system protein-coding loci in the copepod Tigriopus californicus. Genetics 173: 1465-1477.
101. WITTBRODT, J., D. ADAM, B. MALITSCHEK, W. MAUELER, F. RAULF et al., 1989 Novel putative receptor tyrosine kinase encoded by the melanoma-inducing Tu locus in Xiphophorus. Nature 341: 415-421.
102. WU, C.-I, T. W. LYTTLE, M.-L. WU and G.-F. LIN, 1988 Association between a satellite DNA-sequence and the responder of Segregation distorter in Drosophila melanogaster. Cell 54: 179-189.
103. 2 test. J. R. Stat. Soc. 1(Suppl.): 217-235.
104. ZAR, J. H., 1999 Biostatistical Analysis, Ed. 4. Prentice-Hall, Englewood Cliffs, NJ.