#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Fine Mapping of Dominant -Linked Incompatibility Alleles in Hybrids


The inviability or sterility of interspecific hybrids is one of the mechanisms of reproductive isolation that keep species apart. In this report, we use the genetic tools of Drosophila melanogaster to assess the cytological locations and relative frequency of dominant X-linked alleles involved in hybrid inviability in three different interspecific crosses. We map the genomic regions of the D. melanogaster X-chromosome that cause inviability in hybrids produced by D. melanogaster females crossed to males of three other Drosophila species: D. simulans, D. mauritiana and D. santomea. For each hybrid inviability allele we identified, we characterized the developmental defects that occur in the inviable hybrids. Our results show that the effect of these X-linked lethal regions is lineage-specific, as is the total number of alleles that cause hybrid inviability. These results can be expanded and will allow for the exact identification of X-linked D. melanogaster alleles in these three different hybrid contexts.


Vyšlo v časopise: Fine Mapping of Dominant -Linked Incompatibility Alleles in Hybrids. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004270
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004270

Souhrn

The inviability or sterility of interspecific hybrids is one of the mechanisms of reproductive isolation that keep species apart. In this report, we use the genetic tools of Drosophila melanogaster to assess the cytological locations and relative frequency of dominant X-linked alleles involved in hybrid inviability in three different interspecific crosses. We map the genomic regions of the D. melanogaster X-chromosome that cause inviability in hybrids produced by D. melanogaster females crossed to males of three other Drosophila species: D. simulans, D. mauritiana and D. santomea. For each hybrid inviability allele we identified, we characterized the developmental defects that occur in the inviable hybrids. Our results show that the effect of these X-linked lethal regions is lineage-specific, as is the total number of alleles that cause hybrid inviability. These results can be expanded and will allow for the exact identification of X-linked D. melanogaster alleles in these three different hybrid contexts.


Zdroje

1. Coyne JA, Orr HA (2004) Speciation. Sunderland, Mass, Sinauer Associates.

2. Price TD (2007) Speciation in Birds. Roberts & Co. Publishers. Boulder, CO, USA.

3. OrrHA (2001) The genetics of species differences. Trends Ecol Evol 16: 343–350.

4. OrrHA, MaslyJP, PhadnisN (2007) Speciation in Drosophila: from phenotypes to molecules. J Hered 98: 103–110.

5. Dobzhansky T (1937) Genetics and the origin of species. New York: Columbia University Press.

6. ServedioMR, NoorMAF (2003) The role of reinforcement in speciation: theory and data. Annu Rev Ecol Evol Syst 34: 339–364.

7. Nosil P (2012) Ecological speciation. Oxford University Press, Oxford.

8. HopkinsR (2013) Reinforcement in plants. New Phytol 197: 1095–1103.

9. MullerHJ (1942) Isolating mechanisms, evolution, and temperature. Biol Symp 6: 71–125.

10. OrrHA (1995) The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics 139: 1805–1813.

11. MaslyJP, JonesCD, NoorMAF, OrrHA (2006) Gene transposition as a cause of hybrid sterility. Science 313: 1448–1450.

12. MoyleLC, MuirCD, HanMV, HahnMW (2010) The contributions of gene movement to the “two rules of speciation”. Evolution 64: 1541–1557.

13. MaheshwariS, BarbashDA (2011) The genetics of hybrid incompatibilities. Annu Rev Genet 45: 331–55.

14. NosilP, SchluterD (2011) The genes underlying the process of speciation. Trends Ecol Evol 26: 160–167.

15. HaldaneJBS (1922) Sex-ratio and unisexual sterility in hybrid animals. J Genetics 12: 101–109.

16. OrrHA (1997) Haldane's rule. Annu Rev Ecol Syst 28: 195–218.

17. PresgravesDC, BalagopalanL, AbmayrSM, OrrHA (2003) Adaptive evolution drives divergence of a hybrid inviability gene in Drosophila. Nature 423: 715–719.

18. TangS, PresgravesDC (2009) Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323: 779–782.

19. PhadnisN, OrrHA (2009) A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323: 376–378.

20. MaslyJP, PresgravesDC (2007) High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol 5: e243.

21. OrrHA, TurelliM (2001) The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55: 1085–1094.

22. MatuteDR, ButlerIA, TurissiniDA, CoyneJA (2010) A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science 329: 1518–1521.

23. MoyleLC, NakazatoT (2010) Hybrid Incompatibility ‘snowballs’ between Solanum species. Science 329: 1521–1523.

24. BreeuwerH, WerrenJH (1990) Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346: 558–560.

25. BreeuwerJAJ, WerrenJH (1995) Hybrid breakdown between two haplodiploid species: The role of nuclear and cytoplasmic genes. Evolution 49: 705–717.

26. TurelliM, MoyleLC (2007) Asymmetric postmating isolation: Darwin's corollary to Haldane's rule. Genetics 176: 1059–1088.

27. BolnickDI, TurelliM, López-FernándezH, WainwrightPC, NearTJ (2008) Accelerated mitochondrial evolution and ‘Darwin's corollary’: Asymmetric viability of reciprocal F1 hybrids in centrarchid fishes. Genetics 178: 1037–1048.

28. LeeHY, ChouJY, CheongL, ChangNH, et al. (2008) Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135: 1065–1073.

29. ChouJY, HungYS, LinKH, LeeHY, LeuJY (2010) Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol 8: e1000432.

30. OrrHA (1993) A mathematical model of Haldane's rule. Evolution 47: 1606–1611.

31. OrrHA (1993) Haldane's rule has multiple genetic causes. Nature 361: 532–533.

32. TurelliM, OrrHA (1995) The dominance theory of Haldane's rule. Genetics 140: 389–402.

33. OrrHA, TurelliM (1995) Dominance and Haldane's rule. Genetics 143: 613–616.

34. PresgravesDC, OrrHA (1998) Haldane's rule is obeyed in taxa lacking a hemizygous sex. Science 282: 952–954.

35. CharlesworthB, CoyneJA, BartonNH (1987) The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130: 113–146.

36. TurelliM, BegunDJ (1997) Haldane's rule and X chromosome size in Drosophila. Genetics 147: 1799–1815.

37. TurelliM, OrrHA (2000) Dominance, epistasis and the genetics of postzygotic isolation. Genetics 154: 1663–1679.

38. CoyneJA, SimeonidisS, RooneyP (1998) Relative paucity of genes causing inviability in hybrids between Drosophila melanogaster and D. simulans. Genetics 150: 1091–1103.

39. SawamuraK, TairaT, WatanabeTK (1993) Hybrid lethal systems in the Drosophila melanogaster species complex. I. The maternal hybrid rescue (mhr) gene of Drosophila simulans. Genetics 133: 299–305.

40. SawamuraK, YamamotoM (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.

41. CattaniMV, PresgravesDC (2012) Incompatibility between X chromosome Factor and pericentric heterochromatic region causes lethality in hybrids between Drosophila melanogaster and its sibling species. Genetics 191: 549–559.

42. CabotEL, DavisAW, JohnsonNA, WuC-I (1994) Genetics of reproductive isolation in the Drosophila simulans clade: Complex epistasis underlying hybrid male sterility. Genetics 137: 175–189.

43. TurelliM, BartonNH, CoyneJA (2001) Theory and speciation. Trends Ecol Evol 16: 330–343.

44. OrrHA, TurelliM (2001) The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55: 1085–1094.

45. MoyleLC, NakazatoT (2009) Complex Epistasis for Dobzhansky-Muller Hybrid Incompatibility in Solanum. Genetics 181: 347–351.

46. TrueJR, WeirBS, LaurieCC (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.

47. PalopoliMF, WuC-I (1994) Genetics of hybrid male sterility between Drosophila sibling species: a complex web of epistasis is revealed in interspecific studies. Genetics 138: 329–341.

48. PresgravesDC (2003) A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. Genetics 163: 955–972.

49. PresgravesDC, BalagopalanL, AbmayrSM, OrrHA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423: 715–719.

50. TangS, PresgravesDC (2009) Evolution of the Drosophila nuclear pore complex results in multiple hybrid incompatibilities. Science 323: 779–782.

51. FerreePM, BarbashDA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7: e1000234.

52. CookRK, DealME, DealJA, GartonRD, BrownCD, et al. (2010) A new resource for characterizing X-linked genes in Drosophila melanogaster: systematic coverage and subdivision of the X chromosome with nested, Y-linked duplications. Genetics 186: 1095–1109.

53. Gavin-SmythJ, MatuteDR (2013) Embryonic lethality leads to hybrid male inviability in hybrids between Drosophila melanogaster and D. santomea. Ecology and Evolution 3: 1580–1589.

54. SturtevantAH (1929) The genetics of Drosophila simulans. Carnegie Inst Wash Publ 399: 1–62.

55. OrrHA, MaddenLD, CoyneJA, GoodwinR, HawleyRS (1997) The developmental genetics of hybrid inviability: a mitotic defect in Drosophila hybrids. Genetics 145: 1031–1040 32.

56. BolkanBJ, BookerR, GoldbergML, BarbashDA (2007) Developmental and cell cycle progression defects in Drosophila hybrid males. Genetics 177: 2233–2241.

57. WieschausE, SweetonD (1988) Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development 104: 483–93.

58. BirchlerJA, HiebertJC, KrietzmanM (1989) Gene expression in adult metafemales of Drosophila melanogaster. Genetics 122: 869–879.

59. FrostJN (1960) The occurrence of partially fertile metafemales in Drosophila melanogaster. Proc Natl Acad Sci U S 46: 47–51.

60. TakamuraT, WatanabeTK (1980) Further studies on the Lethal hybrid rescue (Lhr) gene of Drosophila simulans. Jap J Genet 55: 405–408.

61. Pal BhadraM, BhadraU, BirchlerJA (2006) Misregulation of sex-lethal and disruption of male-specific lethal complex localization in Drosophila species hybrids. Genetics 174: 1151–1159.

62. ChatterjeeRN, ChatterjeeP, PalA, Pal BhadraM (2007) Drosophila simulans Lethal hybrid rescue mutation (Lhr) rescues inviable hybrids by restoring X chromosomal dosage compensation and causes fluctuating asymmetry of development. J Genet 86: 203–215.

63. KlimanRM, AndolfattoP, CoyneJA, DepaulisF, KreitmanM, et al. (2000) The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics 156: 1913–1931.

64. ShapiroJA, HuangW, ZhangC, HubiszMJ, LuJ, et al. (2007) Adaptive genic evolution in the Drosophila genomes. Proc Natl Acad Sci U S A 104: 2271–2276.

65. LefflerEM, BullaugheyK, MatuteDR, MeyerWK, SegurelL, et al. (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10: e1001388.

66. SanchezL, SantamariaP (1997) Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics 147: 231–242.

67. LachaiseD, HarryM, SolignacM, LemeunierF, BénassiV, et al. (2000) Evolutionary Novelties in Islands: Drosophila santomea, a new melanogaster Sister Species from São Tomé. Proc R Soc Lond B 267: 1487–1495.

68. LlopartA, LachaiseD, CoyneJA (2005) Multilocus analysis of introgression between two sympatric sister species of Drosophila: Drosophila yakuba and D. santomea. Genetics 171: 197–210.

69. BeloteJM, LucchesiJC (1980) Male-specific lethal mutations of Drosophila melanogaster. Genetics 96: 165–186.

70. ClineTW (1984) Autoregulatory functioning of a Drosophila gene product that establishes and maintains the sexually determined state. Genetics 107: 231–277.

71. ConradT, AkhtarA (2012) Dosage compensation in Drosophila melanogaster: epigenetic fine-tuning of chromosome-wide transcription. Nature Reviews Genetics 13: 123–134.

72. SunL, FernandezHR, DonohueRC, LiJ, ChengJ, BirchlerJA (2013) Male-specific lethal complex in Drosophila counteracts histone acetylation and does not mediate dosage compensation. Proc Natl Acad Sci U S A 110: E808–E817.

73. BellLR, HorabinJI, SchedlP, ClineTW (1991) Positive autoregulation of Sex-lethal by alternative splicing maintains the female determined state in Drosophila. Cell 65: 229–239.

74. BellLR, MaineEM, SchedlP, ClineTW (1988) Sex-lethal, a Drosophila sex determination switch gene, exhibits sex-specific RNA splicing and sequence similarity to RNA binding proteins. Cell 55: 1037–1046.

75. ClineTW (1978) Two closely linked mutations in Drosophila melanogaster that are lethal to opposite sexes and interact with daughterless. Genetics 90: 683–697.

76. BarbashDA (2010) Genetic testing of the hypothesis that hybrid male lethality results from a failure in dosage compensation. Genetics 184: 313–316.

77. BarbashDA (2011) Comment on “A test of the snowball theory for the rate of evolution of hybrid incompatibilities”. Science 333: 1576.

78. MatuteDR, TurissiniDA, CoyneJA (2011) Response to Comment on “A test of the snowball theory for the rate of evolution of hybrid incompatibilities”. Science 333: 1576.

79. LindsleyDL, NovitskiE (1950) The synthesis of an attached XY chromosome. Drosophila Information System 24: 84–85.

80. LindsleyDL, NovitskiE (1959) Compound chromosomes involving the X and Y chromosomes of Drosophila melanogaster. Genetics 44: 187–196.

81. YamamotoMT (1992) Inviability of hybrids between D. melanogaster and D. simulans results from the absence of simulans X not the presence of simulans Y chromosome. Genetica 87: 151–158.

82. BarbashDA, AshburnerM (2003) A novel system of fertility rescue in Drosophila hybrids reveals a link between hybrid lethality and female sterility. Genetics 163: 217–226.

83. HutterP, AshburnerM (1987) Genetic rescue of inviable hybrids between Drosophila melanogaster and its sibling species. Nature 327: 331–333.

84. BarbashDA, RooteJ, AshburnerM (2000) The Drosophila melanogaster hybrid male rescue gene causes inviability in male and female species hybrids. Genetics 154: 1747–1771.

85. MorganLV (1922) Non-criss-cross inheritance in Drosophila melanogaster. Biol Bull Wood's Hole 42: 267–274.

86. AndersonEG (1925) Crossing over in a case of attached X chromosomes in Drosophila melanogaster. Genetics 10: 403–417.

87. Lindsey DL, Zimm GG (1992) The Genome of Drosophila melanogaster. Academic Press, New York.

88. ClineTW (1993) The Drosophila sex determination signal: how do flies count to two? Trends Genet 9: 385–390.

89. BeadleGW, EmersonS (1935) Further studies of crossing over in attached-X chromosomes of Drosophila melanogaster. Genetics 20: 192.

90. MorganLV (1938) Effects of a compound duplication of the X chromosome of Drosophila melanogaster. Genetics 23: 423–462.

91. MullerHJ (1943) A stable double X chromosome. Drosophila Information Service 17: 61–62.

92. MatuteDR, NovakCJ, CoyneJA (2009) Thermal adaptation and extrinsic reproductive isolation in two species of Drosophila. Evolution 63: 583–594.

93. MatuteDR, CoyneJA (2010) Intrinsic reproductive isolation between two sister species of Drosophila. Evolution 64: 903–920.

94. CoyneJA, BeecharnE (1987) Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics 117: 727–737.

95. SattaY, ToyoharaN, OhtakaC, TatsunoY, WatanabeT, et al. (1988) Dubious maternal inheritance of mitochondrial DNA in Drosophila simulans and evolution of Drosophila mauritiana. Genet Res 52: 1–6.

96. CoyneJA (1992) Genetics of sexual isolation in females of the Drosophila simulans species complex. Genet Res 60: 25–31.

97. LangleyCH, StevensK, CardenoC, LeeYC, SchriderDR, et al. (2012) Genomic variation in natural populations of Drosophila melanogaster. Genetics 192: 533–598.

98. PoolJE, Corbett-DetigRB, SuginoRP, StevensKA, CardenoCM, et al. (2012) Population genomics of sub-Saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet 8: ee1003080.

99. Thompson JGP, Schedl P, Pulak R (2004) Sex-specific GFP-expression in Drosophila embryos and sorting by Copas flow cytometry technique. Presented at the 45th Annual Drosophila Research Conference, Washington, DC, 24–28 March 2004.

100. 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.

101. SidakZ (1967) Rectangular confidence regions for the means of multivariate normal distributions. Journal of the American Statistical Association 62: 626–633.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 4
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#