Female heterogamety and speciation: Reduced introgression of the z chromosome between two species of nightingales

Evolution

Volumn 64, Issue 2, 2010, Pages 456-471

  Storchová, Radka ^a,b   Reif, Jiří ^c   Nachman, Michael W ^a  

^a University of Arizona   (United States)

^b CHARLES UNIVERSITY   (Czech Republic)

^c Charles University   (Czech Republic)

Author keywords

Birds; Hybrid zone; Reproductive isolation; Sex chromosomes; Speciation

Indexed keywords

CHROMOSOME; DIVERGENCE; HYBRID ZONE; INTROGRESSION; POLYMORPHISM; REPRODUCTIVE ISOLATION; SEXUAL SELECTION; SONGBIRD; STERILITY;

ANIMAL; ARTICLE; CHROMOSOME; FEMALE; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; SONGBIRD; SPECIES DIFFERENCE;

ANIMALS; CHROMOSOMES; FEMALE; LINKAGE (GENETICS); MOLECULAR SEQUENCE DATA; PASSERIFORMES; POLYMERASE CHAIN REACTION; POLYMORPHISM, GENETIC; SPECIES SPECIFICITY;

AVES; LUSCINIA LUSCINIA; MYA;

EID: 75149153490     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2009.00841.x     Document Type: Article

References (90)

1. Albert, A. Y., and S. P. Otto. 2005. Sexual selection can resolve sex-linked sexual antagonism. Science 310 : 119 121.
2. Andrés, A. M., A. G. Clark, L. Shimmin, E. Boerwinkle, C. F. Sing, and J. E. Hixson. 2007. Understanding the accuracy of statistical haplotype inference with sequence data of known phase. Genet. Epidemiol. 31 : 659 671.
3. Backström, N., M. Brandström, L. Gustafsson, A. Qvarnström, H. Cheng, and H. Ellegren. 2006. Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome. Genetics 174 : 377 386.
4. Backström, N., S. Fagerberg, and H. Ellegren. 2008. Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol. Ecol. 17 : 964 980.
5. Baines, J. F., S. A. Sawyer, D. L. Hartl, and J. Parsch. 2008. Effects of X-linkage and sex-biased gene expression on the rate of adaptive protein evolution in Drosophila. Mol. Biol. Evol. 25 : 1639 1650.
6. Becker, J. 2007. About Nightingales (Luscinia megarhynchos), Trush Nightingales (Luscinia luscinia) and their hybrids - further results of an investigation via bird ringing in the Frankfurt (Oder) area. Vogelwarte 45 : 15 26.
7. Betancourt, A. J., D. C. Presgraves, and W. J. Swanson. 2002. A test for faster X evolution in Drosophila. Mol. Biol. Evol. 19 : 1816 1819.
8. Borge, T., M. T. Webster, G. Andersson, and G. P. Sætre. 2005. Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species. Genetics 171 : 1861 1873.
9. Carling, M. D., and R. T. Brumfield. 2008. Haldane's rule in an avian system: using cline theory and divergence population genetics to test for differential introgression of mitochondrial, autosomal, and sex-linked loci across the Passerina bunting hybrid zone. Evolution 62 : 2600 2615.
10. Carling, M. D., and R. T. Brumfield. 2009. Speciation in Passerina buntings: introgression patterns of sex-linked loci identify a candidate gene region for reproductive isolation. Mol. Ecol. 18 : 834 847.
11. Carneiro, M., N. Ferrand, and M. W. Nachman. 2009. Recombination and speciation: loci near centromeres are more differentiated than loci near telomeres between subspecies of the European rabbit (Oryctolagus cuniculus). Genetics 181 : 593 606.
12. Connallon, T. 2007. Adaptive protein evolution of X-linked and autosomal genes in Drosophila: implications for faster-X hypotheses. Mol. Biol. Evol. 24 : 2566 2572.
13. Counterman, B. A., D. Ortiz-Barrientos, and M. A. Noor. 2004. Using comparative genomic data to test for fast-X evolution. Evolution 58 : 656 660.
14. Coyne, J. A., and H. A. Orr. 1989. Two rules of speciation. Pp. 180 207 in D. Otte and J. Endler, eds. Speciation and its consequences. Sinauer Associates, Sunderland, MA.
15. Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer Associates, Sunderland, MA.
16. Cramp, S. 1988. The Birds of the Western Palearctic. Oxford Univ. Press, Oxford, UK.
17. Ellegren, H. 2009. Genomic evidence for a large-Z effect. Proc. R. Soc. Lond. B 276 : 361 366.
18. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8 : 186 194. (Pubitemid 28177230)
19. Ewing, B., L. Hillier, M. C. Wendl, and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8 : 175 185. (Pubitemid 28177229)
20. Gelter, H. P., H. Tegelström, and L. Gustafsson. 1992. Evidence from hatching success and DNA fingerprinting for the fertility of hybrid Pied x Collared Flycatchers Ficedula hypoleuca x albicollis. Ibis 134 : 62 68.
21. Good, J. M., M. D. Dean, and M. W. Nachman. 2008. A complex genetic basis to X-linked hybrid male sterility between two species of house mice. Genetics 179 : 2213 2228.
22. Gordon, D., C. Abajian, and P. Green. 1998. Consed: a graphical tool for sequence finishing. Genome Res. 8 : 195 202.
23. Hall, T. A. 1999. BioEdit: a user friendly biological sequence alignment editor and analyses program for Windows 95/98/NT. Nucleic Acids Symp. Series : 95 98.
24. Hall, D. W., and M. Kirkpatrick. 2006. Reinforcement and sex linkage. Evolution 60 : 908 921.
25. Hastings, I. M. 1994. Manifestations of sexual selection may depend on the genetic bases of sex determination. Proc. R. Soc. Lond. B 258 : 83 87.
26. Hewitt, G. 2000. The genetic legacy of the Quaternary ice ages. Nature 405 : 907 913.
27. Hey, J., and R. Nielsen. 2004. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167 : 747 760.
28. Hey, J., and R. Nielsen. 2007. Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Natl. Acad. Sci. USA 104 : 2785 2790.
29. Hey, J., and J. Wakeley. 1997. A coalescent estimator of the population recombination rate. Genetics 145 : 833 846.
30. Hudson, R. R., M. Kreitman, and M. Aguade. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116 : 153 159.
31. Hudson, R. R., D. D. Boos, and N. L. Kaplan. 1992. A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 9 : 138 151.
32. Itoh, Y., K. Kampf, and A. P. Arnold. 2006. Comparison of the chicken and zebra finch Z chromosomes shows evolutionary rearrangements. Chromosome Res. 14 : 805 815.
33. Iyengar, V. K., H. K. Reeve, and T. Eisner. 2002. Paternal inheritance of a female moth's mating preference. Nature 419 : 830 832.
34. Jiggins, C. D., M. Linares, R. E. Naisbit, C. Salazar, Z. H. Yang, and J. Mallet. 2001. Sex-linked hybrid sterility in a butterfly. Evolution 55 : 1631 1638.
35. Jønsson, K. A., and J. Fjeldså. 2006. A phylogenetic supertree of oscine passerine birds (Aves: Passeri). Zool. Scripta 35 : 149 186.
36. Kirkpatrick, M., and D. W. Hall. 2004. Sexual selection and sex linkage. Evolution 58 : 683 691.
37. Klicka, J., and R. M. Zink. 1997. The importance of recent ice ages in speciation: a failed paradigm. Science 277 : 1666 1669.
38. Kverek, P., R. Storchová, J. Reif, and M. W. Nachman. 2008. Occurrence of a hybrid between the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (Luscinia luscinia) in the Czech Republic confirmed by genetic analysis. Sylvia 44 : 17 26.
39. Lewontin, R. C. 1964. The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49 : 49 67.
40. Li, N., and M. Stephens. 2003. Modelling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165 : 2213 2233.
41. Machado, C. A., R. M. Kliman, J. A. Markert, and J. Hey. 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.
42. Macholán, M., P. Munclinger, M. Šugerková, P. Dufková, B. Bímová, E. Božíková, J. Zima, and J. Piálek. 2007. Genetic analysis of autosomal and X-linked markers across a mouse hybrid zone. Evolution 61 : 746 771.
43. Mank, J. E., E. Axelsson, and H. Ellegren. 2007. Fast-X on the Z: rapid evolution of sex-linked genes in birds. Genome Res. 17 : 618 624.
44. Masly, J. P., and D. C. Presgraves. 2007. High-resolution genome-wide dissection of the two rules of speciation in Drosophila. PLoS Biol. 5 : e243.
45. Moriyama, E. N., and J. R. Powell. 1996. Intraspecific nuclear DNA variation in Drosophila. Mol. Biol. Evol. 13 : 261 277.
46. Naisbit, R. E., C. D. Jiggins, M. Linares, C. Salazar, and J. Mallet. 2002. Hybrid sterility, Haldane's rule and speciation in Heliconius cydno and H. melpomene. Genetics 161 : 1517 1526.
47. Nanda, I., K. Schlegelmilch, T. Haaf, M. Schartl, and M. Schmid. 2008. Synteny conservation of the Z chromosome in 14 avian species (11 families) supports a role for Z dosage in avian sex determination. Cytogenet. Genome Res. 122 : 150 156.
48. Nei, M. 1987. Molecular Evolutionary Genetics. Columbia Univ. Press, New York, NY.
49. Nickerson, D. A., V. O. Tobe, and S. L. Taylor. 1997. PolyPhred: automating the detection and genotyping of single nucleotide substitutions using fluorescence-based resequencing. Nucleic Acids Res. 25 : 2745 2751.
50. Nielsen, R., and J. Wakeley. 2001. Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158 : 885 896.
51. Noor, M. A. 1999. Reinforcement and other consequences of sympatry. Heredity 83 : 503 508.
52. Oka, A., A. Mita, N. Sakurai-Yamatani, H. Yamamoto, N. Takagi, T. Takano-Shimizu, K. Toshimori, K. Moriwaki, and T. Shiroishi. 2004. Hybrid breakdown caused by substitution of the X chromosome between two mouse subspecies. Genetics 166 : 913 924.
53. Payseur, B. A., J. G. Krenz, and M. W. Nachman. 2004. Differential patterns of introgression across the X chromosome in a hybrid zone between two species of house mice. Evolution 58 : 2064 2078.
54. Pigozzi, M. I. 2008. Relationship between physical and genetic distances along the zebra finch Z chromosome. Chromosome Res. 2008 : 839 849.
55. Presgraves, D. C. 2008. Sex chromosomes and speciation in Drosophila. Trends Genet. 24 : 336 343.
56. Price, T. 2007. Speciation in birds. Roberts & Company Publishers, Greenwood Village, CO.
57. Provan, J., and K. D. Bennett. 2008. Phylogeographic insights into cryptic glacial refugia. Trends Ecol. Evol. 23 : 564 571.
58. Qvarnström, A., and R. I. Bailey. 2008. Speciation through evolution of sex-linked genes. Heredity 102 : 4 15.
59. Reeve, H. K., and D. W. Pfennig. 2003. Genetic biases for showy males: are some genetic systems especially conducive to sexual selection? Proc. Natl. Acad. Sci. USA 100 : 1089 1094.
60. Ritchie, M. G. 2007. Sexual selection and speciation. Annu. Rev. Ecol. Evol. Syst. 38 : 79 102.
61. Rozas, J., J. C. Sánchez-DelBarrio, X. Messeguer, and R. Rozas. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 : 2496 2497.
62. Sæther, S. A., G. P. Sætre, T. Borge, C. Wiley, N. Svedin, G. Andersson, T. Veen, J. Haavie, M. R. Servedio, S. Bureš, et al. 2007. Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers. Science 318 : 95 97.
63. Sætre, G. P., T. Moum, S. Bureš, M. Král, M. Adamjan, and J. Moreno. 1997. A sexually selected character displacement in flycatchers reinforces premating isolation. Nature 387 : 589 592.
64. Sætre, G. P., T. Borge, K. Lindroos, J. Haavie, B. C. Sheldon, C. Primmer, and A. C. Syvänen. 2003. Sex chromosome evolution and speciation in Ficedula flycatchers. Proc. R. Soc. Lond. B 270 : 53 59.
65. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4 : 406 425.
66. Schoenmakers, S., E. Wassenaar, J. W. Hoogerbrugge, J. S. Laven, J. A. Grootegoed, and W. M. Baarends. 2009. Female meiotic sex chromosome inactivation in chicken. PLoS Genet. 5 : e1000466.
67. Servedio, M. R., and G. P. Sætre. 2003. Speciation as a positive feedback loop between postzygotic and prezygotic barriers to gene flow. Proc. R. Soc. Lond. B 270 : 1473 1479.
68. Sorjonen, J. 1986. Mixed singing and interspecific territoriality - consequences of secondary contact of 2 ecologically and morphologically similar nightingale species in Europe. Ornis Scand. 17 : 53 67.
69. Stadie, C. 1991. Erdsanger I; Nachtigall und Sprosser. Europaische Vogelwelt 3, Sonderheft : 130 189.
70. Stephens, M., and P. Donnelly. 2003. A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 73 : 1162 1169.
71. Stephens, M., N. J. Smith, and P. Donnelly. 2001. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68 : 978 989.
72. Storchová, R., S. Gregorová, D. Buckiová, V. Kyselová, P. Divina, and J. Forejt. 2004. Genetic analysis of X-linked hybrid sterility in the house mouse. Mamm. Genome 15 : 515 524.
73. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 : 585 595.
74. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24 : 1596 1599.
75. Tao, Y., S. Chen, D. L. Hartl, and C. C. Laurie. 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. (Pubitemid 37102204)
76. Tao, Y., L. Araripe, S. B. Kingan, Y. Ke, H. Xiao, and D. L. Hartl. 2007. A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. PLoS Biol. 5 : e303.
77. Teeter, K. C., B. A. Payseur, L. W. Harris, M. A. Bakewell, L. M. Thibodeau, J. E. O'Brien, J. G. Krenz, M. A. Sans-Fuentes, M. W. Nachman, and P. K. Tucker. 2008. Genome-wide patterns of gene flow across a house mouse hybrid zone. Genome Res. 18 : 67 76.
78. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22 : 4673 4680.
79. Thornton, K., and M. Long. 2002. Rapid divergence of gene duplicates on the Drosophila melanogaster X chromosome. Mol. Biol. Evol. 19 : 918 925.
80. Torgerson, D. G., and R. S. Singh. 2003. Sex-linked mammalian sperm proteins evolve faster than autosomal ones. Mol. Biol. Evol. 20 : 1705 1709.
81. 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.
82. Turelli, M., and D. J. Begun. 1997. Haldane's rule and X-chromosome size in Drosophila. Genetics 147 : 1799 1815.
83. Wahlberg, P., L. Strömstedt, X. Tordoir, M. Foglio, S. Heath, D. Lechner, A. R. Hellström, M. Tixier-Boichard, M. Lathrop, I. G. Gut, et al. 2007. A high-resolution linkage map for the Z chromosome in chicken reveals hot spots for recombination. Cytogenet. Genome Res. 117 : 22 29.
84. Wang, R. L., J. Wakeley, and J. Hey. 1997. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics 147 : 1091 1106.
85. Watterson, G. A. 1975. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7 : 256 276.
86. Weir, J. T., and D. Schluter. 2004. Ice sheets promote speciation in boreal birds. Proc. R. Soc. Lond. B 271 : 1881 1887.
87. Wilson, A. C., R. L. Cann, S. M. Carr, M. George, U. B. Gyllensten, K. M. Helm-Bychowski, R. G. Higuchi, S. R. Palumbi, E. M. Prager, R. D. Sage, et al. 1985. Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26 : 375 400.
88. Wink, M., H. Sauer-Gurth, and E. Gwinner. 2002. Evolutionary relationships of stonechats and related species inferred from mitochondrial-DNA sequences and genomic fingerprinting. British Birds 95 : 349 355.
89. Woerner, A. E., M. P. Cox, and M. F. Hammer. 2007. Recombination-filtered genomic datasets by information maximization. Bioinformatics 23 : 1851 1853.
90. Wu, C. I. 2001. The genic view of the process of speciation. J. Evol. Biol. 14 : 851 865.