Trade-off between selection for dosage compensation and masculinization on the avian Z chromosome

Genetics

Volumn 192, Issue 4, 2012, Pages 1433-1445

  Wright, Alison E ^a,b   Moghadam, Hooman K ^a   Mank, Judith E ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOSOME; BIRD; CONTROLLED STUDY; FEMALE; GALLUS GALLUS; GENE DOSAGE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENOME; INHERITANCE; MALE; NONHUMAN; ORTHOLOGY; PRIORITY JOURNAL; SEX CHROMOSOME; SEX RATIO; VIRILIZATION; X CHROMOSOME;

ANIMALS; BIOLOGICAL EVOLUTION; BIRDS; CHICKENS; CHROMOSOME MAPPING; DOSAGE COMPENSATION, GENETIC; FEMALE; GENE EXPRESSION; MALE; SELECTION, GENETIC; SEX CHROMOSOMES;

AVES; GALLUS GALLUS;

EID: 84870712349     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.112.145102     Document Type: Article

References (106)

1. Agrawal, A. F., and M. C. Whitlock, 2011. Inferences about the distribution of dominance drawn from yeast gene knockout data. Genetics 187: 553-566
2. Albert, A. Y. K., and S. P. Otto, 2005. Sexual selection can resolve sex-linked sexual antagonism. Science 310: 119-121
3. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. H. Zhang, Z. Zhang et al., 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402
4. Arnqvist, G., and L. Rowe, 2005. Sexual Conflict. Princeton University Press, Princeton, NJ
5. Axelsson, E., N. G. C. Smith, H. Sundström, S. Berlin, and H. Ellegren, 2004. Male-biased mutation rate and divergence in autosomal, Z-Linked and W-Linked introns of chicken and turkey. Mol. Biol. Evol. 21: 1538-1547
6. Axelsson, E., L. Hultin-Rosenberg, M. Brandström, M. Zwahlen, D. F. Clayton et al., 2008. Natural selection in avian protein-coding genes expressed in brain. Mol. Ecol. 17: 3008-3017
7. Bachtrog, D., 2008. The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179: 1513-1525
8. Bachtrog, D., M. Kirkpatrick, J. E. Mank, S. F. McDaniel, J. C. Pires et al., 2011. Are all sex chromosomes created equal? Trends Genet. 27: 350-357
9. Backstrom, N., H. Ceplitis, S. Berlin, and H. Ellegren 2005. Gene conversion drives the evolution of HINTW, an ampliconic gene on the female-specific avian W chromosome. Mol. Biol. Evol. 22: 1992-1999
10. Backstrom, N., E. Palkopoulou, A. Qvarnstrom, and H. Ellegren, 2010. No evidence for Z-chromosome rearrangements between the pied flycatcher and the collared flycatcher as judged by genebased comparative genetic maps. Mol. Ecol. 19: 3394-3405
11. Benjamini, Y., and Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300
12. Bergero, R., and D. Charlesworth, 2009. The evolution of restricted recombination in sex chromosomes. Trends Ecol. Evol. 24: 94-102
13. Bergero, R., A. Forrest, E. Kamau, and D. Charlesworth, 2007. Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes. Genetics 175: 1945-1954
14. Berlin, S., M. Brandstrom, N. Backstrom, E. Axelsson, N. Smith et al., 2006. Substitution rate heterogeneity and the male mutation bias. J. Mol. Evol. 62: 226-233
15. Bierne, N., and A. Eyre-Walker, 2003. The problem of counting sites in the estimation of the synonymous and nonsynonymous substitution rates: implications for the correlation between the synonymous substitution rate and codon usage bias. Genetics 165: 1587-1597
16. Busby, M., J. Gray, A. Costa, C. Stewart, M. Stromberg et al., 2011. Expression divergence measured by transcriptome sequencing of four yeast species. BMC Genomics 12: 635
17. Carrel, L., and H. F. Willard, 2005. X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404
18. Charif, D., and J. R. Lobry, 2007. Seqin{R} 1.0-2: a contributed package to the {R} project for statistical computing devoted to biological sequences retrieval and analysis, pp. 207-232 in Structural Approaches to Sequence Evolution: Molecules, Networks, Populations. Springer-Verlag, Berlin
19. Charlesworth, B., 1978. Model for evolution of Y chromosomes and dosage compensation. Proc. Natl. Acad. Sci. USA 75: 5618-5622
20. Charlesworth, B., 1996. The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 6: 149-162
21. Charlesworth, B., J. A. Coyne, and N. H. Barton, 1987. The relative rates of evolution of sex chromosomes and autosomes. Am. Nat. 130: 113-146
22. Charlesworth, D., B. Charlesworth, and G. Marais, 2005. Steps in the evolution of heteromorphic sex chromosomes. Heredity 95: 118-128
23. Chen, Z.-X., Y. E. Zhang, M. Vibranovski, J. Luo, G. Gao et al., 2011. Deficiency of X-linked inverted duplicates with male-biased expression and the underlying evolutionary mechanisms in the Drosophila genome. Mol. Biol. Evol. 28: 2823-2832
24. Chippindale, A. K., J. R. Gibson, and W. R. Rice, 2001. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl. Acad. Sci. USA 98: 1671-1675
25. Comeron, J. M., 1995. A method for estimating the numbers of synonymous and nonsynonymous substitutions per site. J. Mol. Evol. 41: 1152-1159
26. Comeron, J. M., 1999. K-estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals. Bioinformatics 15: 763-764
27. Connallon, T., and L. L. Knowles, 2005. Intergenomic conflict revealed by patterns of sex-biased gene expression. Trends Genet. 21: 495-499
28. Connallon, T., and A. G. Clark, 2010. Sex linkage, sex-specific selection and the role of recombination in the evolution of sexually dimorphic gene expression. Evolution 64: 3417-3442
29. Connallon, T., R. M. Cox, and R. Calsbeek, 2010. Fitness consequences of sex-specific selection. Evolution 64: 1671-1682
30. Davis, J. K., P. J. Thomas, and N. C. S. Progra, 2010. A W-linked palindrome and gene conversion in New World sparrows and blackbirds. Chromosome Res. 18: 543-553
31. Deakin, J. E., T. A. Hore, E. Koina, and J. A. M. Graves, 2008. The status of dosage compensation in the multiple X chromosomes of the platypus. PLoS Genet. 4: e1000140
32. Deng, X., J. B. Hiatt, N. Di Kim, S. Ercan, D. Sturgill et al., 2011. Evidence for compensatory upregulation of expressed X-linked genes in mammals, Caenorhabditis elegans and Drosophila melanogaster. Nat. Genet. 43: 1179-1185
33. Dimcheff, D. E., S. V. Drovetski, and D. P. Mindell, 2002. Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol. Phylogenet. Evol. 24: 203-215
34. Eden, E., D. Lipson, S. Yogev, and Z. Yakhini, 2007. Discovering motifs in ranked lists of DNA sequences. PLOS Comput. Biol. 3: 508-522
35. Eden, E., R. Navon, I. Steinfeld, D. Lipson, and Z. Yakhini, 2009. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 10: 48
36. Ellegren, H., 2011. Emergence of male-biased genes on the chicken Z-chromosome: contrasts between male and female heterogametic systems. Genome Res. 21: 2082-2086
37. Ellegren, H., and A. Carmichael, 2001. Multiple and independent cessation of recombination between avian sex chromosomes. Genetics 158: 325-331
38. Ellegren, H., and J. Parsch, 2007. The evolution of sex-biased genes and sex-biased gene expression. Nat. Rev. Genet. 8: 689-698
39. Ellegren, H., L. Hultin-Rosenberg, B. Brunstrom, L. Dencker, K. Kultima et al., 2007. Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol. 5: 40
40. Forgy, E. W., 1965. Cluster analysis of multivariate data: efficiency vs. interpretability of classifications. Biometrics 21: 768-769
41. Galtier, N., 2003. Gene conversion drives GC content evolution in mammalian histones. Trends Genet. 19: 65-68
42. Graur, D., and W.-H. Li, 2000. Fundamentals of Molecular Evolution. Sinauer Associates, Sunderland, MA
43. Hackstein, J. H. P., R. Hockstenbach, E. Hacksteinjungen, and L. W. Beukeboom, 1996. Is the Y chromosome of Drosophila an evolved supernumerary chromosome? Bioessays 18: 317-323
44. Handley, L. L., H. Ceplitis, and H. Ellegren, 2004. Evolutionary strata on the chicken Z chromosome: implications for sex chromosome evolution. Genetics 167: 367-376
45. Harlid, A. B., S. Berlin, N. G. C. Smith, A. P. Mosller, and H. Ellegren, 2003. Life history and the male mutation bias. Evolution 57: 2398-2406
46. Hartigan, J. A., and M. A. Wong, 1979. Algorithm AS 136: a kmeans clustering algorithm. J. R. Stat. Soc. Ser. C Appl. Stat. 28: 100-108
47. Hedges, S. B., 2002. The origin and evolution of model organisms. Nat. Rev. Genet. 3: 838-849
48. Innocenti, P., and E. H. Morrow, 2010. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol. 8: e1000336
49. Itoh, Y., E. Melamed, X. Yang, K. Kampf, S. Wang et al., 2007. Dosage compensation is less effective in birds than in mammals. J. Biol. 6: 2
50. Itoh, Y., E. Replogle, Y. H. Kim, J. Wade, D. F. Clayton et al., 2010. Sex bias and dosage compensation in the zebra finch vs. chicken genomes: general and specialized patterns among birds. Genome Res. 20: 512-518
51. Julien, P., D. Brawand, M. Soumillon, A. Necsulea, A. Ljuechti et al., 2012. Mechanisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol. 10: e1001328
52. Kaiser, V. B., and H. Ellegren, 2006. Nonrandom distribution of genes with sex-biased expression in the chicken genome. Evolution 60: 1945-1951
53. Karlin, S., and S. F. Altschul, 1990. Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc. Natl. Acad. Sci. USA 87: 2264-2268
54. Karlin, S., and S. F. Altschul, 1993. Applications and statistics for multiple high-scoring segments in molecular sequences. Proc. Natl. Acad. Sci. USA 90: 5873-5877
55. Khil, P. P., N. A. Smirnova, P. J. Romanienko, and R. D. Camerini-Otero, 2004. The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation. Nat. Genet. 36: 642-646
56. Kirkpatrick, M., and D. W. Hall, 2004. Sexual selection and sex linkage. Evolution 58: 683-691
57. Lahn, B. T., and D. C. Page, 1999. Four evolutionary strata on the human X chromosome. Science 286: 964-967
58. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg, 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25
59. Lin, F., K. Xing, J. Zhang, and X. He, 2012. Expression reduction in mammalian X chromosome evolution refutes Ohno's hypothesis of dosage compensation. Proc. Natl. Acad. Sci. USA 109: 11752-11757
60. Lin, H., V. Gupta, M. D. VerMilyea, F. Falciani, J. T. Lee et al., 2007. Dosage compensation in the mouse balances up-regulation and silencing of X-linked genes. PLoS Biol. 5: 2809-2820
61. Lloyd, S. P., 1982. Least-squares quantization in PCM. IEEE Trans. Inf. Theory 28: 129-137
62. Loytynoja, A., and N. Goldman, 2005. An algorithm for progressive multiple alignment of sequences with insertions. Proc. Natl. Acad. Sci. USA 102: 10557-10562
63. Lucchesi, J. C., 1973. Dosage compensation in Drosophila. Annu. Rev. Genet. 7: 225-237
64. MacQueen, J., 1967. Some methods for classification and analysis of multivariate observations, pp. 281-297 in Proceedings of the Fifth Berkeley Symposium on Mathematical Statistics and Probability. University of California Press, Berkley, CA
65. Mank, J. E., 2009. Sex chromosomes and the evolution of sexual dimorphism: lessons from the genome. Am. Nat. 173: 141-150
66. Mank, J. E., and H. Ellegren, 2009a. All dosage compensation is local: gene-by-gene regulation of sex-biased expression on the chicken Z chromosome. Heredity 102: 312-320
67. Mank, J. E., and H. Ellegren, 2009b. Sex-linkage of sexually antagonistic genes is predicted by female, but not male, effects in birds. Evolution 63: 1464-1472
68. Mank, J. E., K. Nam, B. Brunstrom, and H. Ellegren, 2010. Ontogenetic complexity of sexual dimorphism and sexspecific selection. Mol. Biol. Evol. 27: 1570-1578
69. Mank, J. E., D. J. Hosken, and N. Wedell, 2011. Some inconvenient truths about sex chromosome dosage compensation and the potential role of sexual conflict. Evolution 65: 2133-2144
70. Meiklejohn, C. D., E. L. Landeen, J. M. Cook, S. B. Kingan, and D. C. Presgraves, 2011. Sex chromosome-specific regulation in the Drosophila male germline but little evidence for chromosomal dosage compensation or meiotic inactivation. PLoS Biol. 9: e1001126
71. Melamed, E., and A. P. Arnold, 2007. Regional differences in dosage compensation on the chicken Z chromosome. Genome Biol. 8: R202
72. Meunier, J., and L. Duret, 2004. Recombination drives the evolution of GC-content in the human genome. Mol. Biol. Evol. 21: 984-990
73. Moghadam, H. K., M. A. Pointer, A. E. Wright, S. Berlin, and J. E Mank, 2012. W chromosome expression responds to femalespecific selection. Proc. Natl. Acad. Sci. USA 109: 8207-8211
74. Morrow, E. H., A. D. Stewart, and W. R. Rice, 2008. Assessing the extent of genome-wide intralocus sexual conflict via experimentally enforced gender-limited selection. J. Evol. Biol. 21: 1046-1054
75. Muyle, A., N. Zemp, C. Deschamps, S. Mousset, A. Widmer et al., 2012. Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biol. 10: e1001308
76. Nam, K., and H. Ellegren, 2008. The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata. Genetics 180: 1131-1136
77. Ohno, S., 1967. Sex Chromosomes and Sex Linked Genes. Springer-Verlag, Berlin
78. Oliver, B., 2007. Sex, dose, and equality. PLoS Biol. 5: e340
79. Parisi, M., R. Nuttall, D. Naiman, G. Bouffard, J. Malley et al., 2003. Paucity of genes on the Drosophila X chromosome showing male-biased expression. Science 299: 697-700
80. Pessia, E., T. Makino, M. Bailly-Bechet, A. McLysaght, and G. A. B. Marais, 2012. Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proc. Natl. Acad. Sci. USA 109: 5346-5351
81. Pollack, J. R., T. Sorlie, C. M. Perou, C. A. Ress, S. S. Jeffrey et al., 2002. Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc. Natl. Acad. Sci. USA 99: 12963-12968
82. 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
83. Rice, W. R., 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38: 735-742
84. Ridley, M., 2003. Evolution. John Wiley & Sons, New York
85. Ross, M. T., D. V. Grafham, A. J. Coffey, S. Scherer, K. McLay et al., 2005. The DNA sequence of the human X chromosome. Nature 434: 325-337
86. Rozen, S., H. Skaletsky, J. D. Marszalek, P. J. Minx, and H. S. Cordum, 2003. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423: 873-876
87. Schoenmakers, S., E. Wassenaar, J. W. Hoogerbrugge, J. S. E. Laven, J. A. Grootegoed et al., 2009. Female meiotic sex chromosome inactivation in chicken. PLoS Genet. 5: e1000466
88. Slattery, J. P., L. Sanner-Wachter, and S. J. O'Brien, 2000. Novel gene conversion between X-Y homologues located in the nonrecombining region of the Y chromosome in Felidae (Mammalia). Proc. Natl. Acad. Sci. USA 97: 5307-5312
89. Storchova, R., and P. Divina, 2006. Nonrandom representation of sex-biased genes on chicken Z chromosome. J. Mol. Evol. 63: 676-681
90. Sturgill, D., Y. Zhang, M. Parisi, and B. Oliver, 2007. Demasculinization of X chromosomes in the Drosophila genus. Nature 450: 238-241
91. Suh, A., J. O. Kriegs, J. Brosius, and J. Schmitz, 2011. Retroposon insertions and the chronology of avian sex chromosome evolution. Mol. Biol. Evol. 28: 2993-2997
92. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei et al., 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739
93. Teranishi, M., Y. Shimada, T. Hori, O. Nakabayashi, T. Kikuchi et al., 2001. Transcripts of the MHM region on the chicken Z chromosome accumulate as non-coding RNA in the nucleus of female cells adjacent to the DMRT1 locus. Chromosome Res. 9: 147-165
94. Torres, E. M., B. R. Williams, and A. Amon, 2008. Aneuploidy: cells losing their balance. Genetics 179: 737-746
95. Toups, M. A., J. B. Pease, and M. W. Hahn, 2011. No excess gene movement is detected off the avian or lepidopteran Z chromosome. Genome Biol. Evol. 3: 1381-1390
96. Trapnell, C., B. A. Williams, G. Pertea, A. Mortazavi, G. Kwan et al., 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28: 511-515
97. Vibranovski, M. D., H. F. Lopes, T. L. Karr, and M. Long, 2009a. Stage-specific expression profiling of Drosophila spermatogenesis suggests that meiotic sex chromosome inactivation drives genomic relocation of testis-expressed genes. PLoS Genet. 5: e1000731
98. Vibranovski, M. D., Y. Zhang, and M. Long, 2009b. General gene movement off the X chromosome in the Drosophila genus. Genome Res. 19: 897-903
99. Vicoso, B., and B. Charlesworth, 2006. Evolution on the X chromosome: unusual patterns and processes. Nat. Rev. Genet. 7: 645-653
100. Vicoso, B., and D. Bachtrog, 2011. Lack of global dosage compensation in Schistosoma mansoni, a female-heterogametic parasite. Genome Biol. Evol. 3: 230-235
101. Warren, W. C., D. F. Clayton, H. Ellegren, A. P. Arnold, L. W. Hillier et al., 2010. The genome of a songbird. Nature 464: 757-762
102. Webster, M. T., E. Axelsson, and H. Ellegren, 2006. Strong regional biases in nucleotide substitution in the chicken genome. Mol. Biol. Evol. 23: 1203-1216
103. Yang, Z., 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24: 1586-1591
104. Zhang, Y. E., M. D. Vibranovski, B. H. Krinsky, and M. Long, 2010a. Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res. 20: 1526-1533
105. Zhang, Y. E., M. D. Vibranovski, P. Landback, G. A. B. Marais, and M. Long, 2010b. Chromosomal redistribution of male-biased genes in mammalian evolution with two bursts of gene gain on the X Chromosome. PLoS Biol. 8: e1000494
106. Zhou, Q., and D. Bachtrog, 2012. Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 337: 341-345