Temporal genomic evolution of bird sex chromosomes

BMC Evolutionary Biology

Volumn 14, Issue 1, 2014, Pages

  Wang, Zongji ^a,b   Zhang, Jilin ^b   Yang, Wei ^b   An, Na ^b   Zhang, Pei ^b   Zhang, Guojie ^b,c   Zhou, Qi ^d  

^a SOUTH CHINA UNIVERSITY OF TECHNOLOGY   (China)

^b BGI SHENZHEN   (China)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Avian genome; Dosage compensation; Evolutionary strata; Fast Z evolution; Male driven evolution

Indexed keywords

BIRD; CHROMOSOME; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; GENETIC DRIFT; GENOMICS;

AVES; MAMMALIA;

TRANSCRIPTOME;

ANIMAL; BIRD; CHICKEN; CLASSIFICATION; DNA BASE COMPOSITION; EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GENOME; MALE; SEX CHROMOSOME;

ANIMALS; BASE COMPOSITION; BIOLOGICAL EVOLUTION; BIRDS; CHICKENS; DOSAGE COMPENSATION, GENETIC; FEMALE; GENOME; MALE; SEX CHROMOSOMES; TRANSCRIPTOME;

EID: 84923902306     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/s12862-014-0250-8     Document Type: Article

References (91)

1. Bull JJ: Evolution of Sex Determining Mechanisms. San Francisco: The Benjamin/Cummings Publishing Company, Inc.; 1983.
2. Bellott DW, Skaletsky H, Pyntikova T, Mardis ER, Graves T, Kremitzki C, Brown LG, Rozen S, Warren WC, Wilson RK, Page DC: Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 2010, 466 (7306):612-616.
3. Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grutzner F, Kaessmann H: Origins and functional evolution of Y chromosomes across mammals. Nature 2014, 508(7497):488-493.
4. Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, Gilbert MTP, Zhang G: Sex chromosomes demonstrate complex evolutionary trajectories across bird taxa. Science 2014, in press.
5. Lahn BT, Page DC: Four evolutionary strata on the human X chromosome. Science 1999, 286(5441):964-967.
6. Nam K, Ellegren H: The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata. Genetics 2008, 180(2):1131-1136.
7. Roesti M, Moser D, Berner D: Recombination in the threespine stickleback genome-patterns and consequences. Mol Ecol 2013, 22 (11):3014-3027.
8. Bergero R, Qiu S, Forrest A, Borthwick H, Charlesworth D: Expansion of the pseudo-autosomal region and ongoing recombination suppression in the Silene latifolia sex chromosomes. Genetics 2013, 194(3):673-686.
9. Natri HM, Shikano T, Merila J: Progressive recombination suppression and differentiation in recently evolved neo-sex chromosomes. Mol Biol Evol 2013, 30(5):1131-1144.
10. Vicoso B, Charlesworth B: Evolution on the X chromosome: unusual patterns and processes. Nat Rev Genet 2006, 7(8):645-653.
11. Ellegren H: Sex-chromosome evolution: recent progress and the influence of male and female heterogamety. Nat Rev Genet 2011, 12(3):157-166.
12. Xu K, Oh S, Park T, Presgraves DC, Yi SV: Lineage-specific variation in slowand fast-X evolution in primates. Evolution 2012, 66(6):1751-1761.
13. Lu J, Wu CI: Weak selection revealed by the whole-genome comparison of the X chromosome and autosomes of human and chimpanzee. Proc Natl Acad Sci U S A 2005, 102 (11):4063-4067.
14. Li WH, Yi S, Makova K: Male-driven evolution. Curr Opin Genet Dev 2002, 12(6):650-656.
15. Charlesworth B, Coyne J, Barton N: The relative rates of evolution of sex chromosomes and autosomes. Am Nat 1987, 130:113-146.
16. Meisel RP, Connallon T: The faster-X effect: integrating theory and data. Trends Genet 2013, 29(9):537-544.
17. Nielsen R, Bustamante C, Clark AG, Glanowski S, Sackton TB, Hubisz MJ, Fledel-Alon A, Tanenbaum DM, Civello D, White TJ, JS J, Adams MD, Cargill M: A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol 2005, 3 (6):e170.
18. Hvilsom C, Qian Y, Bataillon T, Li Y, Mailund T, Salle B, Carlsen F, Li R, Zheng H, Jiang T, Jiang H, Jin X, Munch K, Hobolth A, Siegismund HR, Wang J, Schierup MH: Extensive X-linked adaptive evolution in central chimpanzees. Proc Natl Acad Sci U S A 2012, 109(6):2054-2059.
19. Torgerson DG, Singh RS: Enhanced adaptive evolution of spermexpressed genes on the mammalian X chromosome. Heredity 2006, 96(1):39-44.
20. Torgerson DG, Singh RS: Sex-linked mammalian sperm proteins evolve faster than autosomal ones. Mol Biol Evol 2003, 20(10):1705-1709.
21. Sturgill D, Zhang Y, Parisi M, Oliver B: Demasculinization of X chromosomes in the Drosophila genus. Nature 2007, 450(7167):238-241.
22. Zhang YE, Vibranovski MD, Landback P, Marais GA, Long M: Chromosomal redistribution of male-biased genes in mammalian evolution with two bursts of gene gain on the X chromosome. PLoS Biol 2010, 8(10):e1000494.
23. Wu CI, Xu EY: Sexual antagonism and X inactivation-the SAXI hypothesis. Trends Genet 2003, 19(5):243-247.
24. Potrzebowski L, Vinckenbosch N, Marques AC, Chalmel F, Jegou B, Kaessmann H: Chromosomal gene movements reflect the recent origin and biology of therian sex chromosomes. PLoS Biol 2008, 6(4):e80.
25. Vicoso B, Charlesworth B: The deficit of male-biased genes on the d-melanogaster x chromosome is expression-dependent: a consequence of dosage compensation? J Mol Evol 2009, 68(5):576-583.
26. Bachtrog D, Toda NR, Lockton S: Dosage compensation and demasculinization of X chromosomes in Drosophila. Curr Biol 2010, 20(16):1476-1481.
27. Guioli S, Lovell-Badge R, Turner JM: Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line. PLoS Genet 2012, 8 (3):e1002560.
28. Itoh Y, Replogle K, Kim YH, Wade J, Clayton DF, Arnold AP: Sex bias and dosage compensation in the zebra finch versus chicken genomes: general and specialized patterns among birds. Genome Res 2010, 20(4):512-518.
29. Schoenmakers S, Wassenaar E, Hoogerbrugge JW, Laven JS, Grootegoed JA, Baarends WM: Female meiotic sex chromosome inactivation in chicken. PLoS Genet 2009, 5(5):e1000466.
30. Ellegren H, Fridolfsson AK: Male-driven evolution of DNA sequences in birds. Nat Genet 1997, 17(2):182-184.
31. Axelsson E, Smith NG, Sundstrom H, Berlin S, Ellegren H: Male-biased mutation rate and divergence in autosomal, Z-linked and W-linked introns of chicken and Turkey. Mol Biol Evol 2004, 21(8):1538-1547.
32. Mank JE, Axelsson E, Ellegren H: Fast-X on the Z: rapid evolution of sex-linked genes in birds. Genome Res 2007, 17 (5):618-624.
33. Mank JE, Nam K, Ellegren H: Faster-Z evolution is predominantly due to genetic drift. Mol Biol Evol 2010, 27(3):661-670.
34. Mank JE, Vicoso B, Berlin S, Charlesworth B: Effective population size and the faster-X effect: empirical results and their interpretation. Evolution 2010, 64(3):663-674.
35. Vicoso B, Charlesworth B: Effective population size and the faster-X effect: an extended model. Evolution 2009, 63(9):2413-2426.
36. Tsuda Y, Nishida-Umehara C, Ishijima J, Yamada K, Matsuda Y: Comparison of the Z and W sex chromosomal architectures in elegant crested tinamou (Eudromia elegans) and ostrich (Struthio camelus) and the process of sex chromosome differentiation in palaeognathous birds. Chromosoma 2007, 116(2):159-173.
37. Ayers KL, Davidson NM, Demiyah D, Roeszler KN, Grutzner F, Sinclair AH, Oshlack A, Smith CA: RNA sequencing reveals sexually dimorphic gene expression before gonadal differentiation in chicken and allows comprehensive annotation of the W-chromosome. Genome Biol 2013, 14(3):R26.
38. Zhang G, Li C, Li Q, Wang Z, Jarvis E, Gilbert T: Comparative genomics across modern bird species reveal insights into avian genome evolution and adaptation. Science 2014, in press.
39. Julien P, Brawand D, Soumillon M, Necsulea A, Liechti A, Schutz F, Daish T, Grutzner F, Kaessmann H: Mechanisms and evolutionary patterns of mammalian and avian dosage compensation. PLoS Biol 2012, 10 (5):e1001328.
40. Adolfsson S, Ellegren H: Lack of dosage compensation accompanies the arrested stage of sex chromosome evolution in ostriches. Mol Biol Evol 2013, 30(4):806-810.
41. Vicoso B, Kaiser VB, Bachtrog D: Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc Natl Acad Sci U S A 2013, 110(16):6453-6458.
42. Wright AE, Moghadam HK, Mank JE: Trade-off between selection for dosage compensation and masculinization on the avian Z chromosome. Genetics 2012, 192(4):1433-1445.
43. Jarvis E, Warnow T, Mirarab S, Houde P, Cracraft J, Boussau B, Howard J, Zhang G, Gilbert T: Whole genome analyses resolve the early branches to the tree of life of modern birds. Science 2014, in press.
44. Nanda I, Schlegelmilch K, Haaf T, Schartl M, Schmid M: 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 2008, 122 (2):150-156.
45. Shetty S, Griffin DK, Graves JA: Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res 1999, 7(4):289-295.
46. Derjusheva S, Kurganova A, Habermann F, Gaginskaya E: High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res 2004, 12(7):715-723.
47. Nanda I, Benisch P, Fetting D, Haaf T, Schmid M: Synteny conservation of chicken macrochromosomes 1-10 in different avian lineages revealed by cross-species chromosome painting. Cytogenet Genome Res 2011, 132(3):165-181.
48. Nanda I, Karl E, Volobouev V, Griffin DK, Schartl M, Schmid M: Extensive gross genomic rearrangements between chicken and Old World vultures (Falconiformes: Accipitridae). Cytogenet Genome Res 2006, 112(3-4):286-295.
49. Nishida C, Ishijima J, Kosaka A, Tanabe H, Habermann FA, Griffin DK, Matsuda Y: Characterization of chromosome structures of Falconinae (Falconidae, Falconiformes, Aves) by chromosome painting and delineation of chromosome rearrangements during their differentiation. Chromosome Res 2008, 16(1):171-181.
50. Burt DW: Origin and evolution of avian microchromosomes. Cytogenet Genome Res 2002, 96(1-4):97-112.
51. Miyata T, Hayashida H, Kuma K, Mitsuyasu K, Yasunaga T: Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb Symp Quant Biol 1987, 52:863-867.
52. Carmichael AN, Fridolfsson AK, Halverson J, Ellegren H: Male-biased mutation rates revealed from Z and W chromosome-linked ATP synthase alpha-subunit (ATP5A1) sequences in birds. J Mol Evol 2000, 50(5):443-447.
53. Bartosch-Harlid A, Berlin S, Smith NG, Moller AP, Ellegren H: Life history and the male mutation bias. Evolution 2003, 57(10):2398-2406.
54. Smith SA, Donoghue MJ: Rates of molecular evolution are linked to life history in flowering plants. Science 2008, 322(5898):86-89.
55. Wilson Sayres MA, Venditti C, Pagel M, Makova KD: Do variations in substitution rates and male mutation bias correlate with life-history traits? A study of 32 mammalian genomes. Evolution 2011, 65 (10):2800-2815.
56. Nikolaev SI, Montoya-Burgos JI, Popadin K, Parand L, Margulies EH, Antonarakis SE, Program N: Life-history traits drive the evolutionary rates of mammalian coding and noncoding genomic elements. Proc Natl Acad Sci U S A 2007, 104(51):20443-20448.
57. Jamieson BG: Reproductive Biology and Phylogeny of Birds. London: CRC Press; 2007.
58. International Chicken Genome Sequencing C: Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 2004, 432(7018):695-716.
59. Zhou Q, Bachtrog D: Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 2012, 337(6092):341-345.
60. Singh ND, Davis JC, Petrov DA: X-linked genes evolve higher codon bias in Drosophila and Caenorhabditis. Genetics 2005, 171(1):145-155.
61. Charlesworth B: The effect of life-history and mode of inheritance on neutral genetic variability. Genet Res 2001, 77(2):153-166.
62. Webster MT, Axelsson E, Ellegren H: Strong regional biases in nucleotide substitution in the chicken genome. Mol Biol Evol 2006, 23(6):1203-1216.
63. Rao Y, Wu G, Wang Z, Chai X, Nie Q, Zhang X: Mutation bias is the driving force of codon usage in the Gallus gallus genome. DNA Res 2011, 18(6):499-512.
64. Grath S, Parsch J: Rate of amino acid substitution is influenced by the degree and conservation of male-biased transcription over 50 myr of Drosophila evolution. Genome Biol Evol 2012, 4(3):346-359.
65. Vicoso B, Emerson JJ, Zektser Y, Mahajan S, Bachtrog D: Comparative sex chromosome genomics in snakes: differentiation, evolutionary strata, and lack of global dosage compensation. PLoS Biol 2013, 11(8):e1001643.
66. Sackton TB, Corbett-Detig RB, Nagaraju J, Vaishna L, Arunkumar KP, Hartl DL: Positve selection drives faster-Z evolution in silkmoths. Evolution 2014, 68(8):2331-2342.
67. Dunn PO, Whittingham LA, Pitcher TE: Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 2001, 55 (1):161-175.
68. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH: The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 2009, 461(7261):267-271.
69. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Kunstner A, Searle S, White S, Vilella AJ, Fairley S, Heger A, Kong L, Ponting CP, Jarvis ED, Mello CV, Minx P, Lovell P, Velho TA, Ferris M, Balakrishnan CN, Sinha S, Blatti C, London SE, Li Y, Lin YC, George J, Sweedler J, Southey B, Gunaratne P, Watson M, et al: The genome of a songbird. Nature 2010, 464 (7289):757-762.
70. Stenberg P, Larsson J: Buffering and the evolution of chromosome-wide gene regulation. Chromosoma 2011, 120 (3):213-225.
71. Liu K, Raghavan S, Nelesen S, Linder CR, Warnow T: Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees. Science 2009, 324(5934):1561-1564.
72. Yang Z: PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24(8):1586-1591.
73. Miyata T, Hayashida H, Kuma K, Mitsuyasu K, Yasunaga T: Male-driven molecular evolution: a model and nucleotide sequence analysis. In Cold Spring Harbor Symposia on Quantitative Biology. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1987:863-867.
74. McNab BK: Ecological factors affect the level and scaling of avian BMR. Comp Biochem Physiol A Mol Integr Physiol 2009, 152(1):22-45.
75. Calhim S, Birkhead TR: Testes size in birds: quality versus quantity-assumptions, errors, and estimates. Behav Ecol 2007, 18(1):271-275.
76. Pagel M: Inferring the historical patterns of biological evolution. Nature 1999, 401(6756):877-884.
77. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, Tang J, Wu G, Zhang H, Shi Y, Liu Y, Yu C, Wang B, Lu Y, Han C, Cheung DW, Yiu SM, Peng S, Xiaoqian Z, Liu G, Liao X, Li Y, Yang H, Wang J, Lam TW, Wang J: SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. Giga Sci 2012, 1(1):18.
78. Charlesworth D, Charlesworth B, Marais G: Steps in the evolution of heteromorphic sex chromosomes. Heredity 2005, 95(2):118-128.
79. Vicario S, Moriyama EN, Powell JR: Codon usage in twelve species of Drosophila. BMC Evol Biol 2007, 7:226.
80. Qiu S, Bergero R, Zeng K, Charlesworth D: Patterns of codon usage bias in Silene latifolia. Mol Biol Evol 2011, 28(1):771-780.
81. Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Odeen A, Cui J, Zhou Q, Xu L, Pan H, Wang Z, Jin L, Zhang P, Hu H, Yang W, Hu J, Xiao J, Yang Z, Liu Y, Xie Q, Yu H, Lian J,Wen P, Zhang F, Li H, et al: Comparative genomics reveals insights into avian genome evolution and adaptation. Science 2014, in press.
82. Talavera G, Castresana J: Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56(4):564-577.
83. Axelsson E, Hultin-Rosenberg L, Brandstrom M, Zwahlen M, Clayton DF, Ellegren H: Natural selection in avian protein-coding genes expressed in brain. Mol Ecol 2008, 17(12):3008-3017.
84. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T: Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011, 27(3):431-432.
85. Langmead B, Salzberg SL: Fast gapped-read alignment with Bowtie 2. Nat Methods 2012, 9 (4):357-359.
86. Li R, Li Y, Fang X, Yang H, Wang J, Kristiansen K, Wang J: SNP detection for massively parallel whole-genome resequencing. Genome Res 2009, 19(6):1124-1132.
87. Cingolani P, Platts A, le Wang L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM: A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 2012, 6(2):80-92.
88. Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, Albert FW, Zeller U, Khaitovich P, Grutzner F, Bergmann S, Nielsen R, Paabo S, Kaessmann H: The evolution of gene expression levels in mammalian organs. Nature 2011, 478 (7369):343-348.
89. Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25(9):1105-1111.
90. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L: Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010, 28(5):511-515.
91. Xie Y, Wu G, Tang J, Luo R, Patterson J, Liu S, Huang W, He G, Gu S, Li S, Zhou X, Lam TW, Li Y, Xu X, Wong GK, Wang J: SOAPdenovo-Trans: de novo transcriptome assembly with short RNA-Seq reads. Bioinformatics 2014, 30(12):1660-1666.