Complex evolutionary trajectories of sex chromosomes across bird taxa

Science

Volumn 346, Issue 6215, 2014, Pages

  Zhou, Qi ^a   Zhang, Jilin ^b   Bachtrog, Doris ^a   An, Na ^b   Huang, Quanfei ^b   Jarvis, Erich D ^c   Gilbert, M Thomas P ^d,e   Zhang, Guojie ^b,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BGI SHENZHEN   (China)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e CURTIN UNIVERSITY   (Australia)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BIRD; CHROMOSOME; EVOLUTIONARY BIOLOGY; PHYLOGENETICS; RECOMBINATION;

ARTICLE; AUTOSOME; BIRD; CHROMOSOME INVERSION; EVOLUTION; FEMALE; FRAMESHIFT MUTATION; GENE EXPRESSION; GENE MAPPING; GENOME; HOMOLOGOUS RECOMBINATION; MALE; NONHUMAN; PHYLOGENETIC TREE; PROTEIN FUNCTION; PSEUDOGENE; SEQUENCE HOMOLOGY; SEX CHROMOSOMAL INHERITANCE; SEX CHROMOSOME; SEXUAL SELECTION; SRY GENE; STOP CODON; TRANSPOSON; X CHROMOSOME; Y CHROMOSOME; ANIMAL; CHICKEN; CHROMOSOME MAP; CLASSIFICATION; GENETIC RECOMBINATION; GENETICS; MOLECULAR EVOLUTION; OSTRICH; PHYLOGENY; SPECIES DIFFERENCE; SYNTENY;

AVES; MAMMALIA;

AVIAN PROTEIN; DMRT1 PROTEIN; TRANSCRIPTION FACTOR;

ANIMALS; AVIAN PROTEINS; BIOLOGICAL EVOLUTION; BIRDS; CHICKENS; CHROMOSOME INVERSION; CHROMOSOME MAPPING; EVOLUTION, MOLECULAR; FEMALE; MALE; PHYLOGENY; RECOMBINATION, GENETIC; SEX CHROMOSOMES; SPECIES SPECIFICITY; STRUTHIONIFORMES; SYNTENY; TRANSCRIPTION FACTORS;

EID: 84917708480     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1246338     Document Type: Article

References (50)

1. J. J. Bull, Evolution of Sex Determining Mechanisms (Benjamin/Cummings, Menlo Park, CA, 1983).
2. A. K. Fridolfsson et al., Evolution of the avian sex chromosomes from an ancestral pair of autosomes. Proc. Natl. Acad. Sci. U.S.A. 95, 8147-8152 (1998). doi: 10.1073/pnas.95.14.8147; pmid: 9653155
3. D. W. Bellott et al., Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466, 612-616 (2010). doi: 10.1038/nature09172; pmid: 20622855
4. D. Cortez et al., Origins and functional evolution of Y chromosomes across mammals. Nature 508, 488-493 (2014). doi: 10.1038/nature13151; pmid: 24759410
5. M. T. Ross et al., The DNA sequence of the human X chromosome. Nature 434, 325-337 (2005). doi: 10.1038/nature03440; pmid: 15772651
6. B. Charlesworth, D. Charlesworth, The degeneration of Y chromosomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1563-1572 (2000). doi: 10.1098/rstb.2000.0717; pmid: 11127901
7. H. Skaletsky et al., The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825-837 (2003). doi: 10.1038/nature01722; pmid: 12815422
8. W. R. Rice, The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes. Evolution 41, 911-914 (1987). doi: 10.2307/2408899
9. B. T. Lahn, D. C. Page, Four evolutionary strata on the human X chromosome. Science 286, 964-967 (1999). doi: 10.1126/science.286.5441.964; pmid: 10542153
10. K. Nam, H. Ellegren, The chicken (Gallus gallus) Z chromosome contains at least three nonlinear evolutionary strata. Genetics 180, 1131-1136 (2008). doi: 10.1534/genetics.108.090324; pmid: 18791248
11. G. Li et al., Comparative analysis of mammalian Y chromosomes illuminates ancestral structure and lineage-specific evolution. Genome Res. 23, 1486-1495 (2013). doi: 10.1101/gr.154286.112; pmid: 23788650
12. D. W. Bellott et al., Mammalian Y chromosomes retain widely expressed dosage-sensitive regulators. Nature 508, 494-499 (2014). doi: 10.1038/nature13206; pmid: 24759411
13. C. Lemaitre et al., Footprints of inversions at present and past pseudoautosomal boundaries in human sex chromosomes. Genome Biol. Evol. 1, 56-66 (2009). doi: 10.1093/gbe/evp006; pmid: 20333177
14. S. A. Sandstedt, P. K. Tucker, Evolutionary strata on the mouse X chromosome correspond to strata on the human X chromosome. Genome Res. 14, 267-272 (2004). doi: 10.1101/gr.1796204; pmid: 14762062
15. K. L. Ayers et al., RNA sequencing reveals sexually dimorphic gene expression before gonadal differentiation in chicken and allows comprehensive annotation of the W-chromosome. Genome Biol. 14, R26 (2013). doi: 10.1186/gb-2013-14-3-r26; pmid: 23531366
16. A. E. Wright, H. K. Moghadam, J. E. Mank, Trade-off between selection for dosage compensation and masculinization on the avian Z chromosome. Genetics 192, 1433-1445 (2012). doi: 10.1534/genetics.112.145102; pmid: 22997237
17. L. J. Handley, H. Ceplitis, H. Ellegren, Evolutionary strata on the chicken Z chromosome: Implications for sex chromosome evolution. Genetics 167, 367-376 (2004). doi: 10.1534/genetics.167.1.367; pmid: 15166161
18. H. Ellegren, A. Carmichael, Multiple and independent cessation of recombination between avian sex chromosomes. Genetics 158, 325-331 (2001). pmid: 11333240
19. R. S. de Kloet, S. R. de Kloet, Evolution of the spindlin gene in birds: Independent cessation of the recombination of sex chromosomes at the spindlin locus in neognathous birds and tinamous, a palaeognathous avian family. Genetica 119, 333-342 (2003). doi: 10.1023/B:GENE.0000003842.72339.df; pmid: 14686612
20. J. García-Moreno, D. P. Mindell, Rooting a phylogeny with homologous genes on opposite sex chromosomes (gametologs): A case study using avian CHD. Mol. Biol. Evol. 17, 1826-1832 (2000). doi: 10.1093/oxfordjournals.molbev. a026283; pmid: 11110898
21. J. Rutkowska, M. Lagisz, S. Nakagawa, The long and the short of avian W chromosomes: No evidence for gradual W shortening. Biol. Lett. 8, 636-638 (2012). doi: 10.1098/rsbl.2012.0083; pmid: 22417794
22. S. J. Hackett et al., A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763-1768 (2008). doi: 10.1126/science.1157704; pmid: 18583609
23. E. D. Jarvis et al., Whole genome analyses resolve the early branches to the tree of life of modern birds. Science 346, 1320-1331 (2014).
24. A. Ogawa, K. Murata, S. Mizuno, The location of Z-and W-linked marker genes and sequence on the homomorphic sex chromosomes of the ostrich and the emu. Proc. Natl. Acad. Sci. U.S.A. 95, 4415-4418 (1998). doi: 10.1073/pnas.95.8.4415; pmid: 9539751
25. C. Nishida-Umehara et al., Differentiation of Z and W chromosomes revealed by replication banding and FISH mapping of sex-chromosome-linked DNA markers in the cassowary (Aves, Ratitae). Chromosome Res. 7, 635-640 (1999). doi: 10.1023/A:1009236103013; pmid: 10628664
26. Y. Tsuda, C. Nishida-Umehara, J. Ishijima, K. Yamada, Y. Matsuda, 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 116, 159-173 (2007). doi: 10.1007/s00412-006-0088-y; pmid: 17219176
27. M. I. Pigozzi, Diverse stages of sex-chromosome differentiation in tinamid birds: Evidence from crossover analysis in Eudromia elegans and Crypturellus tataupa. Genetica 139, 771-777 (2011). doi: 10.1007/s10709-011-9581-1; pmid: 21567220
28. M. I. Pigozzi, Origin and evolution of the sex chromosomes in birds. Biocell 23, 79-95 (1999). pmid: 10904535
29. G. Zhang et al., Comparative genomics across modern bird species reveal insights into avian genome evolution and adaptation. Science 346, 1311-1320 (2014).
30. Y. Huang et al., The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat. Genet. 45, 776-783 (2013). doi: 10.1038/ng.2657; pmid: 23749191
31. B. Vicoso, V. B. Kaiser, D. Bachtrog, Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution. Proc. Natl. Acad. Sci. U.S.A. 110, 6453-6458 (2013). doi: 10.1073/pnas.1217027110; pmid: 23547111
32. L. Ye et al., A vertebrate case study of the quality of assemblies derived from next-generation sequences. Genome Biol. 12, R31 (2011). doi: 10.1186/gb-2011-12-3-r31; pmid: 21453517
33. W. L. Fan et al., Genome-wide patterns of genetic variation in two domestic chickens. Genome Biol. Evol. 5, 1376-1392 (2013). doi: 10.1093/gbe/evt097; pmid: 23814129
34. I. Nanda, K. Schlegelmilch, T. Haaf, M. Schartl, M. Schmid, 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 (2008). doi: 10.1159/000163092; pmid: 19096210
35. R. A. Dalloul et al., Multi-platform next-generation sequencing of the domestic turkey (Meleagris gallopavo): Genome assembly and analysis. PLOS Biol. 8, e1000475 (2010). doi: 10.1371/journal.pbio.1000475; pmid: 20838655
36. W. C. Warren et al., The genome of a songbird. Nature 464, 757-762 (2010). doi: 10.1038/nature08819; pmid: 20360741
37. H. Ellegren et al., The genomic landscape of species divergence in Ficedula flycatchers. Nature 491, 756-760 (2012). pmid: 23103876
38. C. A. Smith et al., The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461, 267-271 (2009). doi: 10.1038/nature08298; pmid: 19710650
39. S. Guioli, R. Lovell-Badge, J. M. Turner, Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line. PLOS Genet. 8, e1002560 (2012). doi: 10.1371/journal.pgen.1002560; pmid: 22412389
40. H. P. Yazdi, H. Ellegren, Old but not (so) degenerated-slow evolution of largely homomorphic sex chromosomes in ratites. Mol. Biol. Evol. 31, 1444-1453 (2014). doi: 10.1093/molbev/msu101; pmid: 24618361
41. J. Alföldi et al., The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477, 587-591 (2011). doi: 10.1038/nature10390; pmid: 21881562
42. K. R. Bradnam et al., Assemblathon 2: Evaluating de novo methods of genome assembly in three vertebrate species. Gigascience 2, 10 (2013). doi: 10.1186/2047-217X-2-10; pmid: 23870653
43. A. Kawai et al., Different origins of bird and reptile sex chromosomes inferred from comparative mapping of chicken Z-linked genes. Cytogenet. Genome Res. 117, 92-102 (2007). doi: 10.1159/000103169; pmid: 17675849
44. A. Kawai et al., The ZW sex chromosomes of Gekko hokouensis (Gekkonidae, Squamata) represent highly conserved homology with those of avian species. Chromosoma 118, 43-51 (2009). doi: 10.1007/s00412-008-0176-2; pmid: 18685858
45. S. Berlin, H. Ellegren, Fast accumulation of nonsynonymous mutations on the female-specific W chromosome in birds. J. Mol. Evol. 62, 66-72 (2006). doi: 10.1007/s00239-005-0067-6; pmid: 16320115
46. Y. Itoh, K. Kampf, A. P. Arnold, Disruption of FEM1C-W gene in zebra finch: Evolutionary insights on avian ZW genes. Chromosoma 118, 323-334 (2009). doi: 10.1007/s00412-008-0199-8; pmid: 19139913
47. J. F. Hughes et al., Strict evolutionary conservation followed rapid gene loss on human and rhesus Y chromosomes. Nature 483, 82-86 (2012). doi: 10.1038/nature10843; pmid: 22367542
48. D. Bachtrog, The temporal dynamics of processes underlying Y chromosome degeneration. Genetics 179, 1513-1525 (2008). doi: 10.1534/genetics.107.084012; pmid: 18562655
49. D. Charlesworth, B. Charlesworth, Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet. Res. 35, 205-214 (1980). doi: 10.1017/S0016672300014051; pmid: 6930353
50. M. A. Wilson Sayres, K. D. Makova, Gene survival and death on the human Y chromosome. Mol. Biol. Evol. 30, 781-787 (2013). doi: 10.1093/molbev/mss267; pmid: 23223713