Advertisement

Avian Chromosomal Evolution

  • Joana Damas
  • Rebecca E. O’Connor
  • Darren K. Griffin
  • Denis M. Larkin
Chapter

Abstract

An outstanding feature of avian karyotypes is an extraordinary degree of apparent similarity from one species to the next, with the majority of avian species exhibiting 2n = 74–86. Several exceptions to this rule include avian clades that have a large degree of chromosomal fusion and fission. In this chapter we describe patterns of avian chromosomal evolution, including likely associations between karyotype evolution and phenotype. We also describe novel approaches that will facilitate avian chromosome studies at molecular level to unravel the mystery of the significance of this very distinctive genomic structure.

Keywords

Avian karyotype Chromosome evolution Sex chromosomes Universal probes Macrochromosomes Microchromosomes Evolutionary breakpoint regions Rearrangements Genomes Chicken 

References

  1. Axelsson E, Webster MT, Smith NGC, Burt DW, Ellegren H (2005) Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Res 15:120–125PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ayala FJ, Coluzzi M (2005) Chromosome speciation: humans, drosophila, and mosquitoes. Proc Natl Acad Sci USA 102(Suppl 1):6535–6542PubMedCrossRefPubMedCentralGoogle Scholar
  3. Babarinde IA, Saitou N (2016) Genomic locations of conserved noncoding sequences and their proximal protein-coding genes in mammalian expression dynamics. Mol Biol Evol 33:1807–1817PubMedCrossRefPubMedCentralGoogle Scholar
  4. Baxevanis AD, Ouellette BFF (2004) Bioinformatics: a practical guide to the analysis of genes and proteins. Wiley, New YorkGoogle Scholar
  5. Beçak ML, Benirschke K, Hsu TC (1971) Chromosome atlas: fish, amphibians, reptiles and birds. Springer, BerlinCrossRefGoogle Scholar
  6. Bed’hom B, Vaez M, Coville J-L, Gourichon D, Chastel O, Follett S, Burke T, Minvielle F (2012) The lavender plumage colour in Japanese quail is associated with a complex mutation in the region of MLPH that is related to differences in growth, feed consumption and body temperature. BMC Genomics 13:442PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bellott DW, Skaletsky H, Pyntikova T, Mardis ER, Graves T, Kremitzki C, Brown LG, Rozen S, Warren WC, Wilson RK et al (2010) Convergent evolution of chicken Z and human X chromosomes by expansion and gene acquisition. Nature 466:612–616PubMedPubMedCentralCrossRefGoogle Scholar
  8. Benirschke K, Hsu TC, Becak ML, Becak W, Roberts FL, Shoffner RN, Volpe EP (1973) Chromosome atlas: fish, amphibians, reptiles, and birds. Springer, BerlinGoogle Scholar
  9. Benirschke K, Hsu TC, Becak ML, Becak W, Roberts FL, Shoffner RN, Volpe EP (1975) Chromosome atlas: fish, amphibians, reptiles and birds. Springer, BerlinCrossRefGoogle Scholar
  10. Brown JH, Hall CAS, Sibly RM (2018) Equal fitness paradigm explained by a trade-off between generation time and energy production rate. Nat Ecol Evol 2:262–268PubMedCrossRefPubMedCentralGoogle Scholar
  11. Burt DW (2001) Chromosome rearrangement in evolution. eLS. doi:  https://doi.org/10.1038/npg.els.0001500
  12. Burt DW (2002) Origin and evolution of avian microchromosomes. Cytogenet Genome Res 96:97–112PubMedCrossRefPubMedCentralGoogle Scholar
  13. Burt DW, Bruley C, Dunn IC, Jones CT, Ramage A, Law AS, Morrice DR, Paton IR, Smith J, Windsor D et al (1999) The dynamics of chromosome evolution in birds and mammals. Nature 402:411–413PubMedCrossRefGoogle Scholar
  14. Carbone L, Harris RA, Gnerre S, Veeramah KR, Lorente-Galdos B, Huddleston J, Meyer TJ, Herrero J, Roos C, Aken B et al (2014) Gibbon genome and the fast karyotype evolution of small apes. Nature 513:195–201PubMedPubMedCentralCrossRefGoogle Scholar
  15. Carvalho NDM, Arias FJ, da Silva FA, Schneider CH, Gross MC (2015) Cytogenetic analyses of five amazon lizard species of the subfamilies Teiinae and Tupinambinae and review of karyotyped diversity the family Teiidae. Comp Cytogenet 9:625–644PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chan JE, Kolodner RD (2011) A genetic and structural study of genome rearrangements mediated by high copy repeat Ty1 elements. PLoS Genet 7:e1002089PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chen N, Bellott DW, Page DC, Clark AG (2012) Identification of avian W-linked contigs by short-read sequencing. BMC Genomics 13:183PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chen S, Krinsky BH, Long M (2013) New genes as drivers of phenotypic evolution. Nat Rev Genet 14:645–660PubMedPubMedCentralCrossRefGoogle Scholar
  19. Christidis L (1990) Aves. In: John B et al (eds) Animal cytogenetics. Volume 4: Chordata 3 B. Gebrüder Borntraeger, BerlinGoogle Scholar
  20. Clarke J, Wu H-C, Jayasinghe L, Patel A, Reid S, Bayley H (2009) Continuous base identification for single-molecule nanopore DNA sequencing. Nat Nano 4:265–270CrossRefGoogle Scholar
  21. Coyle S, Kroll E (2008) Starvation induces genomic rearrangements and starvation-resilient phenotypes in yeast. Mol Biol Evol 25:310–318PubMedCrossRefPubMedCentralGoogle Scholar
  22. Damas J, O'Connor R, Farré M, Lenis VPE, Martell HJ, Mandawala A, Fowler K, Joseph S, Swain MT, Griffin DK et al (2017) Upgrading short-read animal genome assemblies to chromosome level using comparative genomics and a universal probe set. Genome Res 27:875–884PubMedPubMedCentralCrossRefGoogle Scholar
  23. Davis JK, Mittel LB, Lowman JJ, Thomas PJ, Maney DL, Martin CL, Thomas JW (2011) Haplotype-based genomic sequencing of a chromosomal polymorphism in the white-throated sparrow (Zonotrichia albicollis). J Hered 102:380–390PubMedPubMedCentralCrossRefGoogle Scholar
  24. de Oliveira EH, Habermann FA, Lacerda O, Sbalqueiro IJ, Wienberg J, Muller S (2005) Chromosome reshuffling in birds of prey: the karyotype of the world’s largest eagle (Harpy eagle, Harpia harpyja) compared to that of the chicken (Gallus gallus). Chromosoma 114:338–343PubMedCrossRefPubMedCentralGoogle Scholar
  25. De Smet WHO (1981) The nuclear Feulgen-DNA content of the vertebrates (especially reptiles), with notes on the cell and chromosome size. Acta Zool Pathol Antverp 76:119–167Google Scholar
  26. Deakin JE, Ezaz T (2014) Tracing the evolution of amniote chromosomes. Chromosoma 123:201–216PubMedPubMedCentralCrossRefGoogle Scholar
  27. Delany ME, Gessaro TM, Rodrigue KL, Daniels LM (2007) Chromosomal mapping of chicken mega-telomere arrays to GGA9, 16, 28 and W using a cytogenomic approach. Cytogenet Genome Res 117:54–63PubMedCrossRefPubMedCentralGoogle Scholar
  28. Derjusheva S, Kurganova A, Habermann F, Gaginskaya E (2004) High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosom Res 12:715–723CrossRefGoogle Scholar
  29. Dodgson JB, Delany ME, Cheng HH (2011) Poultry genome sequences: progress and outstanding challenges. Cytogenet Genome Res 134:19–26PubMedCrossRefPubMedCentralGoogle Scholar
  30. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, Rosenzweig F, Botstein D (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 99:16144–16149PubMedCrossRefGoogle Scholar
  31. Eid J, Fehr A, Gray J, Luong K, Lyle J, Otto G, Peluso P, Rank D, Baybayan P, Bettman B et al (2009) Real-time DNA sequencing from single polymerase molecules. Science 323:133–138PubMedCrossRefGoogle Scholar
  32. Ellegren H (2010) Evolutionary stasis: the stable chromosomes of birds. Trends Ecol Evol 25:283–291PubMedCrossRefGoogle Scholar
  33. Ezaz T, Srikulnath K, Graves JA (2017) Origin of amniote sex chromosomes: an ancestral super-sex chromosome, or common requirements? J Hered 108:94–105PubMedCrossRefPubMedCentralGoogle Scholar
  34. Farré M, Bosch M, López-Giráldez F, Ponsà M, Ruiz-Herrera A (2011) Assessing the role of tandem repeats in shaping the genomic architecture of great apes. PLoS One 6:e27239PubMedPubMedCentralCrossRefGoogle Scholar
  35. Farré M, Narayan J, Slavov GT, Damas J, Auvil L, Li C, Jarvis ED, Burt DW, Griffin DK, Larkin DM (2016) Novel insights into chromosome evolution in birds, archosaurs, and reptiles. Genome Biol Evol 8:2442–2451PubMedPubMedCentralCrossRefGoogle Scholar
  36. Graphodatsky AS, Trifonov VA, Stanyon R (2011) The genome diversity and karyotype evolution of mammals. Mol Cytogenet 4:22PubMedPubMedCentralCrossRefGoogle Scholar
  37. Graves JA (2013) How to evolve new vertebrate sex determining genes. Dev Dyn 242:354–359PubMedCrossRefPubMedCentralGoogle Scholar
  38. Graves JA (2014) Avian sex, sex chromosomes, and dosage compensation in the age of genomics. Chromosom Res 22:45–57CrossRefGoogle Scholar
  39. Gregory TR (2002) A bird’s-eye view of the c-value enigma: genome size, cell size, and metabolic rate in the class aves. Evolution 56:121–130PubMedCrossRefPubMedCentralGoogle Scholar
  40. Gregory TR (2005) The evolution of the genome. Elsevier Academic, Burlington, MAGoogle Scholar
  41. Gregory TR (2017) Animal genome size databaseGoogle Scholar
  42. Gregory TR, Andrews CB, McGuire JA, Witt CC (2009) The smallest avian genomes are found in hummingbirds. Proc R Soc B Biol Sci 276:3753–3757.  https://doi.org/10.1098/rspb.2009.1004 CrossRefGoogle Scholar
  43. Griffin DK, Haberman F, Masabanda J, O'Brien P, Bagga M, Sazanov A, Smith J, Burt DW, Ferguson-Smith M, Wienberg J (1999) Micro- and macrochromosome paints generated by flow cytometry and microdissection: tools for mapping the chicken genome. Cytogenet Cell Genet 87:278PubMedCrossRefGoogle Scholar
  44. Griffin DK, Robertson LB, Tempest HG, Skinner BM (2007) The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet Genome Res 117:64–77PubMedCrossRefGoogle Scholar
  45. Groenen MA, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF, Rogel-Gaillard C, Park C, Milan D, Megens HJ et al (2012) Analyses of pig genomes provide insight into porcine demography and evolution. Nature 491:393–398PubMedPubMedCentralCrossRefGoogle Scholar
  46. Guttenbach M, Nanda I, Feichtinger W, Masabanda JS, Griffin DK, Schmid M (2003) Comparative chromosome painting of chicken autosomal paints 1–9 in nine different bird species. Cytogenet Genome Res 103:173–184PubMedCrossRefGoogle Scholar
  47. Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, Bauer K, Wienberg J, Cremer C, Cremer T, Solovei I (2001) Arrangements of macro- and microchromosomes in chicken cells. Chromosom Res 9:569–584CrossRefGoogle Scholar
  48. Hansmann T, Nanda I, Volobouev V, Yang F, Schartl M, Haaf T, Schmid M (2009) Cross-species chromosome painting corroborates microchromosome fusion during karyotype evolution of birds. Cytogenet Genome Res 126:281–304PubMedCrossRefGoogle Scholar
  49. Harewood L, Fraser P (2014) The impact of chromosomal rearrangements on regulation of gene expression. Hum Mol Genet 23:R76–R82PubMedCrossRefGoogle Scholar
  50. Hughes AL, Friedman R (2008) Genome size reduction in the chicken has involved massive loss of ancestral protein-coding genes. Mol Biol Evol 25:2681–2688PubMedPubMedCentralCrossRefGoogle Scholar
  51. Itoh Y, Arnold AP (2005) Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosom Res 13:47–56CrossRefGoogle Scholar
  52. Itoh Y, Kampf K, Balakrishnan CN, Arnold AP (2011) Karyotypic polymorphism of the zebra finch Z chromosome. Chromosoma 120:255–264PubMedPubMedCentralCrossRefGoogle Scholar
  53. Jones BR, Rajaraman A, Tannier E, Chauve C (2012) ANGES: reconstructing ANcestral GEnomeS maps. Bioinformatics (Oxford, England) 28:2388–2390CrossRefGoogle Scholar
  54. Kapusta A, Suh A (2017) Evolution of bird genomes—a transposon’s-eye view. Ann N Y Acad Sci 1389:164–185PubMedCrossRefGoogle Scholar
  55. Kasai F, O'Brien PC, Martin S, Ferguson-Smith MA (2012) Extensive homology of chicken macrochromosomes in the karyotypes of Trachemys scripta elegans and Crocodylus niloticus revealed by chromosome painting despite long divergence times. Cytogenet Genome Res 136:303–307PubMedCrossRefGoogle Scholar
  56. Kawai A, Ishijima J, Nishida C, Kosaka A, Ota H, Kohno S, Matsuda Y (2009) The ZW sex chromosomes of Gekko hokouensis (Gekkonidae, Squamata) represent highly conserved homology with those of avian species. Chromosoma 118:43–51PubMedCrossRefGoogle Scholar
  57. Kim J, Farré M, Auvil L, Capitanu B, Larkin DM, Ma J, Lewin HA (2017) Reconstruction and evolutionary history of eutherian chromosomes. Proc Natl Acad Sci 114:E5379–E5388PubMedCrossRefGoogle Scholar
  58. Kim J, Larkin DM, Cai Q, Asan ZY, Ge R-L, Auvil L, Capitanu B, Zhang G, Lewin HA et al (2013) Reference-assisted chromosome assembly. Proc Natl Acad Sci 110:1785–1790PubMedCrossRefGoogle Scholar
  59. Kolmogorov M, Armstrong J, Raney BJ, Streeter I, Dunn M, Yang F, Odom D, Flicek P, Keane T, Thybert D et al (2016) Chromosome assembly of large and complex genomes using multiple references. bioRxiv.  https://doi.org/10.1101/088435
  60. Kolmogorov M, Raney B, Paten B, Pham S (2014) Ragout—a reference-assisted assembly tool for bacterial genomes. Bioinformatics (Oxford, England) 30:i302–i309CrossRefGoogle Scholar
  61. Korlach J, Gedman G, Kingan SB, Chin CS, Howard JT, Audet JN, Cantin L, Jarvis ED (2017) De novo PacBio long-read and phased avian genome assemblies correct and add to reference genes generated with intermediate and short reads. GigaScience 6:1–16PubMedPubMedCentralCrossRefGoogle Scholar
  62. Kupper C, Stocks M, Risse JE, Dos Remedios N, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI et al (2016) A supergene determines highly divergent male reproductive morphs in the ruff. Nat Genet 48:79–83PubMedCrossRefGoogle Scholar
  63. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedCrossRefGoogle Scholar
  64. Ledesma M, Freitas T, Da Silva J, Da Silva F, Gunski R (2003) Descripción cariotípica de Spheniscus magellanicus (Spheniscidae). Hornero 18:61–64Google Scholar
  65. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO et al (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293PubMedPubMedCentralCrossRefGoogle Scholar
  66. Lindblad-Toh K, Garber M, Zuk O, Lin MF, Parker BJ, Washietl S, Kheradpour P, Ernst J, Jordan G, Mauceli E et al (2011) A high-resolution map of human evolutionary constraint using 29 mammals. Nature 478:476–482PubMedPubMedCentralCrossRefGoogle Scholar
  67. Lithgow PE, O'Connor R, Smith D, Fonseka G, Al Mutery A, Rathje C, Frodsham R, O'Brien P, Kasai F, Ferguson-Smith MA et al (2014) Novel tools for characterising inter and intra chromosomal rearrangements in avian microchromosomes. Chromosom Res 22:85–97Google Scholar
  68. Lovell PV, Wirthlin M, Wilhelm L, Minx P, Lazar NH, Carbone L, Warren WC, Mello CV (2014) Conserved syntenic clusters of protein coding genes are missing in birds. Genome Biol 15:565PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lynch M (2007) The origins of genome architecture. Sinauer Associates, Sunderland, MAGoogle Scholar
  70. Ma J, Zhang L, Suh BB, Raney BJ, Burhans RC, Kent WJ, Blanchette M, Haussler D, Miller W (2006) Reconstructing contiguous regions of an ancestral genome. Genome Res 16:1557–1565PubMedPubMedCentralCrossRefGoogle Scholar
  71. Mak ACY, Lai YYY, Lam ET, Kwok T-P, Leung AKY, Poon A, Mostovoy Y, Hastie AR, Stedman W, Anantharaman T et al (2016) Genome-wide structural variation detection by genome mapping on nanochannel arrays. Genetics 202:351–362PubMedCrossRefPubMedCentralGoogle Scholar
  72. Masabanda JS, Burt DW, O’Brien PCM, Vignal A, Fillon V, Walsh PS, Cox H, Tempest HG, Smith J, Habermann F et al (2004) Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics 166:1367–1373PubMedPubMedCentralCrossRefGoogle Scholar
  73. Matsubara K, Tarui H, Toriba M, Yamada K, Nishida-Umehara C, Agata K, Matsuda Y (2006) Evidence for different origin of sex chromosomes in snakes, birds, and mammals and step-wise differentiation of snake sex chromosomes. Proc Natl Acad Sci 103:18190–18195PubMedCrossRefPubMedCentralGoogle Scholar
  74. Matsuda Y, Nishida-Umehara C, Tarui H, Kuroiwa A, Yamada K, Isobe T, Ando J, Fujiwara A, Hirao Y, Nishimura O et al (2005) Highly conserved linkage homology between birds and turtles: bird and turtle chromosomes are precise counterparts of each other. Chromosom Res 13:601–615CrossRefGoogle Scholar
  75. Moore JK, Haber JE (1996) Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol Cell Biol 16:2164–2173PubMedPubMedCentralCrossRefGoogle Scholar
  76. Murphy WJ, Larkin DM, Everts-van der Wind A, Bourque G, Tesler G, Auvil L, Beever JE, Chowdhary BP, Galibert F, Gatzke L et al (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309:613–617PubMedCrossRefPubMedCentralGoogle Scholar
  77. Nam K, Mugal C, Nabholz B, Schielzeth H, Wolf JB, Backstrom N, Kunstner A, Balakrishnan CN, Heger A, Ponting CP et al (2010) Molecular evolution of genes in avian genomes. Genome Biol 11:R68PubMedPubMedCentralCrossRefGoogle Scholar
  78. Nanda I, Benisch P, Fetting D, Haaf T, Schmid M (2011) Synteny conservation of chicken macrochromosomes 1-10 in different avian lineages revealed by cross-species chromosome painting. Cytogenet Genome Res 132:165–181PubMedCrossRefGoogle Scholar
  79. Nanda I, Karl E, Griffin DK, Schartl M, Schmid M (2007) Chromosome repatterning in three representative parrots (Psittaciformes) inferred from comparative chromosome painting. Cytogenet Genome Res 117:43–53PubMedCrossRefGoogle Scholar
  80. Nanda I, Shan Z, Schartl M, Burt DW, Koehler M, Nothwang H-G, Grutzner F, Paton IR, Windsor D, Dunn I et al (1999) 300 million years of conserved synteny between chicken Z and human chromosome 9. Nat Genet 21:258–259PubMedCrossRefPubMedCentralGoogle Scholar
  81. Nie W, O’Brien PC, Ng BL, Fu B, Volobouev V, Carter NP, Ferguson-Smith MA, Yang F (2009) Avian comparative genomics: reciprocal chromosome painting between domestic chicken (Gallus gallus) and the stone curlew (Burhinus oedicnemus, Charadriiformes)—an atypical species with low diploid number. Chromosom Res 17:99–113CrossRefGoogle Scholar
  82. Nishida C, Ishijima J, Kosaka A, Tanabe H, Habermann FA, Griffin DK, Matsuda Y (2008) Characterization of chromosome structures of Falconinae (Falconidae, Falconiformes, Aves) by chromosome painting and delineation of chromosome rearrangements during their differentiation. Chromosom Res 16:171–181CrossRefGoogle Scholar
  83. O’Hare TH, Delany ME (2009) Genetic variation exists for telomeric array organization within and among the genomes of normal, immortalized, and transformed chicken systems. Chromosom Res 17:947–964CrossRefGoogle Scholar
  84. O'Meally D, Ezaz T, Georges A, Sarre SD, Graves JA (2012) Are some chromosomes particularly good at sex? Insights from amniotes. Chromosom Res 20:7–19CrossRefGoogle Scholar
  85. Olmo E (2008) Trends in the evolution of reptilian chromosomes. Integr Comp Biol 48:486–493PubMedCrossRefPubMedCentralGoogle Scholar
  86. Organ CL, Moreno RG, Edwards SV (2008) Three tiers of genome evolution in reptiles. Integr Comp Biol 48:494–504PubMedPubMedCentralCrossRefGoogle Scholar
  87. Organ CL, Shedlock AM, Meade A, Pagel M, Edwards SV (2007) Origin of avian genome size and structure in non-avian dinosaurs. Nature 446:180–184PubMedCrossRefPubMedCentralGoogle Scholar
  88. Pigozzi MI (2016) The chromosomes of birds during meiosis. Cytogenet Genome Res 150:128–138PubMedCrossRefPubMedCentralGoogle Scholar
  89. Pokorna M, Giovannotti M, Kratochvil L, Caputo V, Olmo E, Ferguson-Smith MA, Rens W (2012) Conservation of chromosomes syntenic with avian autosomes in squamate reptiles revealed by comparative chromosome painting. Chromosoma 121:409–418PubMedCrossRefPubMedCentralGoogle Scholar
  90. Puerma E, Orengo DJ, Aguadé M (2016) The origin of chromosomal inversions as a source of segmental duplications in the Sophophora subgenus of Drosophila. Sci Rep 6:30715PubMedPubMedCentralCrossRefGoogle Scholar
  91. Putnam NH, O'Connell BL, Stites JC, Rice BJ, Blanchette M, Calef R, Troll CJ, Fields A, Hartley PD, Sugnet CW et al (2016) Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res 26:342–350PubMedPubMedCentralCrossRefGoogle Scholar
  92. Raudsepp T, Houck ML, O'Brien PC, Ferguson-Smith MA, Ryder OA, Chowdhary BP (2002) Cytogenetic analysis of California condor (Gymnogyps californianus) chromosomes: comparison with chicken (Gallus gallus) macrochromosomes. Cytogenet Genome Res 98:54–60PubMedCrossRefPubMedCentralGoogle Scholar
  93. Richards MP (2003) Genetic regulation of feed intake and energy balance in poultry. Poult Sci 82:907–916PubMedCrossRefPubMedCentralGoogle Scholar
  94. Romanov MN, Farré M, Lithgow PE, Fowler KE, Skinner BM, O’Connor R, Fonseka G, Backström N, Matsuda Y, Nishida C et al (2014) Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor. BMC Genomics 15:1–18CrossRefGoogle Scholar
  95. Ross MT, Grafham DV, Coffey AJ, Scherer S, McLay K, Muzny D, Platzer M, Howell GR, Burrows C, Bird CP et al (2005) The DNA sequence of the human X chromosome. Nature 434:325–337PubMedPubMedCentralCrossRefGoogle Scholar
  96. Rutkowska J, Lagisz M, Nakagawa S (2012) The long and the short of avian W chromosomes: no evidence for gradual W shortening. Biol Lett 8:636–638PubMedPubMedCentralCrossRefGoogle Scholar
  97. Scanes CG (2014) Sturkie’s avian physiology. Elsevier Science, AmsterdamGoogle Scholar
  98. Segura J, Ferretti L, Ramos-Onsins S, Capilla L, Farré M, Reis F, Oliver-Bonet M, Fernández-Bellón H, Garcia F, Garcia-Caldés M et al (2013) Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference. Proc R Soc B Biol Sci 280:20131945CrossRefGoogle Scholar
  99. Shang WH, Hori T, Toyoda A, Kato J, Popendorf K, Sakakibara Y, Fujiyama A, Fukagawa T (2010) Chickens possess centromeres with both extended tandem repeats and short non-tandem-repetitive sequences. Genome Res 20:1219–1228PubMedPubMedCentralCrossRefGoogle Scholar
  100. Shetty S, Griffin DK, Graves JA (1999) Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosom Res 7:289–295CrossRefGoogle Scholar
  101. Shibusawa M, Nishida-Umehara C, Masabanda J, Griffin DK, Isobe T, Matsuda Y (2002) Chromosome rearrangements between chicken and guinea fowl defined by comparative chromosome painting and FISH mapping of DNA clones. Cytogenet Genome Res 98:225–230PubMedCrossRefPubMedCentralGoogle Scholar
  102. Shields GF, Jarell GH, Redrupp E (1982) Enlarged sex chromosomes of woodpeckers (Piciformes). Auk 99:767–771Google Scholar
  103. Skinner BM, Griffin DK (2012) Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints. Heredity (Edinb) 108:37–41CrossRefGoogle Scholar
  104. Smeds L, Warmuth V, Bolivar P, Uebbing S, Burri R, Suh A, Nater A, Bureš S, Garamszegi LZ, Hogner S et al (2015) Evolutionary analysis of the female-specific avian W chromosome. Nat Commun 6:7330PubMedPubMedCentralCrossRefGoogle Scholar
  105. Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267–271PubMedCrossRefPubMedCentralGoogle Scholar
  106. Smith E, Shi L, Drummond P, Rodriguez L, Hamilton R, Powell E, Nahashon S, Ramlal S, Smith G, Foster J (2000) Development and characterization of expressed sequence tags for the turkey (Meleagris gallopavo) genome and comparative sequence analysis with other birds. Anim Genet 31:62–67PubMedCrossRefPubMedCentralGoogle Scholar
  107. Thomas JW, Cáceres M, Lowman JJ, Morehouse CB, Short ME, Baldwin EL, Maney DL, Martin CL (2008) The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455–1468PubMedPubMedCentralCrossRefGoogle Scholar
  108. Tiersch TR, Wachtel SS (1991) On the evolution of genome size of birds. J Hered 82:363–368PubMedCrossRefPubMedCentralGoogle Scholar
  109. Tomaszkiewicz M, Medvedev P, Makova KD (2017) Y and W chromosome assemblies: approaches and discoveries. Trends Genet 33:266–282PubMedCrossRefPubMedCentralGoogle Scholar
  110. Tuiskula-Haavisto M, Honkatukia M, Vilkki J, de Koning DJ, Schulman NF, Maki-Tanila A (2002) Mapping of quantitative trait loci affecting quality and production traits in egg layers. Poult Sci 81:919–927PubMedCrossRefPubMedCentralGoogle Scholar
  111. Ullastres A, Farré M, Capilla L, Ruiz-Herrera A (2014) Unraveling the effect of genomic structural changes in the rhesus macaque—implications for the adaptive role of inversions. BMC Genomics 15:530PubMedPubMedCentralCrossRefGoogle Scholar
  112. Uno Y, Nishida C, Tarui H, Ishishita S, Takagi C, Nishimura O, Ishijima J, Ota H, Kosaka A, Matsubara K et al (2012) Inference of the protokaryotypes of amniotes and tetrapods and the evolutionary processes of microchromosomes from comparative gene mapping. PLoS One 7:e53027PubMedPubMedCentralCrossRefGoogle Scholar
  113. Venturini G, D'Ambrogi R, Capanna E (1986) Size and structure of the bird genome—I. DNA content of 48 species of Neognathae. Comp Biochem Physiol B Comp Biochem 85:61–65CrossRefGoogle Scholar
  114. Volker M, Backstrom N, Skinner BM, Langley EJ, Bunzey SK, Ellegren H, Griffin DK (2010) Copy number variation, chromosome rearrangement, and their association with recombination during avian evolution. Genome Res 20:503–511PubMedPubMedCentralCrossRefGoogle Scholar
  115. Voss SR, Kump DK, Putta S, Pauly N, Reynolds A, Henry RJ, Basa S, Walker JA, Smith JJ (2011) Origin of amphibian and avian chromosomes by fission, fusion, and retention of ancestral chromosomes. Genome Res 21:1306–1312PubMedPubMedCentralCrossRefGoogle Scholar
  116. Warren WC, Hillier LW, Tomlinson C, Minx P, Kremitzki M, Graves T, Markovic C, Bouk N, Pruitt KD, Thibaud-Nissen F et al (2016) A new chicken genome assembly provides insight into avian genome structure. G3: Genes|Genomes|Genetics 7:109–117.  https://doi.org/10.1534/g3.116.035923 CrossRefPubMedCentralPubMedGoogle Scholar
  117. Wessler SR (2006) Transposable elements and the evolution of eukaryotic genomes. Proc Natl Acad Sci 103:17600–17601PubMedCrossRefPubMedCentralGoogle Scholar
  118. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, Vavouri T, Smith SF, North P, Callaway H, Kelly K et al (2004) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3:e7PubMedPubMedCentralCrossRefGoogle Scholar
  119. Wright NA, Gregory TR, Witt CC (2014) Metabolic ‘engines’ of flight drive genome size reduction in birds. Proc R Soc B Biol Sci 281:20132780CrossRefGoogle Scholar
  120. Wurster DH, Benirschke K (1970) Indian Muntjac, Muntiacus muntiak: a deer with a low diploid chromosome number. Science 168:1364–1366PubMedCrossRefPubMedCentralGoogle Scholar
  121. Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA, Fang X, Wynne JW, Xiong Z, Baker ML, Zhao W et al (2013) Comparative analysis of bat genomes provides insight into the evolution of flight and immunity. Science 339:456–460PubMedCrossRefPubMedCentralGoogle Scholar
  122. Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW et al (2014) Comparative genomics reveals insights into avian genome evolution and adaptation. Science (New York, NY) 346:1311–1320CrossRefGoogle Scholar
  123. Zhang J, Li C, Zhou Q, Zhang G (2015) Improving the ostrich genome assembly using optical mapping data. GigaScience 4:24PubMedPubMedCentralGoogle Scholar
  124. Zheng GXY, Lau BT, Schnall-Levin M, Jarosz M, Bell JM, Hindson CM, Kyriazopoulou-Panagiotopoulou S, Masquelier DA, Merrill L, Terry JM et al (2016) Haplotyping germline and cancer genomes with high-throughput linked-read sequencing. Nat Biotech 34:303–311CrossRefGoogle Scholar
  125. Zinzow-Kramer WM, Horton BM, McKee CD, Michaud JM, Tharp GK, Thomas JW, Tuttle EM, Yi S, Maney DL (2015) Genes located in a chromosomal inversion are correlated with territorial song in white-throated sparrows. Genes Brain Behav 14:641–654PubMedPubMedCentralCrossRefGoogle Scholar
  126. Zlotina A, Galkina S, Krasikova A, Crooijmans RP, Groenen MA, Gaginskaya E, Deryusheva S (2012) Centromere positions in chicken and Japanese quail chromosomes: de novo centromere formation versus pericentric inversions. Chromosom Res 20:1017–1032CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Joana Damas
    • 1
  • Rebecca E. O’Connor
    • 2
  • Darren K. Griffin
    • 2
  • Denis M. Larkin
    • 1
  1. 1.Department of Comparative Biomedical Sciences, Royal Veterinary CollegeUniversity of LondonLondonUK
  2. 2.School of BiosciencesUniversity of KentCanterburyUK

Personalised recommendations