Cross-species chromosome painting can directly visualize syntenies between diverged karyotypes and, thus, increase our knowledge on avian genome evolution. DNA libraries of chicken (Gallus gallus, GGA) macrochromosomes 1 to 10 were hybridized to metaphase spreads of 9 different species from 3 different orders (Anseriformes, Gruiformes and Passeriformes). Depending on the analyzed species, GGA1–10 delineated 11 to 13 syntenic chromosome regions, indicating a high degree of synteny conservation. No exchange between the GGA macrochromosome complement and microchromosomes of the analyzed species was observed. GGA1 and GGA4 were distributed on 2 or 3 chromosomes each in some of the analyzed species, indicating rare evolutionary rearrangements between macrochromosomes. In all 6 analyzed species of Passeriformes, GGA1 was diverged on 2 macrochromosomes, representing a synapomorphic marker for this order. GGA4 was split on 2 chromosomes in most karyotypes, but syntenic to a single chromosome in blackcap (Passeriformes). GGA5/10 and also GGA8/9 associations on chromosomes were found to be important cytogenetic features of the Eurasian nuthatch (Passeriformes) karyotype. Fusion of GGA4 and GGA5 segments and of entire GGA6 and GGA7, respectively, was seen in the 2 analyzed species of Gruiformes. Consistent with the literature, our inter-species chromosome painting demonstrates remarkable conservation of macrochromosomal synteny over 100 million years of avian evolution. The low rate of rearrangements between macrochromosomes and the absence of detectable macrochromosome-microchromosome exchanges suggests a predominant role for rearrangements within the gene-dense microchromosome complement in karyotypic diversification.

1.
Ansari HA, Takagi N, Sasaki M: Interordinal conservatism of chromosome banding patterns in Gallus domesticus (Galliformes) and Melopsittacus undulatus (Psittaciformes). Cytogenet Cell Genet 43:6–9 (1986).
2.
Axelsson E, Webster MT, Smith NG, Burt DW, Ellegren H: Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes. Genome Res 15:120–125 (2005).
3.
Backström N, Karaiskou N, Leder EH, Gustafsson L, Primmer CR, et al: A gene-based genetic linkage map of the collared flycatcher (Ficedula albicollis) reveals extensive synteny and gene-order conservation during 100 million years of avian evolution. Genetics 179:1479–1495 (2008).
4.
Bed ’Hom B, Coullin P, Guillier-Gencik Z, Moulin S, Bernheim A, Volobouev V: Characterization of the atypical karyotype of the black winged kite Elanus caeruleus (Falconiformes: Accipitridae) by means of classical and molecular cytogenetic techniques. Chromosome Res 11:335–343 (2003).
5.
Bloom SE, Delaney ME, Muscarella DE: Constant and variable features of avian chromosomes, in Etches RJ, Gibbins AMV (eds): Manipulation of the Avian Genome, pp 39–60 (CRC Press, Boca Raton 1993).
6.
Burt DW: Origin and evolution of avian microchromosomes. Cytogenet Genome Res 96:97–112 (2002).
7.
Burt DW, Bruley C, Dunn IC, Jones CT, Ramage A, et al: The dynamics of chromosome evolution in birds and mammals. Nature 402:411–413 (1999).
8.
Chowdhary BP, Raudsepp T, Fronicke L, Scherthan H: Emerging patterns of comparative genome organization in some mammalian species as revealed by Zoo-FISH. Genome Res 8:577–589 (1998).
9.
Christidis L: Aves, in John B (ed): Animal Cytogenetics, Vol 4, Chordata 3 (Gebrüder Bornträger, Berlin 1990).
10.
De Boer LEM: The somatic chromosome complements of 16 species of Falconiformes (Aves) and the karyological relationships of the order. Genetica 46:77–113 (1976).
11.
de Oliveira EHC, Habermann FA, Lacerda O, Sbalqueiro IJ, Wienberg J, Müller S: 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 114:338–343 (2005).
12.
de Oliveira EH, de Moura SP, dos Anjos LJ, Nagamachi CY, Pieczarka JC, et al: Comparative chromosome painting between chicken and spectacled owl (Pulsatrix perspicillata): implications for chromosomal evolution in the Strigidae (Aves, Strigiformes). Cytogenet Genome Res 122:157–162 (2008).
13.
Derjusheva S, Kurganova A, Habermann F, Gaginskaya E: High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosome Res 12:715–723 (2004).
14.
Ericson PG, Anderson CL, Britton T, Elzanowski A, Johansson US, et al: Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2:543–547 (2006).
15.
Ferguson-Smith MA, Trifonov V: Mammalian karyotype evolution. Nat Rev Genet 8:950–962 (2007).
16.
Gordon L, Yang S, Tran-Gyamfi M, Baggott D, Christensen M, et al: Comparative analysis of chicken chromosome 28 provides new clues to the evolutionary fragility of gene-rich vertebrate regions. Genome Res 17:1603–1613 (2007).
17.
Grandy I, Hardt T, Schmid M, Haaf T: Effects of higher-order nuclear structure and Rad51 overexpression on radiation-induced chromosome rearrangements. Cytogenet Genome Res 98:265–269 (2002).
18.
Grant PR, Grant BR: Hybridization of bird species. Science 256:193–197 (1992).
19.
Griffin DK, Robertson LB, Tempest HG, Skinner BM: The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet Genome Res 117:64–77 (2007).
20.
Guttenbach M, Nanda I, Feichtinger W, Masabanda JS, Griffin DK, Schmid M: Comparative chromosome painting of chicken autosomal paints 1–9 in nine different bird species. Cytogenet Genome Res 103:173–184 (2003).
21.
Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, et al: Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res 9:569–584 (2001).
22.
Hale MC, Jensen H, Birkhead TR, Burke T, Slate J: A comparison of synteny and gene order on the homologue of chicken chromosome 7 between two passerine species and between passerines and chicken. Cytogenet Genome Res 121:120–129 (2008).
23.
Hammar B: The karyotypes of thirty-one birds. Hereditas 65:29–58 (1970).
24.
Hansmann T, Nanda I, Volobouev V, Yang F, Schartl M, et al: Cross-species chromosome painting corroborates microchromosome fusion during karyotype evolution of birds. Cytogenet Genome Res 126:281–304 (2009).
25.
Hansson B, Akesson M, Slate J, Pemberton JM: Linkage mapping reveals sex-dimorphic map distances in a passerine bird. Proc Biol Sci 272:2289–2298 (2005).
26.
Irestedt M, Johansson US, Parsons TJ, Ericson PGP: Phylogeny of major lineages of suboscines (Passeriformes) analysed by nuclear DNA sequence data. J Avian Biol 32:15–25 (2001).
27.
Itoh Y, Arnold AP: Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 13:47–56 (2005).
28.
Jaari S, Li MH, Merilä J: A first-generation microsatellite-based genetic linkage map of the Siberian jay (Perisoreus infaustus): insights into avian genome evolution. BMC Genomics 10:1 (2009).
29.
Kasai F, Garcia C, Arruga MV, Ferguson-Smith MA: Chromosome homology between chicken (Gallus gallus domesticus) and the red-legged partridge (Alectoris rufa); evidence of the occurrence of a neocentromere during evolution. Cytogenet Genome Res 102:326–330 (2003).
30.
Masabanda JS, Burt DW, O’Brien PC, Vignal A, Fillon V, et al: Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics 166:1367–1373 (2004).
31.
Matsuda Y, Nishida-Umehara C, Tarui H, Kuroiwa A, Yamada K, et al: Highly conserved linkage homology between birds and turtles: bird and turtle chromosomes are precise counterparts of each other. Chromosome Res 13:601–615 (2005).
32.
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 112:286–295 (2006).
33.
Nanda I, Karl E, Griffin DK, Schartl M, Schmid M: Chromosome repatterning in three representative parrots (Psittaciformes) inferred from comparative chromosome painting. Cytogenet Genome Res 117:43–53 (2007).
34.
Neusser M, Stanyon R, Bigoni F, Wienberg J, Müller S: Molecular cytotaxonomy of New World monkeys (Platyrrhini) – comparative analysis of five species by multi-color chromosome painting gives evidence for a classification of Callimico goeldii within the family of Callitrichidae. Cytogenet Cell Genet 94:206–215 (2001).
35.
Nie W, O’Brien PC, Ng BL, Fu B, Volobouev V, et al: 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. Chromosome Res 17:99–113 (2009).
36.
Nishida-Umehara C, Tsuda Y, Ishijima J, Ando J, Fujiwara A, et al: The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds. Chromosome Res 15:721–734 (2007).
37.
O’Brien SJ, Stanyon R: Ancestral primate viewed. Nature 402:365–366 (1999).
38.
Prager EM, Wilson AC: Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution. Proc Natl Acad Sci USA 72:200–204 (1975).
39.
Raikow RJ: Monophyly of the Passeriformes: test of a phylogenetic hypothesis. Auk 99:431–455 (1982).
40.
Raudsepp T, Houck ML, O’Brien PC, Ferguson-Smith MA, Ryder OA, Chowdhary BP: Cytogenetic analysis of California condor (Gymnogyps californianus) chromosomes: comparison with chicken (Gallus gallus) macrochromosomes. Cytogenet Genome Res 98:54–60 (2002).
41.
Scherthan H, Cremer T, Arnason U, Weier HU, Lima-de-Faria A, Frönicke L: Comparative chromosome painting discloses homologous segments in distantly related mammals. Nat Genet 6:342–347 (1994).
42.
Schmid M, Enderle E, Schindler D, Schempp W: Chromosome banding and DNA replication patterns in bird karyotypes. Cytogenet Cell Genet 52:139–146 (1989).
43.
Schmid M, Nanda I, Guttenbach M, Steinlein C, Hoehn M, et al: First report on chicken genes and chromosomes 2000. Cytogenet Cell Genet 90:169–218 (2000).
44.
Schmid M, Nanda I, Hoehn H, Schartl M, Haaf T, et al: Second report on chicken genes and chromosomes 2005. Cytogenet Genome Res 109:415–479 (2005).
45.
Shetty S, Griffin DK, Graves JAM: Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res 7:289–295 (1999).
46.
Shibusawa M, Nishibori M, Nishida-Umehara C, Tsudzuki M, Masabanda J, et al: Karyotypic evolution in the Galliformes: An examination of the process of karyotypic evolution by comparison of the molecular cytogenetic findings with the molecular phylogeny. Cytogenet Genome Res 106:111–119 (2004).
47.
Stanyon R, Arnold N, Koehler U, Bigoni F, Wienberg J: Chromosomal painting shows that ‘marked chromosomes’ in lesser apes and Old World monkeys are not homologous and evolved by convergence. Cytogenet Cell Genet 68:74–78 (1995).
48.
Stauss M, Tomiuk J, Segelbacher G, Driesel S, Fietz J, et al: Sex-specific recombination rates in Parus major and P. caeruleus, an exception to Huxley’s rule. Hereditas 139:199–205 (2003).
49.
Stock AD, Arrighi FE, Stefos K: Chromosome homology in birds: banding patterns of the chromosomes of the domestic chicken, ring-necked dove, and domestic pigeon. Cytogenet Cell Genet 13:410–418 (1974).
50.
Sumner AT: Simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306 (1972).
51.
Takagi N, Sasaki M: A phylogenetic study of bird karyotypes. Chromosoma 46:91–120 (1974).
52.
Telenius H, Pelmear AH, Tunnacliffe A, Carter NP, Behmel A, et al: Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4:257–263 (1992).
53.
van Tuinen M, Sibley CG, Hedges SB: The early history of modern birds inferred from DNA sequences of nuclear and mitochondrial ribosomal genes. Mol Biol Evol 17:451–457 (2000).
54.
Wienberg J: The evolution of eutherian chromosomes. Curr Opin Genet Dev 14:657–666 (2004).
55.
Yang F, Müller S, Just R, Ferguson-Smith MA, Wienberg J: Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis). Genomics 39:396–401 (1997).
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