Advertisement

Genetica

, Volume 143, Issue 5, pp 535–543 | Cite as

Intrachromosomal rearrangements in two representatives of the genus Saltator (Thraupidae, Passeriformes) and the occurrence of heteromorphic Z chromosomes

  • Michelly da Silva dos Santos
  • Rafael Kretschmer
  • Fabio Augusto Oliveira Silva
  • Mario Angel Ledesma
  • Patricia C. M. O’Brien
  • Malcolm A. Ferguson-Smith
  • Analía Del Valle Garnero
  • Edivaldo Herculano Corrêa de Oliveira
  • Ricardo José Gunski
Article

Abstract

Saltator is a genus within family Thraupidae, the second largest family of Passeriformes, with more than 370 species found exclusively in the New World. Despite this, only a few species have had their karyotypes analyzed, most of them only with conventional staining. The diploid number is close to 80, and chromosome morphology is similar to the usual avian karyotype. Recent studies using cross-species chromosome painting have shown that, although the chromosomal morphology and number are similar to many species of birds, Passeriformes exhibit a complex pattern of paracentric and pericentric inversions in the chromosome homologous to GGA1q in two different suborders, Oscines and Suboscines. Hence, considering the importance and species richness of Thraupidae, this study aims to analyze two species of genus Saltator, the golden-billed saltator (S. aurantiirostris) and the green-winged saltator (S. similis) by means of classical cytogenetics and cross-species chromosome painting using Gallus gallus and Leucopternis albicollis probes, and also 5S and 18S rDNA and telomeric sequences. The results show that the karyotypes of these species are similar to other species of Passeriformes. Interestingly, the Z chromosome appears heteromorphic in S. similis, varying in morphology from acrocentric to metacentric. 5S and 18S probes hybridize to one pair of microchromosomes each, and telomeric sequences produce signals only in the terminal regions of chromosomes. FISH results are very similar to the Passeriformes already analyzed by means of molecular cytogenetics (Turdus species and Elaenia spectabilis). However, the paracentric and pericentric inversions observed in Saltator are different from those detected in these species, an observation that helps to explain the probable sequence of rearrangements. As these rearrangements are found in both suborders of Passeriformes (Oscines and Suboscines), we propose that the fission of GGA1 and inversions in GGA1q have occurred very early after the radiation of this order.

Keywords

Oscines Suboscines FISH C-banding Inversion 

Notes

Acknowledgments

The authors are grateful to the Animal Diversity Research Group (UNIPAMPA) and Pró-Reitoria de Pesquisa (PROPESQ/UNIPAMPA), CAPES, CNPq, SISBIO and Instituto Evandro Chagas for financial and logistic support, and a grant to MAFS from the Welcome Trust in support of the Cambridge Resource Centre for Comparative Genomics.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Alföldi J, Di Palma F, Grabherr M, Williams C, Kong L, Mauceli E et al (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477:587–591PubMedCentralCrossRefPubMedGoogle Scholar
  2. Aslam ML, Bastiaansen JWM, Crooijmans RPMA, Vereijken A, Megens HJ, Groenen MAM (2010) A SNP based linkage map of the turkey genome reveals multiple intrachromosomal rearrangements between the Turkey and Chicken genomes. BMC Genomics 11:647PubMedCentralCrossRefPubMedGoogle Scholar
  3. Barbosa MO, Da Silva RR, Correia VCS, Dos Santos LP, Garnero AV, Gunski RJ (2013) Nucleolar organizer regions in Sittasomus griseicapillus and Lepidocolaptes angustirostris (Aves, Dendrocolaptidae): evidence of a chromosome inversion. Genet Mol Biol 36(1):70–73CrossRefGoogle Scholar
  4. Barker FK, Barrowclough GF, Groth JG (2002) A phylogenetic hypothesis for passerine birds: taxonomic and biogeographic implications of an analysis of nuclear DNA sequence data. Proc Biol Sci 269(1488):295–308PubMedCentralCrossRefPubMedGoogle Scholar
  5. Burns KJ, Shultz AJ, Title PO, Mason NA, Barker FK, Klicka J, Lanyon SM, Lovette IJ (2014) Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest radiation of Neotropical songbirds. Mol Phylogenet Evol 75:41–77CrossRefPubMedGoogle Scholar
  6. Castro MS, Recco-Pimentel SM, Rocha GT (2002) Karyotypic characterization of Ramphastidae (Piciformes, Aves). Genet Mol Biol 25:147–150CrossRefGoogle Scholar
  7. Christidis L (1990) Animal cytogenetics, 4: Chordata 3 B. Aves. Gebrüder Borntraeger, Berlin, StuttgartGoogle Scholar
  8. Clements JF, Schulenberg TS, Iliff MJ, Sullivan BL, Wood CL, Roberson D (2014) The clements checklist of birds of the world: version 6.9. http://www.birds.cornell.edu/clementschecklist/download/. Accessed 16 Aug 2014
  9. Correia VCS, Garnero AV, dos Santos LP, Silva RR, Barbosa M, Bonifácio HL, Gunski RJ (2009) Alta similaridade cariotípica na família Emberezidae (Aves: Passeriformes). Biosci J 25:99–111Google Scholar
  10. Daniels LM, Delany ME (2003) Molecular and cytogenetic organization of the 5S ribosomal DNA array in chicken (Gallus gallus). Chromosome Res 11:305–317CrossRefPubMedGoogle Scholar
  11. De Lucca EJ (1974) Karyotypes of fourteen species of birds of the orders: Cuculiformes, Galliformes, Passeriformes and Tinamiformes. Rev Bras Pesqui Med Biol 7:253–263Google Scholar
  12. de Oliveira EHC, Tagliarini MM, Nagamachi CY, Pieczarka JC (2006) Comparação genômica em aves através de sondas cromossomo-específicas. Revista Brasileira de Ornitologia 14(1):47–52Google Scholar
  13. de Oliveira EHC, Tagliarini MM, Rissino JD, Pieczarka JC, Nagamachi CY et al (2010) Reciprocal chromosome painting between white hawk (Leucopternis albicollis) and chicken reveals extensive fusions and fissions during karyotype evolution of Accipitridae (Aves, Falconiformes). Chromosome Res 18:349–355CrossRefPubMedGoogle Scholar
  14. Ellegren H (2010) Evolutionary stasis: the stable chromosomes of birds. Trends Ecol Evol 25(5):283–291CrossRefPubMedGoogle Scholar
  15. Ericson PGP, Klopfstein S, Irestedt M, Nguyen JMT, Nylander JAA (2014) Dating the diversification of the major lineages of Passeriformes (Aves). BMC Evol Biol 14:8PubMedCentralCrossRefPubMedGoogle Scholar
  16. Ferguson-Smith MA (2006) The economies of evolution. Heredity 96:109CrossRefPubMedGoogle Scholar
  17. Fernández R, Barragán MJL, Bullejos M, Marchal MJA, Díaz De La Guardia R, Sánchez A (2002) New C-band protocol by heat denaturation in the presence of formamide. Hereditas 137:145–148CrossRefPubMedGoogle Scholar
  18. Garnero AV, Gunski RJ (2000) Comparative analysis of the karyotypes of Nothura maculosa and Rynchotus rufescens (Aves: Tinamidae): a case of chromosomal polymorphism. Nucleus 43:64–70Google Scholar
  19. Guerra MS (1986) Reviewing the chromosome nomenclature of Levan et al. Revista Brasileira de Genética 9:741–743Google Scholar
  20. Gunski RJ, Cabanne GS, Ledesma MA, Garnero AV (2000) Análisis cariotípico de siete especies de Tiránidos (Tyrannidae). Hornero 15:103–109Google Scholar
  21. Gunski RJ, Cunha IS, Degrandi TM, Ledesma M, Garnero ADV (2013) Cytogenetic comparison of Podocnemis expansa and Podocnemis unifilis: a case of inversion and duplication involving constitutive heterochromatin. Genet Mol Biol 36(3):353–356PubMedCentralCrossRefPubMedGoogle Scholar
  22. 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 103:173–184CrossRefPubMedGoogle Scholar
  23. Itoh Y, Arnold AP (2005) Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosome Res 13:47–56CrossRefPubMedGoogle Scholar
  24. Itoh Y, Kampf K, Balakrishnan CN, Arnold AP (2011) Karyotypic polymorphism of the zebra finch Z chromosome. Chromosoma 120(3):255–264PubMedCentralCrossRefPubMedGoogle Scholar
  25. Kretschmer R, Gunski RJ, Garnero ADV, Furo IdO, O’Brien PCM, Ferguson-Smith MA, de Oliveira EHC (2014) Molecular cytogenetic characterization of multiple intrachromosomal rearrangements in two representatives of the genus Turdus (Turdidae, Passeriformes). PLoS One 9(7):e103338PubMedCentralCrossRefPubMedGoogle Scholar
  26. Kretschmer R, de Oliveira EHC, Santos MS, Furo IdO, O’Brien P, Ferguson-Smith M, Garnero A, Gunski R (2015) Chromosome mapping of the large Elaenia (Elaenia spectabilis): evidence for a cytogenetic signature for passeriform birds? Biol J Linn Soc 115:391–398CrossRefGoogle Scholar
  27. McPherson MC, Robinson CM, Gehlen LP, Delany ME (2014) Comparative cytogenomics of poultry: mapping of single gene and repeat loci in the Japanese quail (Coturnix japonica). Chromosome Res 22(1):71–83CrossRefPubMedGoogle Scholar
  28. Nanda I, Schlegelmilch K, Haaf T, Schartl M, Schmid M (2008) 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 122:150–156CrossRefPubMedGoogle Scholar
  29. Ohno S, Stenius C, Christian LC, Becak W, Becak ML (1964) Chromosomal uniformity in the avian subclass Carinatae. Chromosoma 15:280–288CrossRefPubMedGoogle Scholar
  30. Ridley M (2006) Evolução. 3a. ed. Porto Alegre, ArtMed Editora, 752 pGoogle Scholar
  31. Rocha GT, De Lucca EJ, De Souza EB (1990) Chromosome polymorphism due to pericentric inversion in Zonotrichia capensis (Emberizidae, Passeriformes, Aves). Genetica 80:201–207CrossRefGoogle Scholar
  32. Rutkowska J, Lagisz M, Nakagawa S (2012) The long and the short of avian W chromosomes: no evidence for gradual W shortening. Biol Lett 8:636–638PubMedCentralCrossRefPubMedGoogle Scholar
  33. Sasaki M, Ikeuchi T, Maino S (1968) A feather pulp culture for avian chromosomes with notes on the chromosomes of the peafowl and the ostrich. Experientia 24:1923–1929Google Scholar
  34. Shetty S, Griffin DK, Graves JAM (1999) Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosome Res 7:289–295CrossRefPubMedGoogle Scholar
  35. Skinner BM, Griffin DK (2012) Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints. Heredity 108:37–41PubMedCentralCrossRefPubMedGoogle Scholar
  36. Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 83:438–442CrossRefGoogle Scholar
  37. Tagliarini MM, O’Brien PCM, Ferguson-Smith MA, de Oliveira EHC (2011) Maintenance of syntenic groups between Cathartidae and Gallus gallus indicates symplesiomorphic karyotypes in new world vultures. Genet Mol Biol 34(1):80–83PubMedCentralCrossRefPubMedGoogle Scholar
  38. Takagi N, Sasaki M (1974) A phylogenetic study of bird karyotypes. Chromosoma 46:91–120CrossRefPubMedGoogle Scholar
  39. 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(3):1455–1468PubMedCentralCrossRefPubMedGoogle Scholar
  40. 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 20:503–511PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Michelly da Silva dos Santos
    • 1
  • Rafael Kretschmer
    • 2
  • Fabio Augusto Oliveira Silva
    • 3
  • Mario Angel Ledesma
    • 4
  • Patricia C. M. O’Brien
    • 5
  • Malcolm A. Ferguson-Smith
    • 5
  • Analía Del Valle Garnero
    • 2
  • Edivaldo Herculano Corrêa de Oliveira
    • 3
    • 6
  • Ricardo José Gunski
    • 2
  1. 1.Programa de Pós-graduação em Genética e Biologia Molecular, PPGBMUniversidade Federal do ParáBelémBrazil
  2. 2.Programa de Pós-graduação em Ciências Biológicas, PPGCBUniversidade Federal do PampaSão GabrielBrazil
  3. 3.Faculdade de Ciências Naturais, Instituto de Ciências Exatas e NaturaisUniversidade Federal do ParáBelémBrazil
  4. 4.Parque Ecologico El PumaCandelariaArgentina
  5. 5.Department of Veterinary Medicine, Cambridge Resource Centre for Comparative GenomicsUniversity of CambridgeCambridgeUK
  6. 6.Laboratório de Cultura de Tecidos e Citogenética, SAMAMInstituto Evandro ChagasAnanindeuaBrazil

Personalised recommendations