Comparative chromosome painting in Columbidae (Columbiformes) reinforces divergence in Passerea and Columbea

Abstract

Pigeons and doves (Columbiformes) are one of the oldest and most diverse extant lineages of birds. However, the karyotype evolution within Columbiformes remains unclear. To delineate the synteny-conserved segments and karyotypic differences among four Columbidae species, we used chromosome painting from Gallus gallus (GGA, 2n = 78) and Leucopternis albicollis (LAL, 2n = 68). Besides that, a set of painting probes for the eared dove, Zenaida auriculata (ZAU, 2n = 76), was generated from flow-sorted chromosomes. Chromosome painting with GGA and ZAU probes showed conservation of the first ten ancestral pairs in Z. auriculata, Columba livia, and Columbina picui, while in Leptotila verreauxi, fusion of the ancestral chromosomes 6 and 7 was observed. However, LAL probes revealed a complex reorganization of ancestral chromosome 1, involving paracentric and pericentric inversions. Because of the presence of similar intrachromosomal rearrangements in the chromosomes corresponding to GGA1q in the Columbidae and Passeriformes species but without a common origin, these results are consistent with the recent proposal of divergence within Neoaves (Passerea and Columbea). In addition, inversions in chromosome 2 were identified in C. picui and L. verreauxi. Thus, in four species of distinct genera of the Columbidae family, unique chromosomal rearrangements have occurred during karyotype evolution, confirming that despite conservation of the ancestral syntenic groups, these chromosomes have been modified by the occurrence of intrachromosomal rearrangements.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Abbreviations

CAK:

Ancestral karyotype of the Columbiformes

CLI:

Columba livia

CPI:

Columbina picui

FISH:

Fluorescent in situ hybridization

GGA:

Gallus gallus

GFU:

Gyps fulvus

LAL:

Leucopternis albicollis

LVE:

Leptotila verreauxi

PAK:

Putative avian ancestral karyotype

ZAU:

Zenaida auriculata

References

  1. Cracraft J (2001) Avian evolution, Gondwana biogeography and the Cretaceous-Tertiary mass extinction event. Proc R Soc B Biol Sci 268:459–469. https://doi.org/10.1098/rspb.2000.1368

    Article  CAS  Google Scholar 

  2. Damas J, O’Connor R, Farré M, Lenis VPE, Martell HJ, Mandawala A, Fowler KE, Jospeh S, Swain M, Griffin DK, Larkin DM (2017) Upgrading short-read animal genome assemblies to chromosome level using comparative genomics and a universal probe set. Genome Res 27:875–884. https://doi.org/10.1101/gr.213660.116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. de Lucca EJ (1984) Chromosomal evolution of South American Columbiformes (Aves). Genetica 62:177–185

    Article  Google Scholar 

  4. de Lucca EJ, de Aguiar MLR (1976) Chromosomal evolution in Columbiformes (Aves). Caryologia 29:59–68

    Article  Google Scholar 

  5. de Oliveira EHC, Tagliarini MM, Rissino JD, Pieczarka JC, Nagamachi CY, O’Brien PCM, Ferguson-Smith MA (2010) Reciprocal chromosome painting between white hawk (Leucopternis albicollis) and chicken reveals extensive fusions and fissions during karyotype evolution of Accipitridae (Aves, Falconiformes). Chromosom Res 18:349–355. https://doi.org/10.1007/s10577-010-9117-z

    Article  CAS  Google Scholar 

  6. Degrandi TM, Garnero ADV, O’Brien PCM, Ferguson-Smith MA, Kretschmer R, de Oliveira EHC, Gunski RJ (2017) Chromosome painting in Trogon s. surrucura (Aves, Trogoniformes) reveals a karyotype derived by chromosomal fissions, fusions, and inversions. Cytogenet Genome Res 151:208–215. https://doi.org/10.1159/000471782

    Article  PubMed  CAS  Google Scholar 

  7. Derjusheva S, Kurganova A, Haberman F, Gaginskaia E (2004) High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosom Res 12:715–723. https://doi.org/10.1023/B:CHRO.0000045779.50641.00

    Article  CAS  Google Scholar 

  8. dos Santos MS, Kretschmer R, Silva FAO, Ledesma MA, O’Brien PCM et al (2015) Intrachromosomal rearrangements in two representatives of the genus Saltator (Thraupidae, Passeriformes) and a case of polymorphism in Z chromosome. Genetica 143:535–543. https://doi.org/10.1007/s10709-015-9851-4

    Article  Google Scholar 

  9. dos Santos MS, Kretschmer R, Frankl-Vilches C, Bakker A, Gahr M et al (2017) Comparative cytogenetics between two important songbird, models: the Zebra finch and the canary. PLoS One 12(1):e0170997. https://doi.org/10.1371/journal.pone.0170997

    Article  PubMed  PubMed Central  Google Scholar 

  10. Furo IO, Monte AA, dos Santos MS, Tagliarini MM, O’Brien PCM et al (2015a) Cytotaxonomy of Eurypyga helias (Gruiformes, Eurypygidae): first karyotypic description and phylogenetic proximity with Rynochetidae. PLoS ONE 10(12):e0143982. https://doi.org/10.1371/journal.pone.0143982

    Article  PubMed Central  CAS  Google Scholar 

  11. Furo IO, Kretschmer R, O’Brien PCM, Ferguson-Smith MA, de Oliveira EHC (2015b) Chromosomal diversity and karyotype evolution in South American macaws (Psittaciformes, Psittacidae). PLoS One 10(6):e0130157. https://doi.org/10.1371/journal.pone.0130157

    Article  CAS  Google Scholar 

  12. Gibbs D, Barnes E, Cox JD (2001) Pigeons and doves: a guide to the pigeons and doves of the world. Pica Press, Mountfield, UK

    Google Scholar 

  13. Gill F, Donsker D (2017) IOC World Bird List (v7.1). doi:https://doi.org/10.14344/IOC.ML.7.1

  14. Griffin DK, Robertson LBW, Tempest HG, Skinner BM (2007) The evolution of the avian genome as revealed by comparative molecular cytogenetic. Cytogenet Genome Res 117:64–77. https://doi.org/10.1159/000103166

    Article  PubMed  CAS  Google Scholar 

  15. 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 103:173–184. https://doi.org/10.1159/000076309

    Article  PubMed  CAS  Google Scholar 

  16. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768. https://doi.org/10.1126/science.1157704

    Article  PubMed  CAS  Google Scholar 

  17. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, Suh A, Weber CC, da Fonseca RR, Li J, Zhang F, Li H, Zhou L, Narula N, Liu L, Ganapathy G, Boussau B, Bayzid MS, Zavidovych V, Subramanian S, Gabaldon T, Capella-Gutierrez S, Huerta-Cepas J, Rekepalli B, Munch K, Schierup M, Lindow B, Warren WC, Ray D, Green RE, Bruford MW, Zhan X, Dixon A, Li S, Li N, Huang Y, Derryberry EP, Bertelsen MF, Sheldon FH, Brumfield RT, Mello CV, Lovell PV, Wirthlin M, Schneider MPC, Prosdocimi F, Samaniego JA, Velazquez AMV, Alfaro-Nunez A, Campos PF, Petersen B, Sicheritz-Ponten T, Pas A, Bailey T, Scofield P, Bunce M, Lambert DM, Zhou Q, Perelman P, Driskell AC, Shapiro B, Xiong Z, Zeng Y, Liu S, Li Z, Liu B, Wu K, Xiao J, Yinqi X, Zheng Q, Zhang Y, Yang H, Wang J, Smeds L, Rheindt FE, Braun M, Fjeldsa J, Orlando L, Barker FK, Jonsson KA, Johnson W, Koepfli KP, O'Brien S, Haussler D, Ryder OA, Rahbek C, Willerslev E, Graves GR, Glenn TC, McCormack J, Burt D, Ellegren H, Alstrom P, Edwards SV, Stamatakis A, Mindell DP, Cracraft J, Braun EL, Warnow T, Jun W, Gilbert MTP, Zhang G (2014) Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320–1331. https://doi.org/10.1126/science.1253451

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Kasai F, Garcia C, Arruga MV, Ferguson-Smith MA (2003) 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. https://doi.org/10.1159/000075770

    Article  PubMed  CAS  Google Scholar 

  19. Kretschmer R, Gunski RJ, Garnero ADV, Furo IO, O’Brien PCM et al (2014) Molecular cytogenetic characterization of multiple intrachromosomal rearrangements in two representatives of the genus Turdus (Turdidae, Passeriformes). PLoS One 9(7):e103338. https://doi.org/10.1371/journal.pone.0103338

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kretschmer R, de Oliveira EHC, dos Santos MS, Furo IO, O’Brien PCM et al (2015a) Chromosome mapping of the large elaenia (Elaenia spectabilis): evidence for a cytogenetic signature for passeriform birds? Biol J Linn Soc 115:391–398. https://doi.org/10.1111/bij.12504

    Article  Google Scholar 

  21. Kretschmer R, Gunski RJ, Garnero ADV, O’Brien PCM, Ferguson-Smith MA et al (2015b) Chromosome painting in Vanellus chilensis: detection of a fusion common to clade Charadrii (Charadriiformes). Cytogenet Genome Res 146:58–63. https://doi.org/10.1159/000431387

    Article  PubMed  Google Scholar 

  22. Kretschmer R, de Oliveira TD, Furo IO, Silva FAO, Gunski RJ et al (2018) Repetitive DNAs and shrink genomes: a chromosomal analysis in nine Columbidae species (Aves, Columbiformes). Genet Mol Biol. https://doi.org/10.1590/1678-4685-GMB-2017-0048

  23. Lapiedra O, Sol D, Carranza S, Beaulieu JM (2013) Behavioural changes and the adaptive diversification of pigeons and doves. Proc R Soc B 280:20122893. https://doi.org/10.1098/rspb.2012.2893

    Article  PubMed  Google Scholar 

  24. Nie W, O’Brien PCM, 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 17:99–113. https://doi.org/10.1007/s10577-009-9021-6

    Article  CAS  Google Scholar 

  25. Nie W, O’Brien PCM, Fu B, Wang J, Su W, He K, Bed’Hom B, Volobouev V, Ferguson-Smith MA, Dobigny G, Yang F (2015) Multidirectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes. BMC Evol Biol 15:205. https://doi.org/10.1186/s12862-015-0484-0

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Pereira SL, Johnson KP, Clayton DH, Baker AJ (2007) Mitochondrial and nuclear DNA sequences support a cretaceous origin of Columbiformes and a dispersal driven radiation in the paleogene. Syst Biol 56:656–672. https://doi.org/10.1080/10635150701549672

    Article  PubMed  CAS  Google Scholar 

  27. Prum RO, Berv JS, Dornburg A, Field DJ, Townsend JP, Lemmon EM, Lemmon AR (2015) A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526:569–573. https://doi.org/10.1038/nature15697

    Article  PubMed  CAS  Google Scholar 

  28. Rocchi M, Archidiacono N, Schempp W, Capozzi O, Stanyon R (2012) Centromere repositioning in mammals. Heredity 108:59–67. https://doi.org/10.1038/hdy.2011.101

    Article  PubMed  CAS  Google Scholar 

  29. 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 24:1923–1929. https://doi.org/10.1007/BF02146680

    Article  Google Scholar 

  30. Shapiro B, Sibthorpe D, Rambaut A, Austin J, Wragg GM, Bininda-Emonds OR, Lee PL, Cooper A (2002) Flight of the dodo. Science 295:1683. https://doi.org/10.1126/science.295.5560.1683

    Article  PubMed  CAS  Google Scholar 

  31. Shapiro MD, Kronenberg Z, Li C, Domyan ET, Pan H, Campbell M, Tan H, Huff CD, Hu H, Vickrey AI, Nielsen SCA, Stringham SA, Hu H, Willerslev E, Gilbert MTP, Yandell M, Zhang G, Wang J (2013) Genomic diversity and evolution of the head crest in the rock pigeon. Science 339(6123):1063–1067. https://doi.org/10.1126/science.1230422

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Skinner BM, Griffin DK (2012) Intrachromosomal rearrangements in avian genome evolution: evidence for regions prone to breakpoints. Heredity 108:37–41. https://doi.org/10.1038/hdy.2011.99

    Article  PubMed  CAS  Google Scholar 

  33. Soares AER, Novak BJ, Haile J, Heupink TH, Fjeldså J, Gilbert MTP, Poinar H, Church GM, Shapiro B (2016) Complete mitochondrial genomes of living and extinct pigeons revise the timing of the columbiform radiation. BMC Evol Biol 16:230. https://doi.org/10.1186/s12862-016-0800-3

    Article  PubMed  PubMed Central  Google Scholar 

  34. Sol D (2008) Artificial selection, naturalization, and fitness: Darwin’s pigeons revisited. Biol J Linn Soc 93:657–665. https://doi.org/10.1111/j.1095-8312.2008.00957.x

    Article  Google Scholar 

  35. Stock AD, Mengden GA (1975) Chromosome banding pattern conservatism in birds and nonhomology of chromosome banding patterns between birds, turtles, snakes and amphibians. Chromosoma 50:69–77

    Article  PubMed  CAS  Google Scholar 

  36. 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 34:80–83. https://doi.org/10.1590/S1415-47572010005000117

    Article  PubMed  PubMed Central  Google Scholar 

  37. Telenius H, Ponder BAJ, Tunnacliffe A, Pelmear AH, Carter NP, Ferguson-Smith MA, Behmel A, Nordenskjöld M, Pfragner R (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4:257–263. https://doi.org/10.1002/gcc.2870040311

    Article  PubMed  CAS  Google Scholar 

  38. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW et al (2010) The genome of a songbird. Nature 464:757–762. https://doi.org/10.1038/nature08819

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to CAPES for the scholarships to R. Kretschmer (PhD scholarship and a scholarship of Programa de Doutorado-sanduíche no Exterior), SISBIO for authorization for the sampling of the specimens examined in the present study, and the Instituto Evandro Chagas for logistical support.

Funding

This study received financial support from Instituto Evandro Chagas. This study was also supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Fundação de Amparo a Pesquisa do Rio Grande do Sul (FAPERGS).

Author information

Affiliations

Authors

Contributions

T.R.O.F., M.A.F.S., and E.H.C.O. conceived, designed, and supervised the project. R.K., I.O.F., and J.C.P. designed and performed most of the experiments and contributed to the interpretation of results. R.K. and I.O.F. analyzed the data and wrote the paper. M.A.F.S., P.C.M.O., R.J.G., A.V.G., E.H.C.O., and T.R.O.F. reviewed the manuscript.

Corresponding author

Correspondence to Rafael Kretschmer.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible Editor: Fengtang Yang

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kretschmer, R., de Oliveira Furo, I., Gunski, R.J. et al. Comparative chromosome painting in Columbidae (Columbiformes) reinforces divergence in Passerea and Columbea. Chromosome Res 26, 211–223 (2018). https://doi.org/10.1007/s10577-018-9580-5

Download citation

Keywords

  • Birds cytogenetics
  • Ancestral karyotype of Columbiformes
  • Chromosome evolution
  • FISH