Detailed cytogenetic analysis of three duck species (the northern pintail, mallard, and common goldeneye) and karyotype evolution in the family Anatidae (Anseriformes, Aves)
https://doi.org/10.18699/vjgb-24-84
Abstract
Galliformes and Anseriformes are two branches of the Galloanserae group, basal to other Neognathae. In contrast to Galliformes, Anseriformes have not been thoroughly researched by cytogenetic methods. This report is focused on representatives of Anseriformes and the evolution of their chromosome sets. Detailed cytogenetic analysis (G-banding, C-banding, and fluorescence in situ hybridization) was performed on three duck species: the northern pintail (Anas acuta, 2n = 80), the mallard (A. platyrhynchos, 2n = 80), and the common goldeneye (Bucephala clangula, 2n = 80). Using stone curlew (Burhinus oedicnemus, 2n = 42, Charadriiformes) chromosome painting probes, we created homology maps covering macrochromosomes and some microchromosomes. The results indicated a high level of syntenic group conservation among the duck genomes. The two Anas species share their macrochromosome number, whereas in B. clangula, this number is increased due to fissions of two ancestral elements. Additionally, in this species, the presence of massive heterochromatic blocks in most macroautosomes and sex chromosomes was discovered. Localization of clusters of ribosomal DNA and telomere repeats revealed that the duck karyotypes contain some microchromosomes that bear ribosomal RNA genes and/or are enriched for telomere repeats and constitutive heterochromatin. Dot plot (D-GENIES) analysis confirmed the established view about the high level of syntenic group conservation among Anatidae genomes. The new data about the three Anatidae species add knowledge about the transformation of macro- and sex chromosomes of Anseriformes during evolution.
Keywords
About the Authors
V. R. BeklemishevaRussian Federation
Novosibirsk
K. V. Tishakova
Russian Federation
Novosibirsk
S. A. Romanenko
Russian Federation
Novosibirsk
D. A. Andreushkova
Russian Federation
Novosibirsk
V. A. Yudkin
Russian Federation
Novosibirsk
E. А. Interesova
Russian Federation
Novosibirsk
Tomsk
F. Yang
China
Zibo
M. A. Ferguson-Smith
United Kingdom
Cambridge
A. S. Graphodatsky
Russian Federation
Novosibirsk
A. A. Proskuryakova
Russian Federation
Novosibirsk
References
1. Abu-Almaaty A.H., Hassan M.K., El Bakary N.E.R., Ahmed S.H. Chromosomal evolution and molecular genetic analysis of four species of genus Anas (Aves: Anatidae). Genetika. 2019;51(1):104-119. DOI 10.2298/GENSR1901103A
2. Beçak M.L., Beçak W., Roberts F.L., Shoffner R.N., Volp E.P. Aves. In: Chromosome Atlas: Fish, Amphibians, Reptiles, and Birds. Berlin: Springer, 1973;129-207
3. Bulatova N.S., Panov E.N., Radzhabli S.I. Description of the karyotypes of several bird species of the USSR fauna. Dokl. Akad. Nauk SSSR. 1971;199(6):1420-1423
4. Burt D.W. Origin and evolution of avian microchromosomes. Cytogenet. Genome Res. 2002;96(1-4):97-112
5. Cabanettes F., Klopp C. D-GENIES: Dot plot large genomes in an interactive, efficient and simple way. PeerJ. 2018;6:e4958. DOI 10.7717/PEERJ.4958/TABLE-2
6. Campagna L., Toews D.P.L. The genomics of adaptation in birds. Curr. Biol. 2022;32(20):R1173-R1186. DOI 10.1016/j.cub.2022.07.076
7. Chowdhary B., Raudsepp T. Cytogenetics and physical gene maps. In: Bowling A.T., Ruvinsky A. (Eds.). The Genetics of the Horse. Oxon, UK: CABI Publishing, CAB International, 2000;171-241
8. Christidis L. Chordata 3: Aves. In: John B., Kayano H., Levan A. (Eds.). Animal Cytogenetics. Vol. 4. Berlin: Gebrueder Borntraeger, 1990
9. Coullin P., Bed’Hom B., Candelier J.J., Vettese D., Maucolin S., Moulin S., Galkina S.A., Bernheim A., Volobouev V. Cytogenetic repartition of chicken CR1 sequences evidenced by PRINS in Galliformes and some other birds. Chromosom. Res. 2005;13(7):665-673. DOI 10.1007/s10577-005-1004-7
10. Damas J., O’Connor R., Farré M., Lenis V.P.E., Martell H.J., Mandawala A., Fowler K., Joseph S., Swain M.T., Griffin D.K., Larkin D.M. Upgrading short-read animal genome assemblies to chromosome level using comparative genomics and a universal probe set. Genome Res. 2017;27(5):875-884. DOI 10.1101/gr.213660.116
11. Damas J., Kim J., Farré M., Griffin D.K., Larkin D.M. Reconstruction of avian ancestral karyotypes reveals differences in the evolutionary history of macro- and microchromosomes. Genome Biol. 2018; 19(1):155. DOI 10.1186/s13059-018-1544-8
12. Damas J., O’Connor R.E., Griffin D.K., Larkin D.M. Avian chromosomal evolution. In: Kraus R.H.S. (Ed.). Avian Genomics in Ecology and Evolution: From the Lab into the Wild. Springer, 2019;69-92
13. de Oliveira A.M., Souza G.M., Toma G.A., Dos Santos N., Dos Santos R.Z., Goes C.A.G., Deon G.A., Setti P.G., Porto-Foresti F., Utsunomia R., Gunski R.J., Del Valle Garnero A., Herculano Correa de Oliveira E., Kretschmer R., Cioffi M.B. Satellite DNAs, heterochromatin, and sex chromosomes of the wattled jacana (Charadriiformes; Jacanidae): a species with highly rearranged karyotype. Genome. 2024;67(4):109-118. DOI 10.1139/gen-2023-0082
14. De Oliveira T.D., Kretschmer R., Bertocchi N.A., Degrandi T.M., De Oliveira E.H.C., De Cioffi M.B., Garnero A.D.V., Gunski R.J. Genomic organization of repetitive DNA in woodpeckers (aves, piciformes): Implications for karyotype and ZW sex chromosome differentiation. PLoS One. 2017;12(1):e0169987. DOI 10.1371/journal.pone.0169987
15. Degrandi T.M., Barcellos S.A., Costa A.L., Garnero A.D.V., Hass I., Gunski R.J. Introducing the bird chromosome database: An overview of cytogenetic studies in birds. Cytogenet. Genome Res. 2020; 160(4):199-205. DOI 10.1159/000507768
16. Delany M.E., Krupkin A.B., Miller M.M. Organization of telomere sequences in birds: evidence for arrays of extreme length and for in vivo shortening. Cytogenet. Cell Genet. 2000;90(1-2):139-145. DOI 10.1159/000015649
17. Delany M.E., Gessaro T.M., Rodrigue K.L., Daniels L.M. Chromosomal mapping of chicken mega-telomere arrays to GGA9, 16, 28 and W using a cytogenomic approach. Cytogenet. Genome Res. 2007;117(1-4):54-63. DOI 10.1159/000103165
18. Delany M.E., Robinson C.M., Goto R.M., Miller M.M. Architecture and organization of chicken microchromosome 16: Order of the NOR, MHC-Y, and MHC-B subregions. J. Hered. 2009;100(5): 507-514. DOI 10.1093/jhered/esp044
19. Derjusheva S., Kurganova A., Habermann F., Gaginskaya E. High chromosome conservation detected by comparative chromosome painting in chicken, pigeon and passerine birds. Chromosom. Res. 2004; 12(7):715-723. DOI 10.1023/B:CHRO.0000045779.50641.00
20. Dos Santos M.S., Kretschmer R., Silva F.A.O., Ledesma M.A., O’Brien P.C.M., Ferguson-Smith M.A., Del Valle Garnero A., de Oliveira E.H.C., Gunski R.J. Intrachromosomal rearrangements in two representatives of the genus Saltator (Thraupidae, Passeriformes) and the occurrence of heteromorphic Z chromosomes. Genetica. 2015;143(5):535-543. DOI 10.1007/s10709-015-9851-4
21. Dos Santos M. da S., Kretschmer R., Frankl-Vilches C., Bakker A., Gahr M., O’Brien P.C.M., Ferguson-Smith M.A., De Oliveira E.H.C. Comparative cytogenetics between two important songbird, models: The zebra finch and the canary. PLoS One. 2017;12(1):e0170997. DOI 10.1371/journal.pone.0170997
22. Ebied A.M., Hassan H.A., Abu Almaaty A.H., Yaseen A.E. Karyotypic characterization of ten species of birds. Cytologia (Tokyo). 2005; 70(2):181-194. DOI 10.1508/cytologia.70.181
23. Ellegren H. The evolutionary genomics of birds. Annu. Rev. Ecol. Evol. Syst. 2013;44:239-259. DOI 10.1146/annurev-ecolsys-110411-160327
24. Fillon V., Vignoles M., Crooijmans R.P.M.A., Groenen M.A.M., Zoorob R., Vignal A. FISH mapping of 57 BAC clones reveals strong conservation of synteny between Galliformes and Anseriformes. Anim. Genet. 2007;38(3):303-307. DOI 10.1111/j.1365-2052.2007. 01578.x
25. Gill F., Donsker D., Rasmussen P. (Eds.). IOC World Bird List (v13.2). 2023. DOI 10.14344/IOC.ML.13.2
26. raphodatsky A.S., Yang F., O’Brien P.C.M., Serdukova N., Milne B.S., Trifonov V., Ferguson-Smith M.A. A comparative chromosome map of the Arctic fox, red fox and dog defined by chromosome painting and high resolution G-banding. Chromosomе Res. 2000;8(3):253- 263. DOI 10.1023/A:1009217400140
27. Graphodatsky A.S., Yang F., O’Brien P.C.M., Perelman P., Milne B.S., Serdukova N., Kawada S.I., Ferguson-Smith M.A. Phylogenetic implications of the 38 putative ancestral chromosome segments for four canid species. Cytogenet. Cell Genet. 2001;92(3-4):243-247. DOI 10.1159/000056911
28. Gregory T.R. The Animal Genome Size Database, 2023
29. Griffin D.K., Haberman F., Masabanda J., O’Brien P., Bagga M., Sazanov A., Smith J., Burt D.W., Ferguson-Smith M., Wienberg J. Micro- and macrochromosome paints generated by flow cytometry and microdissection: Tools for mapping the chicken genome. Cytogenet. Cell Genet. 1999;87(3-4):278-281. DOI 10.1159/000015449
30. Griffin D.K., Robertson L.B.W., Tempest H.G., Skinner B.M. The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet. Genome Res. 2007;117(1-4):64-77. DOI 10.1159/000103166
31. Griffin D.K., Robertson L.B., Tempest H.G., Vignal A., Fillon V., Crooijmans R.P.M.A., Groenen M.A.M., Deryusheva S., Gaginskaya E., Carré W., Waddington D., Talbot R., Völker M., Masabanda J.S., Burt D.W. Whole genome comparative studies between chicken and turkey and their implications for avian genome evolution. BMC Genomics. 2008;9:168. DOI 10.1186/1471-2164-9-168
32. Grützner F., Zend-Ajusch E., Stout K., Munsche S., Niveleau A., Nanda I., Schmid M., Haaf T. Chicken microchromosomes are hypermethylated and can be identified by specific painting probes. Cytogenet. Cell Genet. 2001;93(3-4):265-269. DOI 10.1159/000056996
33. Guillier-Gencik Z., Bernheim A., Coullin P. Generation of whole-chromosome painting probes specific to each chicken macrochromosome. Cytogenet. Cell Genet. 1999;87(3-4):282-285. DOI 10.1159/000015450
34. Guttenbach M., Nanda I., Feichtinger W., Masabanda J.S., Griffin D.K., Schmid M. Comparative chromosome painting of chicken autosomal paints 1-9 in nine different bird species. Cytogenet. Genome Res. 2003;103(1-2):173-184. DOI 10.1159/000076309
35. Habermann F.A., Cremer M., Walter J., Kreth G., Von Hase J., Bauer K., Wienberg J., Cremer C., Cremer T., Solovei I. Arrangements of macro- and microchromosomes in chicken cells. Chromosom. Res. 2001;9(7):569-584. DOI 10.1023/A:1012447318535
36. Hammar B.O. The karyotypes of thirty‐one birds. Hereditas. 1970; 65(1):29-58
37. Hansmann T., Nanda I., Volobouev V., Yang F., Schartl M., Haaf T., Schmid M. Cross-species chromosome painting corroborates microchromosome fusion during karyotype evolution of birds. Cytogenet. Genome Res. 2009;126(3):281-304. DOI 10.1159/000251965
38. Ijdo J.W., Wells R.A., Baldini A., Reeders S.T. Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res. 1991;19(17):4780. DOI 10.1093/nar/19.17.4780
39. Islam F.B., Uno Y., Nunome M., Nishimura O., Tarui H., Agata K., Matsuda Y. Comparison of the chromosome structures between the chickn and three anserid species, the domestic duck (Anas platyrhynchos), muscovy duck (Cairina moschata), and chinese goose (Anser cygnoides), and the delineation of their karyotype evolution by compara. J. Poult. Sci. 2014;51(1):1-13. DOI 10.2141/jpsa.0130090
40. Itoh Y., Arnold A.P. Chromosomal polymorphism and comparative painting analysis in the zebra finch. Chromosom. Res. 2005;13(1): 47-56. DOI 10.1007/s10577-005-6602-x
41. Kiazim L.G., O’Connor R.E., Larkin D.M., Romanov M.N., Narushin V.G., Brazhnik E.A., Griffin D.K. Comparative mapping of the macrochromosomes of eight avian species provides further insight into their phylogenetic relationships and avian karyotype evolution. Cells. 2021;10(2):362. DOI 10.3390/cells10020362
42. Kretschmer R., de Souza M.S., Furo I.O., Romanov M.N., Gunski R.J., Garnero A.D.V., de Freitas T.R.O., de Oliveira E.H.C., O’Connor R.E., Griffin D.K. Interspecies chromosome mapping in caprimulgiformes, piciformes, suliformes, and trogoniformes (Aves): Cytogenomic insight into microchromosome organization and karyotype evolution in birds. Cells. 2021;10(4):826. DOI 10.3390/cells10040826
43. Liehr T., Kreskowski K., Ziegler M., Piaszinski K., Rittscher K. The Standard FISH Procedure. In: Fluorescence In Situ Hybridisation (FISH). Springer Protocols Handbooks. Berlin: Springer, 2017;109- 118. DOI 10.1007/978-3-662-52959-1_9
44. Maden B.E.H., Dent C.L., Farrell T.E., Garde J., McCallum F.S., Wakeman J.A. Clones of human ribosomal DNA containing the complete 18 S-rRNA and 28 S-rRNA genes. Characterization, a detailed map of the human ribosomal transcription unit and diversity among clones. Biochem. J. 1987;246(2):519-527. DOI 10.1042/bj2460519
45. Masabanda J.S., Burt D.W., O’Brien P.C.M., Vignal A., Fillon V., Walsh P.S., Cox H., Tempest H.G., Smith J., Habermann F., Schmid M., Matsuda Y., Ferguson-Smith M.A., Crooijmans R.P.M.A., Groenen M.A.M., Griffin D.K. Molecular cytogenetic definition of the chicken genome: The first complete avian karyotype. Genetics. 2004;166(3):1367-1373. DOI 10.1534/genetics.166.3.1367
46. Nakatani Y., Takeda H., Kohara Y., Morishita S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res. 2007;17(9):1254-1265. DOI 10.1101/gr.6316407
47. Nanda I., Schrama D., Feichtinger W., Haaf T., Schartl M., Schmid M. Distribution of telomeric (TTAGGG)n sequences in avian chromosomes. Chromosoma. 2002;111(4):215-227. DOI 10.1007/s00412-002-0206-4
48. Nanda I., Benisch P., Fetting D., Haaf T., Schmid M. Synteny conservation of chicken macrochromosomes 1–10 in different avian lineages revealed by cross-species chromosome painting. Cytogenet. Genome Res. 2011;132(3):165-181. DOI 10.1159/000322358
49. Nie W., O’Brien P.C.M., Ng B.L., Fu B., Volobouev V., Carter N.P., Ferguson-Smith M.A., Yang F. 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. 2009;17(1):99-113. DOI 10.1007/s10577-009-9021-6
50. Nie W., O’Brien P.C.M., Fu B., Wang J., Su W., He K., Bed’Hom B., Volobouev V., Ferguson-Smith M.A., Dobigny G., Yang F. Multidi- rectional chromosome painting substantiates the occurrence of extensive genomic reshuffling within Accipitriformes. BMC Evol. Biol. 2015;15(1):205. DOI 10.1186/s12862-015-0484-0
51. Nishida-Umehara C., Tsuda Y., Ishijima J., Ando J., Fujiwara A., Matsuda Y., Griffin D.K. The molecular basis of chromosome orthologies and sex chromosomal differentiation in palaeognathous birds. Chromosom. Res. 2007;15(6):721-734. DOI 10.1007/s10577-007-1157-7
52. O’Connor R.E., Kretschmer R., Romanov M.N., Griffin D.K. A bird’seye view of chromosomic evolution in the class aves. Cells. 2024; 13(4):310. DOI 10.3390/cells13040310
53. Pala I., Naurin S., Stervander M., Hasselquist D., Bensch S., Hansson B. Evidence of a neo-sex chromosome in birds. Heredity (Edinb.). 2012;108(3):264-272. DOI 10.1038/hdy.2011.70
54. Prum R.O., Berv J.S., Dornburg A., Field D.J., Townsend J.P., Lemmon E.M., Lemmon A.R. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature. 2015;526(7574):569-573. DOI 10.1038/nature15697
55. Rodrigue K.L., May B.P., Famula T.R., Delany M.E. Meiotic instability of chicken ultra-long telomeres and mapping of a 2.8 megabase array to the W-sex chromosome. Chromosom. Res. 2005;13(6):581- 591. DOI 10.1007/s10577-005-0984-7
56. Rodrigues B.S., de Assis M.D.F.L., O’Brien P.C.M., FergusonSmith M.A., De Oliveira E.H.C. Chromosomal studies on Coscoroba coscoroba (Aves: Anseriformes) reinforce the Coscoroba-Cereopsis clade. Biol. J. Linn. Soc. 2014;111(2):274-279. DOI 10.1111/bij.12202
57. Romanenko S.A., Biltueva L.S., Serdyukova N.A., Kulemzina A.I., Beklemisheva V.R., Gladkikh O.L., Lemskaya N.A., Interesova E.A., Korentovich M.A., Vorobieva N.V., Graphodatsky A.S., Trifonov V.A. Segmental paleotetraploidy revealed in sterlet (Acipenser ruthenus) genome by chromosome painting. Mol. Cytogenet. 2015;8(1):90. DOI 10.1186/s13039-015-0194-8
58. Rutkowska J., Lagisz M., Nakagawa S. The long and the short of avian W chromosomes: No evidence for gradual W shortening. Biol. Lett. 2012;8(4):636-638. DOI 10.1098/rsbl.2012.0083
59. Schartl M., Schmid M., Nanda I. Dynamics of vertebrate sex chromosome evolution: from equal size to giants and dwarfs. Chromosoma. 2016;125(3):553-571. DOI 10.1007/s00412-015-0569-y
60. Schmid M., Nanda I., Hoehn H., Schartl M., Haaf T., Buerstedde J.M., Arakawa H., Caldwell R.B., Weigend S., Burt D.W., Smith J., Griffin D.K., Masabanda J.S., Groenen M.A.M., Crooijmans R.P.M.A., Vignal A., Fillon V., Morisson M., Pitel F., Vignoles M., Garrigues A., Gellin J., Rodionov A.V., Galkina S.A., Lukina N.A., Ben-Ari G., Blum S., Hillel J., Twito T., Lavi U., David L., Feldman M.W., Delany M.E., Conley C.A., Fowler V.M., Hedges S.B., Godbout R., Katyal S., Smith C., Hudson Q., Sinclair A., Mizuno S. Second report on chicken genes and chromosomes 2005. Cytogenet. Genome Res. 2005;109(4):415-479. DOI 10.1159/000084205
61. Seabright M. A rapid banding technique for human chromosomes. Lancet. 1971;298(7731):971-972. DOI 10.1016/s0140-6736(71)90287-x
62. Shetty S., Griffin D.K., Graves J.A.M. Comparative painting reveals strong chromosome homology over 80 million years of bird evolution. Chromosom. Res. 1999;7(4):289-295. DOI 10.1023/A:1009278914829
63. Shibusawa M., Minai S., Nishida-Umehara C., Suzuki T., Mano T., Yamada K., Namikawa T., Matsuda Y. A comparative cytogenetic study of chromosome homology between chicken and Japanese quail. Cytogenet. Cell Genet. 2001;95(1-2):103-109. DOI 10.1159/000057026
64. Shibusawa M., Nishida-Umehara C., Masabanda J., Griffin D.K., Isobe T., Matsuda Y. Chromosome rearrangements between chicken and guinea fowl defined by comparative chromosome painting and FISH mapping of DNA clones. Cytogenet. Genome Res. 2002; 98(2-3):225-230. DOI 10.1159/000069813
65. Shibusawa M., Nishibori M., Nishida-Umehara C., Tsudzuki M., Masabanda J., Griffin D.K., Matsuda Y. 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. 2004;106(1):111-119. DOI 10.1159/00007857
66. Smith J., Bruley C.K., Paton I.R., Dunn I., Jones C.T., Windsor D., Morrice D.R., Law A.S., Masabanda J., Sazanov A., Waddington D., Fries R., Burt D.W. Differences in gene density on chicken macrochromosomes and microchromosomes. Anim. Genet. 2000;31(2): 96-103. DOI 10.1046/j.1365-2052.2000.00565.x
67. Srikulnath K., Ahmad S.F., Singchat W., Panthum T. Why do some vertebrates have microchromosomes? Cells. 2021;10(9):2182. DOI 10.3390/cells10092182
68. Stiglec R., Ezaz T., Graves J.A.M. A new look at the evolution of avian sex chromosomes. Cytogenet. Genome Res. 2007;117(1-4):103-109. DOI 10.1159/000103170
69. Sumner A.T. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 1972;75(1):304-306. DOI 10.1016/0014-4827(72)90558-7
70. Sun Z., Pan T., Hu C., Sun L., Ding H., Wang H., Zhang C., Jin H., Chang Q., Kan X., Zhang B. Rapid and recent diversification patterns in Anseriformes birds: Inferred from molecular phylogeny and diversification analyses. PLoS One. 2017;12(9):e0184529. DOI 10.1371/journal.pone.0184529
71. Takagi N., Makino S. A revised study on the chromosomes of three species of birds. Caryologia. 1966;19(4):443-455. DOI 10.1080/ 00087114.1966.10796235
72. Telenius H., Pelmear A.H., Tunnacliffe A., Carter N.P., Behmel A., Ferguson-Smith M.A., Nordenrkjold M., Pfragner R., Ponder B.A.J. Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosom. Cancer. 1992;4(3):251-263. DOI 10.1002/gcc.2870040311
73. Uno Y., Nishida C., Hata A., Ishishita S., Matsuda Y. Molecular cytogenetic characterization of repetitive sequences comprising centromeric heterochromatin in three Anseriformes species. PLoS One. 2019;14(3):e0214028. DOI 10.1371/journal.pone.0214028
74. Van Tuinen M., Hedges S.B. Calibration of avian molecular clocks. Mol. Biol. Evol. 2001;18(2):206-213. DOI 10.1093/oxfordjournals.molbev.a003794
75. Wang J., Su W., Hu Y., Li S., O’Brien P.C.M., Ferguson-Smith M.A., Yang F., Nie W. Comparative chromosome maps between the stone curlew and three ciconiiform species (the grey heron, little egret and crested ibis). BMC Ecol. Evol. 2022;22(1):23. DOI 10.1186/s12862- 022-01979-x
76. Wójcik E., Smalec E. Description of the mallard duck (Anas platyrhynchos) karyotype. Folia Biol. 2007;55(3-4):115-120
77. Zimmer R., King W.A., Verrinder Gibbins A.M. Generation of chicken Z-chromosome painting probes by microdissection for screening large-insert genomic libraries. Cytogenet. Cell Genet. 1997;78(2): 124-130. DOI 10.1159/000134643
78. Zlotina A., Maslova A., Kosyakova N., Al-Rikabi A.B.H., Liehr T., Krasikova A. Heterochromatic regions in Japanese quail chromosomes: comprehensive molecular-cytogenetic characterization and 3D mapping in interphase nucleus. Chromosom. Res. 2019;27(3):253-270. DOI 10.1007/s10577-018-9597-9.