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Comparison of Karyotypes in Two Hybridizing Passerine Species: Conserved Chromosomal Structure but Divergence in Centromeric Repeats

. 2021 ; 12 () : 768987. [epub] 20211206

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection

Document type Journal Article

Persistent link   https://www.medvik.cz/link/pmid34938317

Changes in chromosomal structure involving chromosomal rearrangements or copy number variation of specific sequences can play an important role in speciation. Here, we explored the chromosomal structure of two hybridizing passerine species; the common nightingale (Luscinia megarhynchos) and the thrush nightingale (Luscinia luscinia), using conventional cytogenetic approaches, immunostaining of meiotic chromosomes, fluorescence in situ hybridization as well as comparative genomic hybridization (CGH). We found that the two nightingale species show conserved karyotypes with the same diploid chromosome number of 2n = 84. In addition to standard chromosomes, both species possessed a small germline restricted chromosome of similar size as a microchromosome. Just a few subtle changes in chromosome morphology were observed between the species, suggesting that only a limited number of chromosomal rearrangements occurred after the species divergence. The interspecific CGH experiment suggested that the two nightingale species might have diverged in centromeric repetitive sequences in most macro- and microchromosomes. In addition, some chromosomes showed changes in copy number of centromeric repeats between the species. The observation of very similar karyotypes in the two nightingale species is consistent with a generally slow rate of karyotype evolution in birds. The divergence of centromeric sequences between the two species could theoretically cause meiotic drive or reduced fertility in interspecific hybrids. Nevertheless, further studies are needed to evaluate the potential role of chromosomal structural variations in nightingale speciation.

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Akera T., Trimm E., Lampson M. A. (2019). Molecular Strategies of Meiotic Cheating by Selfish Centromeres. Cell 178, 1132–1144. 10.1016/j.cell.2019.07.001 PubMed DOI PMC

Albrecht T., Opletalová K., Reif J., Janoušek V., Janoušek L., Cramer E. R. A., et al. (2019). Sperm Divergence in a Passerine Contact Zone: Indication of Reinforcement at the Gametic Level. Evolution 73, 202–213. 10.1111/evo.13677 PubMed DOI

Aslam M. L., Bastiaansen J. W., Crooijmans R. P., Vereijken A., Megens H.-J., Groenen M. A. (2010). A SNP Based Linkage Map of the turkey Genome Reveals Multiple Intrachromosomal Rearrangements between the Turkey and Chicken Genomes. BMC Genomics 11, 647. 10.1186/1471-2164-11-647 PubMed DOI PMC

Auer H., Mayr B., Lambrou M., Schleger W. (1987). An Extended Chicken Karyotype, Including the NOR Chromosome. Cytogenet. Cel Genet. 45, 218–221. 10.1159/000132457 PubMed DOI

Axelsson E., Webster M. T., Smith N. G. C., Burt D. W., Ellegren H. (2005). Comparison of the Chicken and turkey Genomes Reveals a Higher Rate of Nucleotide Divergence on Microchromosomes Than Macrochromosomes. Genome Res. 15, 120–125. 10.1101/gr.3021305 PubMed DOI PMC

Barcellos S. A., Kretschmer R., de Souza M. S., Costa A. L., Degrandi T. M., dos Santos M. S., et al. (2019). Karyotype Evolution and Distinct Evolutionary History of the W Chromosomes in Swallows (Aves, Passeriformes). Cytogenet. Genome Res. 158, 98–105. 10.1159/000500621 PubMed DOI

Bensasson D., Zarowiecki M., Burt A., Koufopanou V. (2008). Rapid Evolution of Yeast Centromeres in the Absence of Drive. Genetics 178, 2161–2167. 10.1534/genetics.107.083980 PubMed DOI PMC

Bi K., Bogart J. P. (2006). Identification of Intergenomic Recombinations in Unisexual Salamanders of the Genus Ambystoma by Genomic In Situ Hybridization (GISH). Cytogenet. Genome Res. 112, 307–312. 10.1159/000089885 PubMed DOI

Bozhko S. I. (1971). Karyotypes of Two Bird Species, Nightingale (Luscinia megarhynchos Brehm) and Song Trush (Turdus philomelos Brehm). Acta Biologica Debrecina 9, 131–136.

Bruders R., Van Hollebeke H., Osborne E. J., Kronenberg Z., Maclary E., Yandell M., et al. (2020). A Copy Number Variant Is Associated with a Spectrum of Pigmentation Patterns in the Rock Pigeon (Columba livia). Plos Genet. 16, e1008274. 10.1371/journal.pgen.1008274 PubMed DOI PMC

Bulatova N. S. (1981). A Comparative Karyological Study of Passerine Birds, 15. Praha: Academia Nakladatelstvi Československé akademie věd, 1–44.

Bulatova N. S., Panov E. N. (1973). Comparative Analysis of Karyotypes of 18 Species Family Turdidae (Aves). Caryologia 26, 229–244. 10.1080/00087114.1973.10796539 DOI

Burt D. W. (2002). Origin and Evolution of Avian Microchromosomes. Cytogenet. Genome Res. 96, 97–112. 10.1159/000063018 PubMed DOI

Butlin R. K. (2005). Recombination and Speciation. Mol. Ecol. 14, 2621–2635. 10.1111/j.1365-294X.2005.02617.x PubMed DOI

Cazaux B., Catalan J., Veyrunes F., Douzery E. J., Britton-Davidian J. (2011). Are Ribosomal DNA Clusters Rearrangement Hotspots? A Case Study in the Genus Mus (Rodentia, Muridae). BMC Evol. Biol. 11, 124. 10.1186/1471-2148-11-124 PubMed DOI PMC

Chmátal L., Gabriel S. I., Mitsainas G. P., Martínez-Vargas J., Ventura J., Searle J. B., et al. (2014). Centromere Strength Provides the Cell Biological Basis for Meiotic Drive and Karyotype Evolution in Mice. Curr. Biol. 24, 2295–2300. 10.1016/j.cub.2014.08.017 PubMed DOI PMC

Christidis L. (1990). Animal Cytogenetics/Vol. 4, Chordata. 3. B, Aves/by Les Christidis. Editor John B. (Berlin: Gebrüder Bornträger; ).

Cioffi M. B., Martins C., Centofante L., Jacobina U., Bertollo L. a. C. (2009). Chromosomal Variability Among Allopatric Populations of Erythrinidae Fish Hoplias malabaricus: Mapping of Three Classes of Repetitive DNAs. Cytogenet. Genome Res. 125, 132–141. 10.1159/000227838 PubMed DOI

de M. C. Sassi F., Perez M. F., Oliveira V. C. S., Deon G. A., de Souza F. H. S., Ferreira P. H. N., et al. (2021). High Genetic Diversity Despite Conserved Karyotype Organization in the Giant Trahiras from Genus Hoplias (Characiformes, Erythrinidae). Genes 12, 252. 10.3390/genes12020252 PubMed DOI PMC

de Oliveira E. A., Bertollo L. A. C., Rab P., Ezaz T., Yano C. F., Hatanaka T., et al. (2019). Cytogenetics, Genomics and Biodiversity of the South American and African Arapaimidae Fish Family (Teleostei, Osteoglossiformes). PLoS ONE 14, e0214225. 10.1371/journal.pone.0214225 PubMed DOI PMC

de Oliveira E. H. C., Habermann F. A., Lacerda O., Sbalqueiro I. J., Wienberg J., Müller 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, 338–343. 10.1007/s00412-005-0009-5 PubMed DOI

Degrandi T. M., Barcellos S. A., Costa A. L., Garnero A. D. V., Hass I., Gunski R. J. (2020a). Introducing the Bird Chromosome Database: An Overview of Cytogenetic Studies in Birds. Cytogenet. Genome Res. 160, 199–205. 10.1159/000507768 PubMed DOI

Degrandi T. M., Gunski R. J., Garnero A. d. V., Oliveira E. H. C. d., Kretschmer R., Souza M. S. d., et al. (2020b). The Distribution of 45S rDNA Sites in Bird Chromosomes Suggests Multiple Evolutionary Histories. Genet. Mol. Biol. 43, e20180331. 10.1590/1678-4685-GMB-2018-0331 PubMed DOI PMC

del Priore L., Pigozzi M. I. (2020). MLH1 Focus Mapping in the guinea Fowl (Numida meleagris) Give Insights into the Crossover Landscapes in Birds. PLoS ONE 15, e0240245. 10.1371/journal.pone.0240245 PubMed DOI PMC

Derjusheva S., Kurganova A., Habermann F., Gaginskaya E. (2004). High Chromosome Conservation Detected by Comparative Chromosome Painting in Chicken, Pigeon and Passerine Birds. Chromosome Res. 12, 715–723. 10.1023/B:CHRO.0000045779.50641.00 PubMed DOI

dos Santos M. d. S., Kretschmer R., Silva F. A. O., Ledesma M. A., O’Brien P. C. M., Ferguson-Smith M. A., et al. (2015). Intrachromosomal Rearrangements in Two Representatives of the Genus Saltator (Thraupidae, Passeriformes) and the Occurrence of Heteromorphic Z Chromosomes. Genetica 143, 535–543. 10.1007/s10709-015-9851-4 PubMed DOI

Ellegren H. (2010). Evolutionary Stasis: the Stable Chromosomes of Birds. Trends Ecol. Evol. 25, 283–291. 10.1016/j.tree.2009.12.004 PubMed DOI

Ellegren H., Smeds L., Burri R., Olason P. I., Backström N., Kawakami T., et al. (2012). The Genomic Landscape of Species Divergence in Ficedula Flycatchers. Nature 491, 756–760. 10.1038/nature11584 PubMed DOI

Ellegren H. (2013). The Evolutionary Genomics of Birds. Annu. Rev. Ecol. Evol. Syst. 44, 239–259. 10.1146/annurev-ecolsys-110411-160327 DOI

Feng S., Stiller J., Deng Y., Armstrong J., Fang Q., Reeve A. H., et al. (2020). Dense Sampling of Bird Diversity Increases Power of Comparative Genomics. Nature 587, 252–257. 10.1038/s41586-020-2873-9 PubMed DOI PMC

Griffin D. K., Haberman F., Masabanda J., O’Brien P., Bagga M., Sazanov A., et al. (1999). Micro- and Macrochromosome Paints Generated by Flow Cytometry and Microdissection: Tools for Mapping the Chicken Genome. Cytogenet. Genome Res. 87, 278–281. 10.1159/000015449 PubMed DOI

Griffin D. K., Robertson L. B. W., Tempest H. G., Skinner B. M. (2007). The Evolution of the Avian Genome as Revealed by Comparative Molecular Cytogenetics. Cytogenet. Genome Res. 117, 64–77. 10.1159/000103166 PubMed DOI

Haaf T., Willard H. F. (1997). Chromosome-specific α-satellite DNA from the Centromere of Chimpanzee Chromosome 4. Chromosoma 106, 226–232. 10.1007/s004120050243 PubMed DOI

Haldane J. B. S. (1922). Sex Ratio and Unisexual Sterility in Hybrid Animals. Journ. Gen. 12, 101–109. 10.1007/BF02983075 DOI

Hale D. W., Ryder E. J., Sudman P. D., Greenbaum I. F. (1988). Application of Synaptonemal Complex Techniques for Determination of Diploid Number and Chromosomal Morphology in Birds. The Auk 4, 776–779.

Henikoff S., Ahmad K., Malik H. S. (2001). The Centromere Paradox: Stable Inheritance with Rapidly Evolving DNA. Science 293, 1098–1102. 10.1126/science.1062939 PubMed DOI

Hoffmann A. A., Rieseberg L. H. (2008). Revisiting the Impact of Inversions in Evolution: From Population Genetic Markers to Drivers of Adaptive Shifts and Speciation? Annu. Rev. Ecol. Evol. Syst. 39, 21–42. 10.1146/annurev.ecolsys.39.110707.173532 PubMed DOI PMC

Homolka D., Ivanek R., Capkova J., Jansa P., Forejt J. (2007). Chromosomal Rearrangement Interferes with Meiotic X Chromosome Inactivation. Genome Res. 17, 1431–1437. 10.1101/gr.6520107 PubMed DOI PMC

Hooper D. M., Griffith S. C., Price T. D. (2019). Sex Chromosome Inversions Enforce Reproductive Isolation across an Avian Hybrid Zone. Mol. Ecol. 28, 1246–1262. 10.1111/mec.14874 PubMed DOI

Hooper D. M., Price T. D. (2017). Chromosomal Inversion Differences Correlate with Range Overlap in Passerine Birds. Nat. Ecol. Evol. 1, 1526–1534. 10.1038/s41559-017-0284-6 PubMed DOI

Hooper D. M., Price T. D. (2015). Rates of Karyotypic Evolution in Estrildid Finches Differ between Island and Continental Clades. Evolution 69, 890–903. 10.1111/evo.12633 PubMed DOI

Huang J., Ma L., Yang F., Fei S.-z., Li L. (2008). 45S rDNA Regions Are Chromosome Fragile Sites Expressed as Gaps In Vitro on Metaphase Chromosomes of Root-Tip Meristematic Cells in Lolium Spp. PLOS ONE 3, e2167. 10.1371/journal.pone.0002167 PubMed DOI PMC

Hurst L. D., Pomiankowski A. (1991). Causes of Sex Ratio Bias May Account for Unisexual Sterility in Hybrids: a New Explanation of Haldane's Rule and Related Phenomena. Genetics 128, 841–858. 10.1093/genetics/128.4.841 PubMed DOI PMC

Iskow R. C., Gokcumen O., Abyzov A., Malukiewicz J., Zhu Q., Sukumar A. T., et al. (2012). Regulatory Element Copy Number Differences Shape Primate Expression Profiles. Proc. Natl. Acad. Sci. 109, 12656–12661. 10.1073/pnas.1205199109 PubMed DOI PMC

Jarvis E. D., Mirarab S., Aberer A. J., Li B., Houde P., Li C., et al. (2014). Whole-genome Analyses Resolve Early Branches in the Tree of Life of Modern Birds. Science 346, 1320–1331. 10.1126/science.1253451 PubMed DOI PMC

Kallioniemi A., Kallioniemi O.-P., Sudar D., Rutovitz D., Gray J. W., Waldman F., et al. (1992). Comparative Genomic Hybridization for Molecular Cytogenetic Analysis of Solid Tumors. Science 258, 818–821. 10.1126/science.1359641 PubMed DOI

King M. (1993). Species Evolution: The Role of Chromosome Change. Cambridge: Cambridge University Press.

Kinsella C. M., Ruiz-Ruano F. J., Dion-Côté A.-M., Charles A. J., Gossmann T. I., Cabrero J., et al. (2019). Programmed DNA Elimination of Germline Development Genes in Songbirds. Nat. Commun. 10, 5468. 10.1038/s41467-019-13427-4 PubMed DOI PMC

Knief U., Forstmeier W., Pei Y., Wolf J., Kempenaers B. (2020). A Test for Meiotic Drive in Hybrids between Australian and Timor Zebra Finches. Ecol. Evol. 10, 13464–13475. 10.1002/ece3.6951 PubMed DOI PMC

Koubová M., Pokorná M. J., Rovatsos M., Farkačová K., Altmanová M., Kratochvíl L. (2014). Sex Determination in Madagascar Geckos of the Genus Paroedura (Squamata: Gekkonidae): Are Differentiated Sex Chromosomes Indeed So Evolutionary Stable? Chromosome Res. 22, 441–452. 10.1007/s10577-014-9430-z PubMed DOI

Kretschmer R., Ferguson-Smith M., De Oliveira E. (2018). Karyotype Evolution in Birds: From Conventional Staining to Chromosome Painting. Genes 9, 181. 10.3390/genes9040181 PubMed DOI PMC

Kretschmer R., Gunski R. J., Garnero A. D. V., Furo I. d. O., O'Brien P. C. M., Ferguson-Smith M. A., et al. (2014). Molecular Cytogenetic Characterization of Multiple Intrachromosomal Rearrangements in Two Representatives of the Genus Turdus (Turdidae, Passeriformes). PLoS ONE 9, e103338. 10.1371/journal.pone.0103338 PubMed DOI PMC

Levan A. (1964). Nomenclature for Centromeric Position on Chromosomes. Hereditas 52, 201–220.

Malinovskaya L. P., Zadesenets K. S., Karamysheva T. V., Akberdina E. A., Kizilova E. A., Romanenko M. V., et al. (2020). Germline-restricted Chromosome (GRC) in the Sand Martin and the Pale Martin (Hirundinidae, Aves): Synapsis, Recombination and Copy Number Variation. Sci. Rep. 10, 1058. 10.1038/s41598-020-58032-4 PubMed DOI PMC

Masabanda J. S., Burt D. W., O'Brien P. C. M., Vignal A., Fillon V., Walsh P. S., et al. (2004). Molecular Cytogenetic Definition of the Chicken Genome: The First Complete Avian Karyotype. Genetics 166, 1367–1373. 10.1534/genetics.166.3.1367 PubMed DOI PMC

McLaughlin R. N., Malik H. S. (2017). Genetic Conflicts: the Usual Suspects and beyond. J. Exp. Biol. 220, 6–17. 10.1242/jeb.148148 PubMed DOI PMC

Minias P., Gutiérrez J. S., Dunn P. O. (2020). Avian Major Histocompatibility Complex Copy Number Variation Is Associated with Helminth Richness. Biol. Lett. 16, 20200194. 10.1098/rsbl.2020.0194 PubMed DOI PMC

Mittal O. P., Satija K. (1978). On the Somatic Chromosomes of Saxicoloides Fulicata Combaiensis (Latham). Proc. 65th Ind. Sci. Cong. Ahmedabad 3, 243.

Moens P. B., Heyting C., Dietrich A. J., van Raamsdonk W., Chen Q. (1987). Synaptonemal Complex Antigen Location and Conservation. J. Cel Biol. 105, 93–103. 10.1083/jcb.105.1.93 PubMed DOI PMC

Mořkovský L., Janoušek V., Reif J., Rídl J., Pačes J., Choleva L., et al. (2018). Genomic Islands of Differentiation in Two Songbird Species Reveal Candidate Genes for Hybrid Female Sterility. Mol. Ecol. 27, 949–958. 10.1111/mec.14479 PubMed DOI PMC

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, 165–181. 10.1159/000322358 PubMed DOI

Nanda I., Schmid M. (1994). Localization of the Telomeric (TTAGGG)n Sequence in Chicken (Gallus domesticus) Chromosomes. Cytogenet. Cel Genet 65, 190–193. 10.1159/000133630 PubMed DOI

Nanda I., Schrama D., Feichtinger W., Haaf T., Schartl M., Schmid M. (2002). Distribution of Telomeric (TTAGGG)n Sequences in Avian Chromosomes. Chromosoma 111, 215–227. 10.1007/s00412-002-0206-4 PubMed DOI

Nguyen P., Sahara K., Yoshido A., Marec F. (2010). Evolutionary Dynamics of rDNA Clusters on Chromosomes of Moths and Butterflies (Lepidoptera). Genetica 138, 343–354. 10.1007/s10709-009-9424-5 PubMed DOI

Nishida C., Ishijima J., Kosaka A., Tanabe H., Habermann F. A., Griffin D. K., et al. (2008). Characterization of Chromosome Structures of Falconinae (Falconidae, Falconiformes, Aves) by Chromosome Painting and Delineation of Chromosome Rearrangements during Their Differentiation. Chromosome Res. 16, 171–181. 10.1007/s10577-007-1210-6 PubMed DOI

Oliveira V. C. S., Altmanová M., Viana P. F., Ezaz T., Bertollo L. A. C., Ráb P., et al. (2021). Revisiting the Karyotypes of Alligators and Caimans (Crocodylia, Alligatoridae) after a Half-century Delay: Bridging the gap in the Chromosomal Evolution of Reptiles. Cells 10, 1397. 10.3390/cells10061397 PubMed DOI PMC

Ortíz-Barrientos D., Reiland J., Hey J., Noor M. A. F. (2002). Recombination and the Divergence of Hybridizing Species. Genet. Mate Choice: Sex. Selection Sex. Isolation 116, 167–178. 10.1007/978-94-010-0265-3_2 PubMed DOI

Pardo-Manuel de Villena F., Sapienza C. (2001). Nonrandom Segregation during Meiosis: the Unfairness of Females. Mamm. Genome 12, 331–339. 10.1007/s003350040003 PubMed DOI

Peona V., Palacios-Gimenez O. M., Blommaert J., Liu J., Haryoko T., Jønsson K. A., et al. (2021). The Avian W Chromosome Is a Refugium for Endogenous Retroviruses with Likely Effects on Female-Biased Mutational Load and Genetic Incompatibilities. Phil. Trans. R. Soc. B. 376, 20200186. 10.1098/rstb.2020.0186 PubMed DOI PMC

Perry G. H., Dominy N. J., Claw K. G., Lee A. S., Fiegler H., Redon R., et al. (2007). Diet and the Evolution of Human Amylase Gene Copy Number Variation. Nat. Genet. 39, 1256–1260. 10.1038/ng2123 PubMed DOI PMC

Pertile M. D., Graham A. N., Choo K. H. A., Kalitsis P. (2009). Rapid Evolution of Mouse Y Centromere Repeat DNA Belies Recent Sequence Stability. Genome Res. 19, 2202–2213. 10.1101/gr.092080.109 PubMed DOI PMC

Peters A. H. F. M., Plug A. W., Van Vugt M. J., Boer P. d. (1997). A Drying-Down Technique for the Spreading of Mammalian Meiocytes from the Male and Female Germline. Chromosome Res. 5 (1), 66–68. 10.1023/a:1018445520117 PubMed DOI

Phadnis N., Orr H. A. (2009). A Single Gene Causes Both Male Sterility and Segregation Distortion in Drosophila Hybrids. Science 323, 376–379. 10.1126/science.1163934 PubMed DOI PMC

Pichugin A. M., Galkina S. A., Potekhin A. A., Punina E. O., Rautian M. S., Rodionov A. V. (2001). Estimation of the Minimal Size of Chicken Gallus gallus domesticus Microchromosomes via Pulsed-Field Electrophoresis. Russ. J. Genet. 37, 535–538. 10.1023/A:1016622816552 PubMed DOI

Pigozzi M. I., Solari A. J. (1998). Germ Cell Restriction and Regular Transmission of an Accessory Chromosome that Mimics a Sex Body in the Zebra Finch, Taeniopygia guttata . Chromosome Res. 6, 105–113. 10.1023/A:1009234912307 PubMed DOI

Pigozzi M. I., Solari A. J. (2005). The Germ-Line-Restricted Chromosome in the Zebra Finch: Recombination in Females and Elimination in Males. Chromosoma 114, 403–409. 10.1007/s00412-005-0025-5 PubMed DOI

Pokorná M., Rens W., Rovatsos M., Kratochvíl L. (2014). A ZZ/ZW Sex Chromosome System in the Thick-Tailed Gecko (Underwoodisaurus milii; Squamata: Gekkota: Carphodactylidae), a Member of the Ancient Gecko Lineage. Cytogenet. Genome Res. 142, 190–196. 10.1159/000358847 PubMed DOI

Reif J., Reifová R., Skoracka A., Kuczyński L. (2018). Competition-driven Niche Segregation on a Landscape Scale: Evidence for Escaping from Syntopy towards Allotopy in Two Coexisting Sibling Passerine Species. J. Anim. Ecol. 87, 774–789. 10.1111/1365-2656.12808 PubMed DOI

Reifová R., Kverek P., Reif J. (2011b). The First Record of a Female Hybrid between the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (Luscinia luscinia) in Nature. J. Ornithol 152, 1063–1068. 10.1007/s10336-011-0700-7 DOI

Reifová R., Reif J., Antczak M., Nachman M. W. (2011a). Ecological Character Displacement in the Face of Gene Flow: Evidence from Two Species of Nightingales. BMC Evol. Biol. 11, 138. 10.1186/1471-2148-11-138 PubMed DOI PMC

Rieseberg L. H. (2001). Chromosomal Rearrangements and Speciation. Trends Ecol. Evol. 16, 351–358. 10.1016/S0169-5347(01)02187-5 PubMed DOI

Rodionov A. V., Myakoshina Y. A., Chelysheva L. A., Solovei I. V., Gaginskaya E. R. (1992). Chiasmata in the Lampbrush Chromosomes of Gallus gallus domesticus: the Cytogenetic Study of Recombination Frequency and Linkage Map Lengths. Genetika 28, 53–63.

Rodrigues B. S., Kretschmer R., Gunski R. J., Garnero A. D. V., O'Brien P. C. M., Ferguson-Smith M., et al. (2017). Chromosome Painting in Tyrant Flycatchers Confirms a Set of Inversions Shared by Oscines and Suboscines (Aves, Passeriformes). Cytogenet. Genome Res. 153, 205–212. 10.1159/000486975 PubMed DOI

Schartl M., Schmid M., Nanda I. (2016). Dynamics of Vertebrate Sex Chromosome Evolution: from Equal Size to Giants and Dwarfs. Chromosoma 125, 553–571. 10.1007/s00412-015-0569-y PubMed DOI

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., et al. (2012). Fiji: an Open-Source Platform for Biological-Image Analysis. Nat. Methods 9, 676–682. 10.1038/nmeth.2019 PubMed DOI PMC

Skinner B. M., Al Mutery A., Smith D., Völker M., Hojjat N., Raja S., et al. (2014). Global Patterns of Apparent Copy Number Variation in Birds Revealed by Cross-Species Comparative Genomic Hybridization. Chromosome Res. 22, 59–70. 10.1007/s10577-014-9405-0 PubMed DOI

Skinner B. M., Robertson L. B., Tempest H. G., Langley E. J., Ioannou D., Fowler K. E., et al. (2009). Comparative Genomics in Chicken and Pekin Duck Using FISH Mapping and Microarray Analysis. BMC Genomics 10, 357. 10.1186/1471-2164-10-357 PubMed DOI PMC

Smith J., Bruley C. K., Paton I. R., Dunn I., Jones C. T., Windsor D., et al. (2000). Differences in Gene Density on Chicken Macrochromosomes and Microchromosomes. Anim. Genet. 31, 96–103. 10.1046/j.1365-2052.2000.00565.x PubMed DOI

Sottas C., Reif J., Kreisinger J., Schmiedová L., Sam K., Osiejuk T. S., et al. (2020). Tracing the Early Steps of Competition-Driven Eco-Morphological Divergence in Two Sister Species of Passerines. Evol. Ecol. 34, 501–524. 10.1007/s10682-020-10050-4 DOI

Sottas C., Reif J., Kuczyński L., Reifová R. (2018). Interspecific Competition Promotes Habitat and Morphological Divergence in a Secondary Contact Zone between Two Hybridizing Songbirds. J. Evol. Biol. 31, 914–923. 10.1111/jeb.13275 PubMed DOI

Storchová R., Reif J., Nachman M. W. (2010). Female Heterogamety and Speciation: Reduced Introgression of the Z Chromosome between Two Species of Nightingales. Evolution 64, 456–471. 10.1111/j.1558-5646.2009.00841.x PubMed DOI PMC

Sumner A. T. (1972). A Simple Technique for Demonstrating Centromeric Heterochromatin. Exp. Cel Res. 75, 304–306. 10.1016/0014-4827(72)90558-7 PubMed DOI

Symonová R., Sember A., Majtánová Z., Ráb P. (2015). “Characterization of Fish Genomes by GISH and CGH,” in Fish Cytogenetic Techniques. Editors Ozouf-Costaz C., Pisano E., Foresti F., de Almeida L. (Boca Paton: CRC Press; ), 118–131. 10.1201/b18534-17 DOI

Teixeira G. A., Aguiar H. J. a. C., Petitclerc F., Orivel J., Lopes D. M., Barros L. a. C. (2021). Evolutionary Insights into the Genomic Organization of Major Ribosomal DNA in Ant Chromosomes. Insect Mol. Biol. 30, 340–354. 10.1111/imb.12699 PubMed DOI

Torgasheva A. A., Malinovskaya L. P., Zadesenets K. S., Karamysheva T. V., Kizilova E. A., Akberdina E. A., et al. (2019). Germline-restricted Chromosome (GRC) Is Widespread Among Songbirds. Proc. Natl. Acad. Sci. USA 116, 201817373. 10.1073/pnas.1817373116 PubMed DOI PMC

Udagawa T. (1955). Karyogram Studies in Birds VI. The Chromosomes of Five Species of the Turdidae. 日本動物学彙報 28 (4), 256–261.

Völker M., Backström N., Skinner B. M., Langley E. J., Bunzey S. K., Ellegren H., et al. (2010). Copy Number Variation, Chromosome Rearrangement, and Their Association with Recombination during Avian Evolution. Genome Res. 20, 503–511. 10.1101/gr.103663.109 PubMed DOI PMC

Weissensteiner M. H., Bunikis I., Catalán A., Francoijs K.-J., Knief U., Heim W., et al. (2020). Discovery and Population Genomics of Structural Variation in a Songbird Genus. Nat. Commun. 11, 3403. 10.1038/s41467-020-17195-4 PubMed DOI PMC

Wellenreuther M., Mérot C., Berdan E., Bernatchez L. (2019). Going beyond SNPs: The Role of Structural Genomic Variants in Adaptive Evolution and Species Diversification. Mol. Ecol. 28, 1203–1209. 10.1111/mec.15066 PubMed DOI

White M. J. D. (1978). Chain Processes in Chromosomal Speciation. Syst. Zoolog. 27, 285. 10.2307/2412880 DOI

Zhang G., Li B., Li B., Li C., Gilbert M. T. P., Jarvis E. D., et al. (2014). Comparative Genomic Data of the Avian Phylogenomics Project. GigaSci 3, 26. 10.1186/2047-217X-3-26 PubMed DOI PMC

Zhang L., Reifová R., Halenková Z., Gompert Z. (2021). How Important Are Structural Variants for Speciation? Genes 12, 1084. 10.3390/genes12071084 PubMed DOI PMC

Zhang L., Sun T., Woldesellassie F., Xiao H., Tao Y. (2015). Sex Ratio Meiotic Drive as a Plausible Evolutionary Mechanism for Hybrid Male Sterility. Plos Genet. 11, e1005073. 10.1371/journal.pgen.1005073 PubMed DOI PMC

Zhou J., Lemos B., Dopman E. B., Hartl D. L. (2011). Copy-Number Variation: The Balance between Gene Dosage and Expression in Drosophila melanogaster . Genome Biol. Evol. 3, 1014–1024. 10.1093/gbe/evr023 PubMed DOI PMC

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