Neo-X-Linked Chromosome Polymorphism: Cytogenetic Insights from Passalites nemorivagus (Mammalia, Cervidae)

. 2025 Aug 30 ; 15 (17) : . [epub] 20250830

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40941352

Grantová podpora
2019/06940-1-GACR Fundação de Amparo à Pesquisa do Estado de São Paulo

Chromosomal instability plays a significant role in karyotype evolution and speciation in mammalian groups with notable intraspecific chromosomal variation. The Cervidae family, known for its rapid karyotypic evolution due to chromosomal fragility, shows substantial chromosomal diversity, making it a focal point for studies on chromosomal evolution, particularly with respect to conservation and taxonomic classification. The Amazon gray brocket deer (Passalites nemorivagus) exhibits pronounced chromosomal polymorphism, including two distinct sex chromosome systems: the ancestral XX/XY system and a new system due to an X-autosome fusion (neo-X), where males present XY1Y2. This variation is intriguing, especially given that the effects on hybrids have not been previously reported. This study uses bovine whole-chromosome painting (WCP) and BAC probes to document karyotypic variation in P. nemorivagus. A male with the XY system and a heterozygous autosomal Robertsonian fusion was paired with a female with neo-X chromosomes, and the resulting female offspring displayed an X-autosome fusion in heterozygosity. The females in this study, hybrids for the sex system, exhibited estrus, copulated, and both gave birth to offspring. This characterization is the first step in investigating the effects of sex chromosome system variation on hybrid viability and fertility, and provides insights into the reproductive biology of Neotropical deer.

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

Faria R., Navarro A. Chromosomal Speciation Revisited: Rearranging Theory with Pieces of Evidence. Trends Ecol. Evol. 2010;25:660–669. doi: 10.1016/j.tree.2010.07.008. PubMed DOI

Graphodatsky A.S., Trifonov V.A., Stanyon R. The Genome Diversity and Karyotype Evolution of Mammals. Mol. Cytogenet. 2011;4:22. doi: 10.1186/1755-8166-4-22. PubMed DOI PMC

Ducos A., Berland H.-M., Bonnet N., Calgaro A., Billoux S., Mary N., Garnier-Bonnet A., Darré R., Pinton A. Chromosomal Control of Pig Populations in France: 2002–2006 Survey. Genet. Sel. Evol. 2007;39:583–597. doi: 10.1186/1297-9686-39-5-583. PubMed DOI PMC

Dobigny G., Britton-Davidian J., Robinson T.J. Chromosomal Polymorphism in Mammals: An Evolutionary Perspective. Biol. Rev. Camb. Philos. Soc. 2017;92:1–21. doi: 10.1111/brv.12213. PubMed DOI

Vargas-Munar D.S.F., Sarria-Perea J.A., Duarte J.M.B. Different Responses to Doxorubicin-Induced Chromosome Aberrations in Brazilian Deer Species. Genet. Mol. Res. 2010;9:1545–1549. doi: 10.4238/vol9-3gmr822. PubMed DOI

Wurster D.H., Benirschke K. Indian Muntjac, Muntiacus muntjak: A Deer with a Low Diploid Chromosome Number. Science. 1970;168:1364–1366. doi: 10.1126/science.168.3937.1364. PubMed DOI

Fontana F., Rubini M. Chromosomal Evolution in Cervidae. Biosystems. 1990;24:157–174. doi: 10.1016/0303-2647(90)90008-O. PubMed DOI

Bernegossi A.M., Vozdova M., Cernohorska H., Kubickova S., Galindo D.J., Kadlcikova D., Rubes J., Duarte J.M.B. Cytogenetic Mapping of Cattle BAC Probes for the Hypothetical Ancestral Karyotype of the Family Cervidae. Cytogenet. Genome Res. 2022;162:140–147. doi: 10.1159/000525592. PubMed DOI

Proskuryakova A.A., Ivanova E.S., Makunin A.I., Larkin D.M., Ferguson-Smith M.A., Yang F., Uphyrkina O.V., Perelman P.L., Graphodatsky A.S. Comparative Studies of X Chromosomes in Cervidae Family. Sci. Rep. 2023;13:11992. doi: 10.1038/s41598-023-39088-4. PubMed DOI PMC

Morales-Donoso J.A., Vacari G.Q., Bernegossi A.M., Sandoval E.D.P., Peres P.H.F., Galindo D.J., De Thoisy B., Vozdova M., Kubickova S., Barbanti Duarte J.M. Revalidation of Passalites Gloger, 1841 for the Amazon Brown Brocket Deer P. nemorivagus (Cuvier, 1817) (Mammalia, Artiodactyla, Cervidae) ZooKeys. 2023;1167:241–264. doi: 10.3897/zookeys.1167.100577. PubMed DOI PMC

Duarte J.M.B., González S., Maldonado J.E. The Surprising Evolutionary History of South American Deer. Mol. Phylogenet. Evol. 2008;49:17–22. doi: 10.1016/j.ympev.2008.07.009. PubMed DOI

Fiorillo B.F., Sarria-Perea J.A., Abril V., Duarte J.M.B. Cytogenetic Description of the Amazonian Brown Brocket Mazama nemorivaga (Artiodactyla, Cervidae) Comp. Cytogenet. 2013;7:25–31. doi: 10.3897/compcytogen.v7i1.4314. PubMed DOI PMC

Galindo D.J., Martins G.S., Vozdova M., Cernohorska H., Kubickova S., Bernegossi A.M., Kadlcikova D., Rubes J., Duarte J.M. Chromosomal Polymorphism and Speciation: The Case of the Genus Mazama (Cetartiodactyla; Cervidae) Genes. 2021;12:165. doi: 10.3390/genes12020165. PubMed DOI PMC

Hughes J.J., Lagunas-Robles G., Campbell P. The Role of Conflict in the Formation and Maintenance of Variant Sex Chromosome Systems in Mammals. J. Hered. 2024;115:601–624. doi: 10.1093/jhered/esae031. PubMed DOI

Kitano J., Peichel C.L. Turnover of Sex Chromosomes and Speciation in Fishes. Environ. Biol. Fishes. 2012;94:549–558. doi: 10.1007/s10641-011-9853-8. PubMed DOI PMC

Yoshida K., Kitano J. The contribution of female meiotic drive to the evolution of neo-sex chromosomes. Evolution. 2012;66:3198–3208. doi: 10.1111/j.1558-5646.2012.01681.x. PubMed DOI PMC

Pathak S., Lin C.C. Synaptonemal Complex of the Sex-Autosome Trivalent in a Male Indian Muntjac. Chromosoma. 1981;82:367–376. doi: 10.1007/BF00285762. PubMed DOI

Cao X., Jiang H., Zhang X. Polymorphic Karyotypes and Sex Chromosomes in the Tufted Deer (Elaphodus cephalophus): Cytogenetic Studies and Analyses of Sex Chromosome-Linked Genes. Cytogenet. Genome Res. 2005;109:512–518. doi: 10.1159/000084212. PubMed DOI

Bernegossi A.M., Cartes J.L., Cernohorska H., Kubickova S., Vozdova M., Caparroz R., González S., Duarte J.M.B. Resurrection of the Genus Subulo Smith, 1827 for the Gray Brocket Deer, with Designation of a Neotype. J. Mammal. 2023;104:619–633. doi: 10.1093/jmammal/gyac068. DOI

Aquino C.I., Abril V.V., Duarte J.M.B. Meiotic Pairing of B Chromosomes, Multiple Sexual System, and Robertsonian Fusion in the Red Brocket Deer Mazama americana (Mammalia, Cervidae) Genet. Mol. Res. 2013;12:3566–3574. doi: 10.4238/2013.September.13.1. PubMed DOI

Peres P.H.F., Luduvério D.J., Bernegossi A.M., Galindo D.J., Nascimento G.B., Oliveira M.L., Sandoval E.D.P., Vozdova M., Kubickova S., Cernohorska H., et al. Revalidation of Mazama rufa (Illiger 1815) (Artiodactyla: Cervidae) as a Distinct Species out of the Complex Mazama americana (Erxleben 1777) Front. Genet. 2021;12:742870. doi: 10.3389/fgene.2021.742870. PubMed DOI PMC

Dobigny G., Ozouf-Costaz C., Bonillo C., Volobouev V. Viability of X-Autosome Translocations in Mammals: An Epigenomic Hypothesis from a Rodent Case-Study. Chromosoma. 2004;113:34–41. doi: 10.1007/s00412-004-0292-6. PubMed DOI

Deuve J.L., Bennett N.C., Ruiz-Herrera A., Waters P.D., Britton-Davidian J., Robinson T.J. Dissection of a Y-Autosome Translocation in Cryptomys hottentotus (Rodentia, Bathyergidae) and Implications for the Evolution of a Meiotic Sex Chromosome Chain. Chromosoma. 2008;117:211–217. doi: 10.1007/s00412-007-0140-6. PubMed DOI

Borodin P.M., Fedyk S., Chętnicki W., Torgasheva A.A., Pavlova S.V., Searle J.B. Meiosis and Fertility Associated with Chromosomal Heterozygosity. In: Searle J.B., Polly P.D., Zima J., editors. Shrews, Chromosomes and Speciation. Cambridge University Press; Cambridge, UK: 2019. pp. 217–270. (Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Bio).

Rahn M.I., Noronha R.C., Nagamachi C.Y., Pieczarka J.C., Solari A.J., Sciurano R.B. Protein Markers of Synaptic Behavior and Chromatin Remodeling of the Neo-XY Body in Phyllostomid Bats. Chromosoma. 2016;125:701–708. doi: 10.1007/s00412-015-0566-1. PubMed DOI

Vozdova M., Ruiz-Herrera A., Fernandez J., Cernohorska H., Frohlich J., Sebestova H., Kubickova S., Rubes J. Meiotic Behaviour of Evolutionary Sex-Autosome Translocations in Bovidae. Chromosome Res. 2016;24:325–338. doi: 10.1007/s10577-016-9524-x. PubMed DOI

De Oliveira M.L., De Faria Peres P.H., Gatti A., Morales-Donoso J.A., Mangini P.R., Duarte J.M.B. Faecal DNA and Camera Traps Detect an Evolutionarily Significant Unit of the Amazonian Brocket Deer in the Brazilian Atlantic Forest. Eur. J. Wildl. Res. 2020;66:28. doi: 10.1007/s10344-020-1367-2. DOI

Comizzoli P., Holt W.V. Breakthroughs and New Horizons in Reproductive Biology of Rare and Endangered Animal Species. Biol. Reprod. 2019;101:514–525. doi: 10.1093/biolre/ioz031. PubMed DOI

Oliveira M.E.F., Zanetti E.D.S., Cursino M.S., De Fátima Carvalho Peroni E., Rola L.D., Feliciano M.A.R., Canola J.C., Duarte J.M.B. First Live Offspring of Amazonian Brown Brocket Deer (Mazama nemorivaga) Born by Artificial Insemination. Eur. J. Wildl. Res. 2016;62:767–770. doi: 10.1007/s10344-016-1040-y. DOI

Oliveira C.C.C., Queiroz Vacari G., Maurício Barbanti Duarte J. A Method to Freeze Skin Samples for Cryobanks: A Test of Some Cryoprotectants for an Endangered Deer. Biopreserv. Biobank. 2024;22:211–216. doi: 10.1089/bio.2023.0030. PubMed DOI

Verma R., Babu A. Human Chromosomes: Principles & Techniques. 2nd ed. McGraw-Hill, Inc.; New York, NY, USA: 1995.

Telenius H., Carter N.P., Bebb C.E., Nordenskjöld M., Ponder B.A., Tunnacliffe A. Degenerate Oligonucleotide-Primed PCR: General Amplification of Target DNA by a Single Degenerate Primer. Genomics. 1992;13:718–725. doi: 10.1016/0888-7543(92)90147-K. PubMed DOI

Kubickova S., Cernohorska H., Musilova P., Rubes J. The Use of Laser Microdissection for the Preparation of Chromosome-Specific Painting Probes in Farm Animals. Chromosome Res. 2002;10:571–577. doi: 10.1023/A:1020914702767. PubMed DOI

Vozdova M., Kubickova S., Cernohorska H., Fröhlich J., Vodicka R., Rubes J. Comparative Study of the Bush Dog (Speothos venaticus) Karyotype and Analysis of Satellite DNA Sequences and Their Chromosome Distribution in Six Species of Canidae. Cytogenet. Genome Res. 2019;159:88–96. doi: 10.1159/000503082. PubMed DOI

Camacho J.P.M., Sharbel T.F., Beukeboom L.W. B-Chromosome Evolution. Phil. Trans. R. Soc. Lond. B. 2000;355:163–178. doi: 10.1098/rstb.2000.0556. PubMed DOI PMC

Abril V.V., Carnelossi E.A.G., González S., Duarte J.M.B. Elucidating the Evolution of the Red Brocket Deer Mazama americana Complex (Artiodactyla; Cervidae) Cytogenet. Genome Res. 2010;128:177–187. doi: 10.1159/000298819. PubMed DOI

Huang N., Zhou J., Lu W., Luo L., Yuan H., Pan L., Ding S., Yang B., Liu Y. Characteristics and Clinical Evaluation of X Chromosome Translocations. Mol. Cytogenet. 2023;16:36. doi: 10.1186/s13039-023-00669-7. PubMed DOI PMC

Bernegossi A.M., Galindo D.J., Peres P.H.F., Vozdova M., Cernohorska H., Kubickova S., Kadlcikova D., Rubes J., Duarte J.M.B. Comparative Karyotype Analysis of the Red Brocket Deer (M. americana Sensu Lato and M. rufa) Complex: Evidence of Drastic Chromosomal Evolution and Implications on Speciation Process. J. Appl. Genet. 2024;65:601–614. doi: 10.1007/s13353-024-00861-4. PubMed DOI

Sandoval E.D.P., Bernegossi A.M., Gallina S., Reyna-Hurtado R., Duarte J.M.B. Cytogenetic, Molecular, and Morphological Characterization of Odocoileus pandora (Merriam, 1901) (Artiodactyla, Cervidae) Can. J. Zool. 2023;101:967–979. doi: 10.1139/cjz-2022-0037. DOI

Sandoval E.D.P., Jędrzejewski W., Molinari J., Vozdova M., Cernohorska H., Kubickova S., Bernegossi A.M., Caparroz R., Duarte J.M.B. Description of Bisbalus, a New Genus for the Gray Brocket, Mazama cita Osgood, 1912 (Mammalia, Cervidae), as a Step to Solve the Neotropical Deer Puzzle. Taxonomy. 2024;4:10–26. doi: 10.3390/taxonomy4010002. DOI

Sandoval E.D.P., Bernegossi A.M., Gallina S., Reyna-Hurtado R., Duarte J.M. Molecular Cytogenetics Markers Reveal the Existence of a Cryptic Complex of Mazama temama Species. Therya. 2024;15:192–200. doi: 10.12933/therya-24-4913. DOI

Hayman D. Marsupial Cytogenetics. Aust. J. Zool. 1989;37:331–349. doi: 10.1071/ZO9890331. DOI

Toder R., O’Neill R.J.W., Wienberg J., O’Brien P.C.M., Voullaire L., Marshall-Graves J.A. Comparative Chromosome Painting between Two Marsupials: Origins of an XX/XY1Y2 Sex Chromosome System. Mamm. Genome. 1997;8:418–422. doi: 10.1007/s003359900459. PubMed DOI

Steinberg E.R., Bressa M.J., Mudry M.D. Sex Chromosome Systems in Neotropical Primates: What Have We Learnt so Far from Cytogenetics and Genomics? J. Evol. Biol. 2022;35:1589–1600. doi: 10.1111/jeb.14039. PubMed DOI

Di-Battista A., Favilla B.P., Zamariolli M., Nunes N., Defelicibus A., Armelin-Correa L., da Silva I.T., Reymond A., Moyses-Oliveira M., Melaragno M.I. Premature Ovarian Insufficiency Is Associated with Global Alterations in the Regulatory Landscape and Gene Expression in Balanced X-Autosome Translocations. Epigenet. Chromatin. 2023;16:19. doi: 10.1186/s13072-023-00493-8. PubMed DOI PMC

Povill C., de Oliveira M.B., de Abreu F.V.S., de Oliveira R.L., Perini F.A., Monticelli C., Bueno C., dos Santos E., Pissinatti A., Bonvicino C.R. Genetic Diversity and Insights into the Distribution of Brown Howler Monkeys (Alouatta guariba Group) (Atelidae, Alouattinae) Int. J. Primatol. 2023;44:517–539. doi: 10.1007/s10764-023-00352-z. DOI

Iannuzzi A., Parma P., Iannuzzi L. Chromosome Abnormalities and Fertility in Domestic Bovids: A Review. Animals. 2021;11:802. doi: 10.3390/ani11030802. PubMed DOI PMC

Charlesworth B., Wall J.D. Inbreeding, Heterozygote Advantage and the Evolution of Neo-X and Neo-Y Sex Chromosomes. Proc. R. Soc. B Biol. Sci. 1999;266:51. doi: 10.1098/rspb.1999.0603. DOI

Rice W.R. Sex Chromosomes and the Evolution of Sexual Dimorphism. Evolution. 1984;38:735–742. doi: 10.2307/2408385. PubMed DOI

Robinson T.J., Harrison W.R., Ponce de León F.A., Davis S.K., Elder F.F. A Molecular Cytogenetic Analysis of X Chromosome Repatterning in the Bovidae: Transpositions, Inversions, and Phylogenetic Inference. Cytogenet. Cell Genet. 1998;80:179–184. doi: 10.1159/000014976. PubMed DOI

Proskuryakova A.A., Kulemzina A.I., Perelman P.L., Makunin A.I., Larkin D.M., Farré M., Kukekova A.V., Lynn Johnson J., Lemskaya N.A., Beklemisheva V.R., et al. X Chromosome Evolution in Cetartiodactyla. Genes. 2017;8:216. doi: 10.3390/genes8090216. PubMed DOI PMC

Shi L., Yang F., Kumamoto A. The Chromosomes of Tufted Deer (Elaphodus cephalophus) Cytogenet. Cell Genet. 1991;56:189–192. doi: 10.1159/000133085. PubMed DOI

Steiner C.C., Charter S.J., Goddard N., Davis H., Brandt M., Houck M.L., Ryder O.A. Chromosomal Variation and Perinatal Mortality in San Diego Zoo Soemmerring’s Gazelles. Zoo. Biol. 2015;34:374–384. doi: 10.1002/zoo.21223. PubMed DOI

Solari A.J., Pigozzi M.I. Fine Structure of the XY Body in the XY1Y2 Trivalent of the Bat Artibeus lituratus. Chromosome Res. 1994;2:53–58. doi: 10.1007/BF01539454. PubMed DOI

Noronha R.C.R., Nagamachi C.Y., O’Brien P.C.M., Ferguson-Smith M.A., Pieczarka J.C. Meiotic Analysis of XX/XY and Neo-XX/XY Sex Chromosomes in Phyllostomidae by Cross-Species Chromosome Painting Revealing a Common Chromosome 15-XY Rearrangement in Stenodermatinae. Chromosome Res. 2010;18:667–676. doi: 10.1007/s10577-010-9146-7. PubMed DOI

Noronha R.C.R., Nagamachi C.Y., Pieczarka J.C., Marques-Aguiar S., Assis M.F.L., Barros R.M.D.S. Meiotic Analyses of the Sex Chromosomes in Carolliinae-Phyllostomidae (Chiroptera): NOR Separates the XY1Y2 into Two Independent Parts. Caryologia. 2004;57:1–9. doi: 10.1080/00087114.2004.10589365. DOI

Ashley T. X-Autosome Translocations, Meiotic Synapsis, Chromosome Evolution and Speciation. Cytogenet. Genome Res. 2002;96:33–39. doi: 10.1159/000063030. PubMed DOI

Cifuentes-Rincón A., Morales-Donoso J.A., Sandoval E.D.P., Tomazella I.M., Mantellatto A.M.B., De Thoisy B., Duarte J.M.B. Designation of a Neotype for Mazama americana (Artiodactyla, Cervidae) Reveals a Cryptic New Complex of Brocket Deer Species. ZooKeys. 2020;958:143–164. doi: 10.3897/zookeys.958.50300. PubMed DOI PMC

Cursino M.S., Salviano M.B., Abril V.V., Zanetti E.d.S., Duarte J.M.B. The Role of Chromosome Variation in the Speciation of the Red Brocket Deer Complex: The Study of Reproductive Isolation in Females. BMC Evol. Biol. 2014;14:40. doi: 10.1186/1471-2148-14-40. PubMed DOI PMC

Salviano M.B., Cursino M.S., Zanetti E.D.S., Abril V.V., Duarte J.M.B. Intraspecific Chromosome Polymorphisms Can Lead to Reproductive Isolation and Speciation: An Example in Red Brocket Deer (Mazama americana) Biol. Reprod. 2017;96:1279–1287. doi: 10.1093/biolre/iox041. PubMed DOI

Lyon M.F. Gene Action in the X-Chromosome of the Mouse (Mus. musculus L.) Nature. 1961;190:372–373. doi: 10.1038/190372a0. PubMed DOI

Chatziparasidou A., Christoforidis N., Samolada G., Nijs M. Sperm Aneuploidy in Infertile Male Patients: A Systematic Review of the Literature. Andrologia. 2015;47:847–860. doi: 10.1111/and.12362. PubMed DOI

Nadesapillai S., van der Velden J., Braat D., Fleischer K., Peek R. Exploring X Chromosomal Aberrations in Ovarian Cells by Using Fluorescence In Situ Hybridization. J. Vis. Exp. 2023;194:e64734. doi: 10.3791/64734. PubMed DOI

Bonato R.M., Bernegossi A.M., Sandoval E.D.P., Cernohorska H., Vozdova M., Duarte J.M.B. Genética da conservação: Polimorfismo sexual no Veado-roxo e implicações para o manejo reprodutivo em cativeiro; Proceedings of the Anais do 48º Congresso da Associação de Zoológicos e Aquários do Brasil (AZAB); Brasília, Brazil. 10–13 June 2025.

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