{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,18]],"date-time":"2025-10-18T14:42:08Z","timestamp":1760798528411,"version":"build-2065373602"},"reference-count":49,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2020,3,30]],"date-time":"2020-03-30T00:00:00Z","timestamp":1585526400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["19-14-00034"],"award-info":[{"award-number":["19-14-00034"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002261","name":"Russian Foundation for Basic Research","doi-asserted-by":"publisher","award":["19-04-00538"],"award-info":[{"award-number":["19-04-00538"]}],"id":[{"id":"10.13039\/501100002261","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX\/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, molecular cytogenetic methods, and single chromosome DNA sequencing. Among 205 karyotyped voles, one male and three female combinations of sex chromosomes were revealed. The chromosome segregation pattern and karyomorph-related reproductive performances suggested an aberrant sex determination with almost half of the females carrying neo-X\/neo-Y combination. The comparative chromosome painting strongly supported this proposition and revealed the mandarin vole sex chromosome systems originated due to at least two de novo autosomal translocations onto the ancestral X chromosome. The polymorphism in autosome 2 was not related to sex chromosome variability and was proved to result from pericentric inversions. Sequencing of microdissection derived of sex chromosomes allowed the determination of the coordinates for syntenic regions but did not reveal any Y-specific sequences. Several possible sex determination mechanisms as well as interpopulation karyological differences are discussed.<\/jats:p>","DOI":"10.3390\/genes11040374","type":"journal-article","created":{"date-parts":[[2020,4,1]],"date-time":"2020-04-01T05:52:30Z","timestamp":1585720350000},"page":"374","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Complex Structure of Lasiopodomys mandarinus vinogradovi Sex Chromosomes, Sex Determination, and Intraspecific Autosomal Polymorphism"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0951-5209","authenticated-orcid":false,"given":"Svetlana A.","family":"Romanenko","sequence":"first","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Antonina V.","family":"Smorkatcheva","sequence":"additional","affiliation":[{"name":"Department of Vertebrate Zoology, St. Petersburg State University, St. Petersburg 199034, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yulia M.","family":"Kovalskaya","sequence":"additional","affiliation":[{"name":"Severtzov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow 119071, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8420-5203","authenticated-orcid":false,"given":"Dmitry Yu.","family":"Prokopov","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natalya A.","family":"Lemskaya","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Olga L.","family":"Gladkikh","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1556-3984","authenticated-orcid":false,"given":"Ivan A.","family":"Polikarpov","sequence":"additional","affiliation":[{"name":"Department of Vertebrate Zoology, St. Petersburg State University, St. Petersburg 199034, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natalia A.","family":"Serdyukova","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0454-8359","authenticated-orcid":false,"given":"Vladimir A.","family":"Trifonov","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"},{"name":"Department of Natural Science, Novosibirsk State University, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anna S.","family":"Molodtseva","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patricia C. M.","family":"O\u2019Brien","sequence":"additional","affiliation":[{"name":"Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 OES, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2889-4774","authenticated-orcid":false,"given":"Feodor N.","family":"Golenishchev","sequence":"additional","affiliation":[{"name":"Zoological Institute, Russian Academy of Sciences, Saint-Petersburg 199034, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Malcolm A.","family":"Ferguson-Smith","sequence":"additional","affiliation":[{"name":"Cambridge Resource Centre for Comparative Genomics, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 OES, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8282-1085","authenticated-orcid":false,"given":"Alexander S.","family":"Graphodatsky","sequence":"additional","affiliation":[{"name":"Institute of Molecular and Cellular Biology, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,3,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1134\/S1062359009020095","article-title":"Evolution of sex determination in mammals","volume":"36","author":"Bakloushinskaya","year":"2009","journal-title":"Biol. Bull."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1159\/000339294","article-title":"Non-sciuromorph rodent karyotypes in evolution","volume":"137","author":"Romanenko","year":"2012","journal-title":"Cytogenet. Genome Res."},{"key":"ref_3","first-page":"497","article-title":"Unusual sex chromosomes and intrapopulation chromosomal polymorphism in the Chinese vole","volume":"16","author":"Kovalskaya","year":"1974","journal-title":"Tsitologiia"},{"key":"ref_4","first-page":"209","article-title":"Studies on fertility of XO females in the Microtus mandarinus","volume":"44","author":"Zhu","year":"1998","journal-title":"Acta Zool. Sin."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1111\/j.1601-5223.2003.01756.x","article-title":"The origin of the genetical diversity of Microtus mandarinus chromosomes","volume":"139","author":"Zhu","year":"2003","journal-title":"Hereditas"},{"key":"ref_6","first-page":"135","article-title":"Cytogenetic studies of brown field-mouse","volume":"20","author":"Zhu","year":"1993","journal-title":"Yi Chuan Xue Bao"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1034\/j.1601-5223.2003.01615.x","article-title":"Chromosomal polymorphism of mandarin vole, Microtus mandarinus (Rodentia)","volume":"138","author":"Wang","year":"2003","journal-title":"Hereditas"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1111\/j.2006.0018-0661.01950.x","article-title":"Numerical and structural variations of the X chromosomes and no. 2 autosomes in mandarin vole, Microtus mandarinus (Rodentia)","volume":"143","author":"Zhu","year":"2006","journal-title":"Hereditas"},{"key":"ref_9","unstructured":"Kovalskaya, Y.M., and Smorkatcheva, A.V. Overview of geographical variability of karyotype of Chinese vole Lasiopodomys mandarinus Milne-Edwards 1871 (Rodentia, Arvicolinae)\u2013Another group of close species?. Proceedings of the Teriofauna of Russia and adjacent territories."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Gladkikh, O.L., Romanenko, S.A., Lemskaya, N.A., Serdyukova, N.A., O\u2019Brien, P.C., Kovalskaya, J.M., Smorkatcheva, A.V., Golenishchev, F.N., Perelman, P.L., and Trifonov, V.A. (2016). Rapid karyotype evolution in Lasiopodomys involved at least two autosome\u2013sex chromosome translocations. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0167653"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1111\/j.1601-5223.2010.02114.x","article-title":"Two new karyotypes and bandings in Microtus mandarinus faeceus (Rodentia): Two new karyotypes and bandings in M. m. faeceus","volume":"147","author":"Liu","year":"2010","journal-title":"Hereditas"},{"key":"ref_12","first-page":"93","article-title":"Study on synaptonemal complexes in spermatocytes of Microtus mandarinus","volume":"27","author":"Zhang","year":"1999","journal-title":"J. Shaanxi Norm. Univ. Nat. Sci. Ed."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"587","DOI":"10.3724\/SP.J.1005.2009.00587","article-title":"Recent advances on sex determining mechanisms of Microtus mandarinus","volume":"31","author":"Yan","year":"2009","journal-title":"Yi Chuan Hered."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1007\/s10577-011-9261-0","article-title":"Multiple independent evolutionary losses of XY pairing at meiosis in the grey voles","volume":"20","author":"Borodin","year":"2012","journal-title":"Chromosome Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/j.1601-5223.2011.02207.x","article-title":"Exclusion of Sall 4 as the sex-determining gene in the Mandarin vole Microtus mandarinus mandarinus","volume":"148","author":"Chen","year":"2011","journal-title":"Hereditas"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1007\/s00335-007-9076-7","article-title":"Sex determination of Microtus mandarinus mandarinus is independent of Sry gene","volume":"19","author":"Chen","year":"2008","journal-title":"Mamm. Genome"},{"key":"ref_17","unstructured":"Graphodatsky, A.S., and Radjabli, S.I. (1989). Chromosomes of Agricultural and Laboratory Mammals; An atlas, Nauka."},{"key":"ref_18","first-page":"81","article-title":"A rapid fibroblast culture technique for high resolution karyotypes","volume":"58","author":"Stanyon","year":"1991","journal-title":"Ital. J. Zool."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Romanenko, S.A., Perelman, P.L., Trifonov, V.A., Serdyukova, N.A., Li, T., Fu, B., O\u2019Brien, P.C., Ng, B.L., Nie, W., and Liehr, T. (2015). A first generation comparative chromosome map between Guinea pig (Cavia porcellus) and humans. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0127937"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1016\/S0140-6736(71)90287-X","article-title":"A rapid banding technique for human chromosomes","volume":"298","author":"Seabright","year":"1971","journal-title":"Lancet"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1016\/0014-4827(72)90558-7","article-title":"A simple technique for demonstrating centromeric heterochromatin","volume":"75","author":"Sumner","year":"1972","journal-title":"Exp. Cell Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1139\/z03-100","article-title":"Parental care in the captive mandarin vole, Lasiopodomys mandarinus","volume":"81","author":"Smorkatcheva","year":"2003","journal-title":"Can. J. Zool."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Yang, F., Trifonov, V.A., Ng, B.L., Kosyakova, N., and Carter, N.P. (2017). Generation of paint probes from flow-sorted and microdissected chromosomes. Fluorescence in Situ Hybridization (FISH)-Application Guide, Springer.","DOI":"10.1007\/978-3-662-52959-1_6"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1002\/gcc.2870040311","article-title":"Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes","volume":"4","author":"Telenius","year":"1992","journal-title":"Genes. Chromosomes Cancer"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1007\/BF00357691","article-title":"A comparative study of karyotypes of muntjacs by chromosome painting","volume":"103","author":"Yang","year":"1995","journal-title":"Chromosoma"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1007\/s10577-007-1137-y","article-title":"Chromosomal evolution of Arvicolinae (Cricetidae, Rodentia). I. The genome homology of tundra vole, field vole, mouse and golden hamster revealed by comparative chromosome painting","volume":"15","author":"Sitnikova","year":"2007","journal-title":"Chromosome Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1007\/s10577-015-9504-6","article-title":"Genome-wide comparative chromosome maps of Arvicola amphibius, Dicrostonyx torquatus, and Myodes rutilus","volume":"24","author":"Romanenko","year":"2016","journal-title":"Chromosome Res."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"4780","DOI":"10.1093\/nar\/19.17.4780","article-title":"Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR","volume":"19","author":"Ijdo","year":"1991","journal-title":"Nucleic Acids Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1042\/bj2460519","article-title":"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","volume":"246","author":"Maden","year":"1987","journal-title":"Biochem. J."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1006\/geno.1999.5989","article-title":"A Complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps","volume":"62","author":"Yang","year":"1999","journal-title":"Genomics"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1159\/000015513","article-title":"Comparative cytogenetics of hamsters of the genus Calomyscus","volume":"88","author":"Graphodatsky","year":"2000","journal-title":"Cytogenet. Genome Res."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Makunin, A.I., Kichigin, I.G., Larkin, D.M., O\u2019Brien, P.C., Ferguson-Smith, M.A., Yang, F., Proskuryakova, A.A., Vorobieva, N.V., Chernyaeva, E.N., and O\u2019Brien, S.J. (2016). Contrasting origin of B chromosomes in two cervids (Siberian roe deer and grey brocket deer) unravelled by chromosome-specific DNA sequencing. BMC Genomics, 17.","DOI":"10.1186\/s12864-016-2933-6"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"10","DOI":"10.14806\/ej.17.1.200","article-title":"Cutadapt removes adapter sequences from high-throughput sequencing reads","volume":"17","author":"Martin","year":"2011","journal-title":"EMBnet.journal"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","article-title":"Fast and accurate short read alignment with Burrows-Wheeler Transform","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1093\/biostatistics\/kxh008","article-title":"Circular binary segmentation for the analysis of array-based DNA copy number data","volume":"5","author":"Olshen","year":"2004","journal-title":"Biostatistics"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1038\/hdy.1981.97","article-title":"The evolution of XY females in mammals","volume":"47","author":"Bull","year":"1981","journal-title":"Heredity"},{"key":"ref_37","first-page":"S23","article-title":"Aberrant sex chromosome mechanisms in mammals","volume":"23","author":"Fredga","year":"1983","journal-title":"Diffentiation"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1159\/000063029","article-title":"Akodon sex reversed females: The never ending story","volume":"96","author":"Bianchi","year":"2002","journal-title":"Cytogenet. Genome Res."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Fisher, R.A. (1930). The Genetical Theory of Natural Selection, Clarendon Press.","DOI":"10.5962\/bhl.title.27468"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1851","DOI":"10.1101\/gr.2663304","article-title":"Human, mouse, and rat genome large-scale rearrangements: Stability versus speciation","volume":"14","author":"Zhao","year":"2004","journal-title":"Genome Res."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1111\/j.1601-5223.1977.tb00956.x","article-title":"A hypothesis explaining the exceptional sex ratio in the wood lemming (Myopus schisticolor)","volume":"85","author":"Fredga","year":"1977","journal-title":"Hereditas"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/hdy.1979.7","article-title":"Fertile XO males and females in the varying lemming, Dicrostonyx torquatus Pall.(1779)","volume":"42","author":"Gileva","year":"1979","journal-title":"Heredity"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1023\/A:1009273205788","article-title":"XY sex reversal in the wood lemming is associated with deletion of Xp21-23 as revealed by chromosome microdissection and fluorescence in situ hybridization","volume":"6","author":"Liu","year":"1998","journal-title":"Chromosome Res."},{"key":"ref_44","first-page":"1049","article-title":"A novel sex determination system in a close relative of the house mouse","volume":"277","author":"Veyrunes","year":"2009","journal-title":"Proc. R. Soc. Lond. B Biol. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1017\/S0016672300023296","article-title":"Non-random inactivation of the X-chromosome in interspecific hirbid voles","volume":"50","author":"Zakian","year":"1987","journal-title":"Genet Res."},{"key":"ref_46","first-page":"83","article-title":"Relation between polymorphism of chromosome No. 1 and chromosome number in Microtus mandarinus","volume":"28","author":"Zhang","year":"2000","journal-title":"J. Shaanxi Norm. Univ. Nat. Sci. Ed."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1007\/BF00329388","article-title":"Distribution of 18+28S ribosomal genes in mammalian genomes","volume":"53","author":"Hsu","year":"1975","journal-title":"Chromosoma"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Proskuryakova, A., Kulemzina, A., Perelman, P., Serdukova, N., Ryder, O., and Graphodatsky, A. (2018). The Case of X and Y Localization of Nucleolus Organizer Regions (NORs) in Tragulus javanicus (Cetartiodactyla, Mammalia). Genes, 9.","DOI":"10.3390\/genes9060312"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Cazaux, B., Catalan, J., Veyrunes, F., Douzery, E.J., and Britton-Davidian, J. (2011). Are ribosomal DNA clusters rearrangement hotspots? A case study in the genus Mus (Rodentia, Muridae). BMC Evol. Biol., 11.","DOI":"10.1186\/1471-2148-11-124"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/4\/374\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:13:23Z","timestamp":1760174003000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/11\/4\/374"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,30]]},"references-count":49,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2020,4]]}},"alternative-id":["genes11040374"],"URL":"https:\/\/doi.org\/10.3390\/genes11040374","relation":{},"ISSN":["2073-4425"],"issn-type":[{"type":"electronic","value":"2073-4425"}],"subject":[],"published":{"date-parts":[[2020,3,30]]}}}