One more Microtus species with asynaptic sex chromosomes

Authors

  • Jelena Blagojević University of Belgrade, Institute for Biological Research “Siniša Stanković”, Department of Genetic Research, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0001-7102-5510
  • Marija Rajičić University of Belgrade, Institute for Biological Research “Siniša Stanković”, Department of Genetic Research, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-2470-9888
  • Vladimir Jovanović University of Belgrade, Institute for Biological Research “Siniša Stanković”, Department of Genetic Research, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-8056-5065
  • Tanja Adnađević University of Belgrade, Institute for Biological Research “Siniša Stanković”, Department of Genetic Research, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-6665-861X
  • Ivana Budinski University of Belgrade, Institute for Biological Research “Siniša Stanković”, Department of Genetic Research, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0001-8834-4200
  • Branka Pejić University of Belgrade, Institute for Biological Research “Siniša Stanković”, Department of Genetic Research, Bulevar despota Stefana 142, 11060 Belgrade
  • Mladen Vujošević University of Belgrade, Institute for Biological Research “Siniša Stanković”, Department of Genetic Research, Bulevar despota Stefana 142, 11060 Belgrade http://orcid.org/0000-0002-5577-4455

Keywords:

Microtus subterraneus, asynaptic sex chromosomes, meiosis, pine vole, cytotypes

Abstract

Paper description:

  • The Genus Microtus is known as a karyotypically extremely polymorphic group, distinguished by numeric and morphological variations of chromosomes and the presence of species with asynaptic sex chromosomes.
  • Although asynaptic sex chromosomes are frequent in the Microtus genus, this is the first finding for the European pine vole, Microtus subterraneus (2n=52).
  • Up to now, pairing of sex chromosomes during meiosis was investigated in 26 species of which 18 are asynaptic, including this new finding.


Abstract: Arvicoline voles are known as a karyotypically extremely polymorphic group in which the genus Microtus leads with the highest rate of karyotype change. A member of this genus, the European pine vole Microtus subterraneus (de Selys-Longchamps, 1836), is widely distributed in Europe and parts of Asia. There are two cytotypes differing in diploid chromosome number, 2n=54 and 52, each showing different chromosomal polymorphisms. At two localities in southeastern Serbia, Mt. Jastrebac and Vlasina, we found the 2n=52 cytotype. Meiotic preparations from males revealed the presence of asynaptic sex chromosomes. Although asynaptic sex chromosomes are frequent in Microtus, this is the first finding for M. subterraneus. From summarized data it appears that two-thirds of the studied species, mainly from Microtus and Terricola subgenera, possess asynaptic sex chromosomes.

https://doi.org/10.2298/ABS171113004B

Received: November 13, 2017; Revised: January 12, 2018; Accepted: February 1, 2018; Published online: February 7, 2018

How to cite this article: Blagojević J, Rajičić M, Jovanović V, Adnađević T, Budinski I, Pejić B, Vujošević M. One more Microtus species with asynaptic sex chromosomes. Arch Biol Sci. 2018;70(3):…

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References

Skaletsky H, Kuroda-Kawaguchi T, Minx PJ, Cordum HS, Hillier L, Brown LG, Repping S, Pyntikova T, Ali J, Bieri T, Chinwalla A, Delehaunty A, Delehaunty K, Du H, Fewell G, Fulton L, Fulton R, Graves T, Hou SF, Latrielle P, Leonard S, Mardis E, Maupin R, McPherson J, Miner T, Nash W, Nguyen C, Ozersky P, Pepin K, Rock S, Rohlfing T, Scott K, Schultz B, Strong C, Tin-Wollam A, Yang SP, Waterston RH, Wilson RK, Rozen S, Page DC. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature. 2003;423:825-37.

Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD, Grützner F, Kaessmann H. Origins and functional evolution of Y chromosomes across mammals. Nature. 2014;508:488-93.

Matsuda Y, Moens PB, Chapman VM. Deficiency of X and Y chromosomal pairing at meiotic prophase in spermatocytes of sterile interspecific hybrids between laboratory mice (Mus domesticus) and Mus spretus. Chromosoma. 1992;101:483-92.

Lange R, Krause W, Engel W. Analyses of meiotic chromosomes in testicular biopsies of infertile patients. Hum Reprod. 1997;12:2154-8.

Burgoyne PS. Genetic homology and crossing over in the X and Y chromosomes of mammals. Hum Genet. 1982;61:85-90.

Sharp P. Sex chromosome pairing during male meiosis in marsupials. Chromosoma. 1982;86:27-47.

Solari AJ, Ashley T. Ultrastructure and behaviour of the achiasmatic, telosynaptic XY pair of the sand rat (Psammomys obesus). Chromosoma. 1997;62:319-36.

Pathak S, Elder FF, Maxwell BL. Asynaptic behavior of X and Y chromosomes in the Virginia oppossum and the southern pygmy mouse. Cytogenet Cell Genet. 1980;26:142-9.

Borodin PM, Sablina OV, Rodionova MI. Pattern of X-Y chromosome pairing in microtine rodents. Hereditas. 1995;123:17-23.

Maruyama T, Imai HT. Evolutionary rate of the mammalian karyotype. J Theor Biol. 1981;90:111-21.

Zagorodnyuk IV. Karyotypic variability and systematics of the gray voles (Rodentia, Arvicolini). Communication 1. Species composition and chromosomal numbers. Vestnik Zoologii. 1990;2:26-37.

Zima J, Král B. Karyotypes of European mammals II. Acta Sc Nat Brno 1984;18:1-62.

Marchal JA, Acosta MJ, Bullejos M, Diaz de la Guardia R, Sanchez A. Sex chromosomes, sex determination, and sex-linked sequences in Microtidae. Cytogenet Genome Res. 2003;101:266-73.

Megìas-Nogales B, Marchal JA, Acosta MJ, Bullejos M, Diaz de la Guardia R, Sanchez A. Sex chromosomes pairing in two Arvicolidae species: Microtus nivalis and Arvicola sapidus. Hereditas. 2003;138(2):114-21.

Borodin PM, Basheva EA, Dashkevich OA Golenishchev FN, Kartavtseva IV. X-Y Chromosome synapsis and recombination in 3 vole species of Asian lineage of the genus Microtus (Rodentia: Arvicolinae). Cytogenet Genome Res. 2011;132:129-33.

Amori G, Hutterer R, Yigit N, Mitsain G, Kryštufek B, Vohralík V, Zima J, Zagorodnyuk I. Microtus subterraneus. 2016 Dec 16 [errata version 2017; cited 2017 Sep 11]. In: The IUCN Red List of Threatened Species. IUCN; 2016. e.T13489A115115111. Available from: http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T13489A22351439.en

Kryštufek B. Microtus subterraneus (de Selys-Longchamps, 1836). In: Mitchell-Jones AJ, Amori G, Bogdanovicz W, Kryštufek B, Reijnders PJH, Spitzenberger F, Stubbe M, Thissen JBM, Vohralík V, Zima J, editors. The atlas of European mammals. London: Academic Press; 1999. p. 250-1.

Çolak E, Yìğìt, N, Sőzen M, Özukurt S. A Study on taxonomic status of Microtus subterraneus (de Selys Longchamps, 1836) and Microtus majori Thomas, 1906 (Mammalia: Rodentia) in Turkey. Tr J Zool. 1997;22:119-29.

Macholán M, Filippucci MG, Zima J. Genetic variation and zoogeography of pine voles of the Microtus subterraneus/majori group in Europe and Asia Minor. J Zool. 2001;255:31-42.

Bulatova N, Golenishchev F, Bystrakova N, Pavlova S, Kovaĺskaya J, Tikhonov I, Didorchuk M, Ivanov K. Distribution and geographic limits of the alternative cytotypes of two Microtus voles in European Russia. Hystrix. 2007;18(1):99-109.

Živković S, Petrov B, Rimsa D. New data on taxonomy of Balkan Pitymys representatives (Mammalia, Rodentia) in light of karyological analysis. Biosistematika. 1997;1(1):31-42.

Kryštufek B, Fillippucci MG, Macholán M, Zima J, Vujošević M, Simson S.. Does Microtus majori occur in Europe? Z Sauget. 1994;59:349-57.

Kral B, Zima J, Herzig-Straschil B. Karyotype analysis of voles of the genus Pitymys from Southern Austria. Folia Zool. 1978;27(2):129-33.

Sablina OV, Zima J, Radjabli SI, Kryštufek B, Golenisčev FN. New data on karyotype variation in the pine vole, Pitymys subterraneus (Rodentia, Arvicolidae). Vĕst Čs Spol Zool. 1989;53:295-9.

Arrighi FE, Hsu TC. Localization of heterochromatin in human chromosomes. Cytogenetics. 1971;10(2):81-6.

Gamperl R, Ehmann Ch, Bachmann K. Genome size and heterochromatin variation in rodents. Genetica. 1982;58:199-212.

Mitsainas GP, Rovatsos MT, Giagia-Athanasopoulou EB. Heterochromatin study and geographical distribution of Microtus species (Rodentia, Arvicolinae) from Greece. Mamm Biol. 2008;75(3):261-9.

Petrov B, Živković S. Taxonomic status of the representatives of the subgenus Pitymys (Mammalia, Rodentia) from the territory of Yugoslavia based on karyotype analyses (I. Pitymys subterraneus). Arch Biol Sci. 1971;23(3-4):129-33.

Baskevich MI, Kozlovskii AI, Mitev DB. New data on chromosome variability in the pine vole Terricola subterraneus (Rodentia, Cricetidae). Zool Zhurnal. 2000;79:1355-60. Russian.

Chen Y, Guo J. Mammal chromosomes. Beijing: China Science Press; 1986. p. 194-220. Chinese.

Mekada K, Koyasu K, Harada M, Narita Y, Shrestha KC, Oda S-I. Karyotype and X-Y chromosome pairing in the Sikkim vole (Microtus (Neodon) sikimensis). J Zool. 2002;257(3):417-23.

Borodin PM, Rogatcheva MB, Koyasu K, Fukuta K, Mekada K, Oda SI. Pattern of X-Y chromosome pairing in the Japanese field vole, Microtus montebelli. Genome. 1997;40:829-33.

Ashley T, Fredga K. The curious normality of the synaptic association between the sex chromosomes of two arvicoline rodents: Microtus oeconomus and Clethrionomys glareolus. Hereditas. 1994;120:105-11.

Gu W, Wang TZ, Zhu BC. Study on the morphology of sex chromosome pairing in the synaptonamal complexes in Microtus mandarinus. Acta Theriol Sinica. 1999;19:150-4.

Wang JX, Zhao XF, Deng Y, Qi HY, Wang ZJ. Chromosomal polymorphism of mandarin vole, Microtus mandarinus (Rodentia). Hereditas. 2003;138:47-53.

Wolf KW, Baumgart T, Winking H. Meiotic association and segregation of the achiasmatic giant sex chromosomes in the male field vole (Microtus agrestis). Chromosoma. 1988;97:124-33.

Ashley T, Jaarola M, Fredga K. Absence of synapsis during pachynema of the normal sized sex chromosomes of Microtus aralis. Hereditas. 1989;111:295-304.

Borodin PM, Basheva EA, Torgasheva AA, Dashkevich OA, Golenishchev FN, Kartavtseva IV, Mekada K, Dumont BL. Multiple independent evolutionary losses of XY pairing at meiosis in the grey voles. Chromosome Res. 2012;20:259-68.

Jiménez R, Carnero A, Burgos M, Sánchez A, Díaz de la Guardia R. Achiasmatic giant sex chromosomes in the vole Microtus cabrerae (Rodentia, Microtidae). Cytogenet Cell Genet. 1991;57:56-8.

Carnero A, Jiménez R, Burgos M, Sánchez A, Díaz de la Guardia R. Achiasmatic sex chromosomes in Pitymys duodecimcostatus: mechanisms of association and segregation. Cytogenet Cell Genet. 1991;56:78-81.

Rovatsos MT, Mitsainas GP, Stamatopoulos C, Giagia-Athanasopoulou EB. First reports of XXY aneuploidy in natural populations of Thomas’ pine vole Microtus thomasi (Rodentia: Arvicolidae) from Greece. Mamm Biol. 2008;73:342-49.

Jaarola M, Martínková N, Gündüz İ, Brunhoff C, Zima J, Nadachowski A, Amori G, Bulatova NS, Chondropoulos B, Fraguedakis-Tsolis S, González-Esteban J, José López-Fuster M, Kandaurov AS, Kefelioğlu H, da Luz Mathias M, Villate I, Searle JB. Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol. 2004;33:647-63.

Martínková N, Moravec J. Multilocus phylogeny of arvicoline voles (Arvicolini, Rodentia) shows small tree terrace size. Folia Zool. 2012;61:254-67.

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Published

2018-08-20

How to Cite

1.
Blagojević J, Rajičić M, Jovanović V, Adnađević T, Budinski I, Pejić B, Vujošević M. One more Microtus species with asynaptic sex chromosomes. Arch Biol Sci [Internet]. 2018Aug.20 [cited 2024Mar.28];70(3):443-7. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/2364

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