Journal Mobile Options
Table of Contents
Vol. 101, No. 3-4, 2003
Issue release date: 2003
Cytogenet Genome Res 101:266–273 (2003)

Sex chromosomes, sex determination, and sex-linked sequences in Microtidae

Marchal J.A. · Acosta M.J. · Bullejos M. · Díaz de la Guardia R. · Sánchez A.
aDepartamento de Biología Experimental, Facultad de Ciencias Experimentales y de la Salud, Universidad de Jaén, Jaén; bDepartamento de Genética, Facultad de Ciencias, Universidad de Granada, Granada (Spain)

Individual Users: Register with Karger Login Information

Please create your User ID & Password

Contact Information

I have read the Karger Terms and Conditions and agree.

To view the fulltext, please log in

To view the pdf, please log in


The Arvicolidae is a widely distributed rodent group with several interesting characteristics in their sex chromosomes. Here, we summarize the actual knowledge of some of these characteristics. This mammalian group has species with abnormal sex determination systems. In fact, some species present the same karyotype in both males and females, with total absence of a Y chromosome, and hence of SRY and ZFY genes. Other species present fertile, sex-reversed XY females, generally due to mutations affecting X chromosomes. Furthermore, in Microtus oregoni males and females are gonosomic mosaic (the females are XO in the soma and XX in the germ cells, while the males are XY in the soma and OY in the germ cells). Regarding sex chromosomes, some species present enlarged (giant) sex chromosomes because of the presence of large blocks of constitutive heterochromatin, which have been demonstrated to be highly heterogeneous. Furthermore, we also consider the alterations affecting composition and localization of sex-linked genes or repeated sequences. Finally, this rodent group includes species with synaptic and asynaptic sex chromosomes. In fact, several species with asynaptic sex chromosomes have been described. It is interesting to note that within the genus Microtus both types of sex chromosomes are present.   

Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.


  1. Ashley T, Jaarola M, Fredga K: Absence of synapsis during pachynema of the normal sized sex chromosomes of Microtus arvalis. Hereditas 111:295–304 (1989).
  2. Bianchi NO, Bianchi MS, Bailliet G, de la Chapelle A: Characterization and sequencing of the sex determining region Y gene (Sry) in Akodon (Cricetidae) sp. Chromosoma 102:389–395 (1993).
  3. Borodin PM, Sablina OV, Rodionova MI: Pattern of X-Y chromosome pairing in microtine rodents. Hereditas 123:17–23 (1995).
  4. Brockdorff N: X-chromosome inactivation: closing in on proteins that bind Xist RNA. Trends Genet 18:352–358 (2002).
  5. Bullejos M, Sánchez A, Burgos M, Hera C, Jiménez R, Díaz de la Guardia R: Multiple, polymorphic copies of SRY in both males and females of the vole Microtus cabrerae. Cytogenet Cell Genet 79:167–171 (1997).
  6. Bullejos M, Sánchez A, Burgos M, Jiménez R, Díaz de la Guardia R: Multiple mono- and polymorphic Y-linked copies of the SRY HMG-box in Microtidae. Cytogenet Cell Genet 86:46–50 (1999).
  7. Burgos M, Jiménez R, Díaz de la Guardia R: XY females in Microtus cabrerae (Rodentia, Microtidae): a case of possibly Y-linked sex reversal. Cytogenet Cell Genet 49:275–277 (1988a).
  8. Burgos M, Jiménez R, Díaz de la Guardia R: Comparative study of G- and C-banded chromosomes of five species of Microtidae: a chromosomal evolution analysis. Genome 30:540–546 (1988b).
  9. Burgos M, Jiménez R, Olmos DM, Díaz de la Guardia R: Heterogeneous heterochromatin and size variations in the sex chromosomes of Microtus cabrerae. Cytogenet Cell Genet 47:75–79 (1988c).
  10. Burgos M, Olmos DM, Jiménez R, Sánchez A, Díaz de la Guardia R: Fluorescence banding in four species of Microtidae: an analysis of the evolutive changes of the constitutive heterochromatin. Genetica 81:11–16 (1990).
  11. Carleton MD, Musser GG: Muroid rodents, in Anderson S, Jones JK (eds): Orders and families of recent mammals of the world, pp 289–379 (John Wiley and Sons, New York 1984).
  12. 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 56:78–81 (1991).
  13. Chaline J, Graf JD: Phylogeny of the Arvicolidae (Rodentia): Biochemical and paleontological evidence. J. Mammal 69:22–33 (1988).
  14. Clemson CM, McNeil JA, Willard HF, Lawrence JB: XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J Cell Biol 132:259–275 (1996).
  15. Clerc P, Avner P: Multiple elements within the Xic regulate random X inactivation in mice. Semin Cell Dev Biol 14:85–92 (2003).
  16. Elisaphenko EA, Nesterova TB, Duthie SM, Ruldugina OV, Rogozin IB, Brockdorff N, Zakian SM: Repetitive DNA sequences in the common vole: cloning, characterization and chromosome localization of two novel complex repeats MS3 and MS4 from the genome of the East European vole Microtus rossiaemeridionalis. Chrom Res 6:351–360 (1998).
  17. Fernández R, Barragán MJL, Bullejos M, Marchal JA, Martínez S, Díaz de la Guardia, R, Sánchez A: Molecular and cytogenetic characterization of highly repeated DNA sequences in the vole Microtus cabrerae. Heredity 87:637–646 (2001).
  18. Fernández R, Barragán MJL, Bullejos M, Marchal JA, Martínez S, Díaz de la Guardia R, Sánchez A: Mapping the SRY gene in Microtus cabrerae: a vole species with multiple SRY copies in males and females. Genome 45:600–603 (2002).
  19. Fredga K: Bizarre mammalian sex-determining mechanisms, in Short RV, Balaban E (eds): The Differences Between the Sexes, pp 419–431 (Cambridge University Press, Cambridge 1994).
  20. Fredga K, Jaarola M: The origin and distribution of the Lund Y chromosome in Microtus agrestis (Rodentia, Mammalia). Hereditas 126:25–34 (1997).
  21. Fredga K, Lyapunova EA: Fertile males with two X chromosomes in Ellobius tancrei (Rodentia, Mammalia). Hereditas 115:86–97 (1991).
  22. Gileva EA, Chebotar NA: Fertile XO males and females in the varying lemming, Dicrostomix torquatus Pall (1779). Heredity 42:67–77 (1979).
  23. Gubbay J, Collignon J, Koopman P, Capel B, Economou A, Münsterberg A, Vivian N, Goodfellow P, Lovell-Badge R: A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346:245–250 (1990).
  24. Honda T, Suzuki H, Ithu M: An unusual sex chromosome constitution found in the amami spinous country-rat, Tokudaia osimensis osimensis. Jpn Genet 52:247–249 (1977).
  25. Ivanov SV, Modi WS: Molecular characterization of the complex sex-chromosome heterochromatin in the rodent Microtus chrotorrhinus. Cytogenet Cell Genet 75:49–56 (1996).
  26. 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 57:56–58 (1991).
  27. Just W, Rau W, Vogel W, Akhverdian M, Fredga K, Graves JAM, Lyapunova E: Absence of Sry in species of the vole Ellobius. Nature Genet 11:117–118 (1995).
  28. Kalscheuer V, Singh AP, Nanda I, Sperling K, Neitzel H: Evolution of the gonosomal heterochromatin of Microtus agrestis: rapid amplification of a large, multimeric, repeat unit containing a 3.0-kb (GATA)11-positive, middle repetitive element. Cytogenet Cell Genet 73:171–178 (1996).
  29. Kholodilov NG, Mayorov VI, Mullokandov MR, Cheryaukene OV, Nesterova TB, Rogozin IB, Zakian SM: LINE-1 element in the vole Microtus subarvalis. Mammal Genome 4:624–626 (1993).
  30. Lau YFC, Yang-Feng TL, Elder B, Fredga K, Wiberg UH: Unusual distribution of Zfy and Zfx sequences on the sex chromosomes of the wood lemming, a species exhibiting XY sex reversal. Cytogenet Cell Genet 60:48–54 (1992).
  31. Liu W-S, Eriksson L, Fredga K: XY sex reversal in the wood lemming is associated with deletion of Xp21-23 as revealed by chromosome microdissection and fluorescence in situ hybridization. Chrom Res 6:379–383 (1998).
  32. Liu W-S, Nordqvist K, Lau YFC, Fredga K: Characterization of the Xp21-23 region in the wood lemming, a region involved in the XY sex reversal. J exp Zool 290:551–557 (2001).
  33. Lundrigan BL, Tucker PK: Evidence for multiple functional copies of the male sex-determining locus, Sry, in african murine rodents. J molec Evol 45:60–65 (1997).
  34. Mardon G, Page DC: The sex-determining region of the mouse Y chromosome encodes a protein with a highly acidic domain and 13 zinc fingers. Cell 56:765–770 (1989).
  35. Maruyama T, Imai HT: Evolutionary rate of the mammalian karyotype. J theor Biol 90:111–121 (1981).
  36. Matthey R: La formule chromosomique et le problème de la détermination sexuelle chez Ellobius lutescens Tomas (Rodentia-Muridae-Microtinae). Arch Klaus-Stift VererbForsch 28:65–73 (1953).
  37. Matthey R: The chromosome formulae of eutherian mammals, in Chiarelli AB, Capanna E (eds): Cytotaxonomy and vertebrate evolution, pp 531–616 (Academic Press, London 1973).
  38. Mayorov VI, Adkison LR, Vorobyeva NV, Khrapov EuA, Kholodhov NG, Rogozin IB, Nesterova TB, Protopopov AI, Sablina OV, Graphodatsky AS, Zakian SM: Organization and chromosomal localization of a B1-like containing repeat of Microtus subarvalis. Mammal Genome 7:593–597 (1996).
  39. Mayorov VI, Rogozin IB, Adkison LR: Characterization of several LINE-1 elements in Microtus kirgisorum. Mammal Genome 10:724–729 (1999).
  40. Megías-Nogales B, Marchal JA, Acosta MJ, Bullejos M, Díaz de la Guardia R, Sánchez A: Sex chromosomes pairing in two Arvicolidae species: Microtus nivalis and Arvicola sapidus. Hereditas, in press (2003).
  41. Modi WS: Phylogenetic analyses of chromosomal banding patterns among the Neartic Arvicolidae (Mammalia, Rodentia). Syst Zool 36:109–136 (1987a).
  42. Modi WS: C-banding analyses and the evolution heterochromatin among arvicolid rodents. J Mammal 68:704–714 (1987b).
  43. Modi WS: Nucleotide sequence and genomic organization of a tandem satellite array from the rock vole Microtus chrotorrhinus (Rodentia). Mammal Genome 3:226–232 (1992).
  44. Modi WS: Comparative analysis of heterochromatin in Microtus: sequence heterogeneity and localized expansion and contraction of satellite DNA arrays. Cytogenet Cell Genet 62:142–148 (1993a).
  45. Modi WS: Heterogeneity in the concerted evolution process of a tandem satellite array in Meadow Mice (Microtus). J molec Evol 37:48–56 (1993b).
  46. Modi WS: Rapid, localized amplification of a unique satellite DNA family in the rodent Microtus chrotorrhinus. Chromosoma 102:484–490 (1993c).
  47. Nagamine CM: The testis determining gene, SRY, exists in multiple copies in Old World rodents. Genet Res 64:151–159 (1994).
  48. Nagamine CM, Chan K, Hake LE, Lau YF: The two candidate testis-determining Y genes (Zfy-1 and Zfy-2) are differentially expressed in fetal and adult mouse tissues. Genes Dev 4:63–74 (1990).
  49. Nanda I, Neitzel H, Sperling K, Studer R, Epplen JT: Simple GATCA repeats characterize the X chromosome heterochromatin in Microtus agrestis, European field vole (Rodentia, Cricetidae). Chromosoma 96:213–219 (1988).
  50. Neitzel H, Kalscheuer V, Henschel S, Digweed M, Sperling K: Beta-heterochromatin in mammals: evidence from studies in Microtus agrestis based on the extensive accumulation of L1 and non-L1 retroposons in the heterochromatin. Cytogenet Cell Genet 80:165–172 (1998).
  51. Neitzel H, Kalscheuer V, Singh AP, Henschel S, Sperling K: Copy and paste: the impact of a new non-L1 retroposon on the gonosomal heterochromatin of Microtus agrestis. Cytogenet Genome Res 96:179–185 (2002).
  52. Nesterova TB, Mazurok NA, Matveeva NM, Shilov AG, Yantsen EI, Ginsburg Ekh, Goss SJ, Zakian SM: Demonstration of the X-linkage and order of the genes GLA, G6PD, HPRT, and PGK in two vole species of the genus Microtus. Cytogenet Cell Genet 65:250–255 (1994).
  53. Nesterova TB, Duthie SM, Mazurok NA, Isaenko AA, Rubtsova NV, Zakian SM, Brockdorff N: Comparative mapping of the X chromosome in vole species of the genus Microtus. Chrom Res 6:41–48 (1998a).
  54. Nesterova TB, Mazurok NA, Rubtsova NV, Isaenko AA, Zakian SM: The vole gene map. ILAR Journal 39:138–144 (1998b).
  55. Nesterova TB, Slobodyanyuk SY, Elisaphenko EA, Shevchenko AI, Johnston C, Pavlova ME, Rogozin IB, Kolesnikov NN, Brockdorff N, Zakian SM: Characterization of the genomic Xist locus in the rodents reveals conservation of overall gene structure and tandem repeats but rapid evolution of unique sequence. Genome Res 11:833–849 (2001).
  56. Ohno S: Sex chromosomes and sex liked genes (Springer Verlag, Berlin 1967).
  57. Ohno S, Jainchill J, Stenius C: The creeping vole (Microtus oregoni) as a gonosomic mosaic. I. The OY/XY constitution of the male. Cytogenetics 2:232–239 (1963).
  58. Ohno S, Stenius C, Christian L: The XO as the normal female of the creeping vole (Microtus oregoni), in Darlington CD, Lewis KR (eds): Chromosomes Today 1, pp 182–187 (Oliver & Boyd, Edinburgh and London 1966).
  59. Page DC, Mosher R, Simpson EM, Fisher EM, Mardon G, Pollack J, McGillivray B, de la Chapelle A, Brown LG: The sex-determining region of the human Y chromosome encodes a finger protein. Cell 51:1091–1104 (1987).
  60. Shevchenko AI, Mazurok NA, Slobodyanyuk SY, Zakian SM: Comparative analysis of the MSAT-160 repeats in four species of the common vole (Microtus, Arvicolidae). Chrom Res 10:117–126 (2002).
  61. Sinclair AH, Foster JW, Spencer JA, Page DC, Palmer M, Goodfellow PN, Graves JA: Sequences homologous to ZFY, a candidate human sex-determining gene, are autosomal in marsupials. Nature 336:780–783 (1988).
  62. Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN: A gene from the human sex determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 364:240–244 (1990).
  63. Singh AP, Henschel S, Sperling K, Kalscheuer V, Neitzel H: Differences in the meiotic pairing behavior of gonosomal heterochromatin between female and male Microtus agrestis: implications for the mechanism of heterochromatin amplification on the X and Y. Cytogenet Cell Genet 91:253–260 (2000).
  64. Solari AJ: Sex chromosomes pairing and fertility in the heterogametic sex of mammals and birds, in Gillies C (ed): Fertility and Chromosome Pairing: Recent Studies in Plants and Animals, pp 77–107 (CRC Press, Boca Raton 1989).
  65. Solari AJ, Ashley T: Ultrastructure and behavior of the achiasmatic, telosynaptic XY pair of the sand rat (Psammomys obesus). Chromosoma 62:319–336 (1977).
  66. Soullier S, Hanni C, Catzeflis F, Berta P, Laudet V: Male sex determination in the spiny rat Tokudaia osimensis (Rodentia: Muridae) is not Sry dependent. Mammal Genome 9:590–592 (1998).
  67. Sutou S, Mitsui Y, Tsuchiya K: Sex determination without the Y chromosome in two Japanese rodents Tokudaia osimensis osimensis and Tokudaia osimensis spp. Mammal Genome 12:17–21 (2001).
  68. Vogel W, Jainta S, Rau W, Geerkens C, Baumstark A, Corrrea-Cerro L-S, Ebenhoch C, Just W: Sex determination in Ellobius lutescens: The story of an enigma. Cytogenet Cell Genet 80:214–221 (1998).
  69. Zakian SM, Kulbakina NA, Meyer MN, Semenova LA, Bochkarev MN, Radjabli SI, Serov OL: Non-random inactivation of the X-chromosome in interspecific Irbid voles. Genet Res 50:23–27 (1987).
  70. Zakian SM, Nesterova TB, Cheryaukene OV, Bochkarev MN: Heterochromatin as a factor affecting the inactivation of the X-chromosome in interspecific hybrid voles (Microtidae, Rodentia). Genet Res 58:105–110 (1991).
  71. Zambrowicz BP, Zimmermann JW, Harendza CJ, Simpson EM, Page DC, Brinster RL, Palmiter RD: Expression of a mouse Zfy-1/lacZ transgene in the somatic cells of the embryonic gonad and germ cells of the adult testis. Development 120:1549–1559 (1994).

Pay-per-View Options
Direct payment This item at the regular price: USD 38.00
Payment from account With a Karger Pay-per-View account (down payment USD 150) you profit from a special rate for this and other single items.
This item at the discounted price: USD 26.50