Skip to main content
SpringerLink
Log in

Complex evolution of X and Y autosomal translocations in the giant mole-rat, Cryptomys mechowi (Bathyergidae)

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

Cross-species chromosome painting was used to determine homologous chromosomal regions between two species of mole-rat, the naked mole-rat, Heterocephalus glaber (2n = 60), and the giant mole-rat, Cryptomys mechowi (2n = 40), using flow-sorted painting probes representative of all but two of the H. glaber chromosomal complement. In total 43 homologous regions were identified in the C. mechowi genome. Eight H. glaber chromosomes are retained in toto in C. mechowi, and 13 produce two or more signals in this species. The most striking difference in the karyotypes of the two taxa concerns their sex chromosomes. The H. glaber painting probes identified a complex series of translocations that involved the fractionation of four autosomes and the subsequent translocation of segments to the sex chromosomes and to autosomal partners in the C. mechowi genome. An intercalary heterochromatic block (IHB) was detected in sex chromosomes of C. mechowi at the boundary with the translocated autosomal segment. We discuss the likely sequence of evolutionary events that has led to the contemporary composition of the C. mechowi sex chromosomes, and consider these in the light of prevailing views on the genesis of sex chromosomes in mammals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ashley T (2002) X-Autosome translocations, meiotic synapsis, chromosome evolution and speciation. Cytogenet Genome Res 96: 33–39.

    Article  PubMed  CAS  Google Scholar 

  • Bailey J, Carrel L, Chakravarti A, Eichler E (2000) Molecular evidence for a relationship between LINE-1 elements and X chromosome inactivation: the Lyon repeat hypothesis. Proc Natl Acad Sci USA 97: 6634–6639.

    Article  PubMed  CAS  Google Scholar 

  • Baker RJ, Bickham JW (1980) Karyotypic evolution in bats: evidence of extensive and conservative chromosomal evolution in closely related taxa. Syst Zool 29: 239–253.

    Article  Google Scholar 

  • Bennett NC, Faulkes CG (2000). African Mole-Rats: Ecology and Eusociality. Cambridge: Cambridge University Press.

    Google Scholar 

  • Boyle AL, Ballard SG, Ward DC (1990) Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization. Proc Natl Acad Sci USA 87: 7757–7761.

    Article  PubMed  CAS  Google Scholar 

  • Burda H (2001). Determinants of the distribution and radiation of African mole-rats (Bathyergidae, Rodentia). Ecology or geography? Proceedings of the 8th International Symposium on African Small Mammals, Paris, July 1999. Paris: IRD Editions.

  • Casavant NC, Scott L, Cantrell MA et al. (2000) The end of the LINE?: lack of recent L1 activity in a group of South American rodents. Genetics 154: 1809–1817.

    PubMed  CAS  Google Scholar 

  • Dobigny G (2002). Speciation chromosomique chez les especes ouest-africaines de Taterillus (Rodentia, Gerbillinae): implication systematiques et biogeographiques, hypotheses genomiques. Paris: Museum National d'Histoire Naturelle.

    Google Scholar 

  • Dobigny G, Aniskin V, Volobouev V (2002) Explosive chromosome evolution and speciation in the gerbil genus Taterillus (Rodentia, Gerbillinae): a case of two new cryptic species. Cytogenet Genome Res 96: 117–124.

    Article  PubMed  CAS  Google Scholar 

  • Dobigny G, Ozouf-Costaz C, Bonillo C (2004a) Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113: 34–41.

    Article  PubMed  CAS  Google Scholar 

  • Dobigny G, Ozouf-Costaz C, Waters PD et al. (2004b) LINE-1 amplification accompanies explosive genome repatterning in rodents. Chromosome Res 12: 787–793.

    Article  PubMed  CAS  Google Scholar 

  • Ellerman JR, Hayman RW, Holt GWC (1940) The Families and Genera of Living Rodents. London: Trustees of the British Museum (National History), pp. 79–95.

    Google Scholar 

  • Faulkes CG, Bennett NC, Bruford MW et al. (1997) Ecological constraints drive social evolution in the African mole-rats. Proc R Soc Lond B Biol Sci 264: 1619–1627.

    Article  CAS  Google Scholar 

  • Faulkes CG, Verheyen E, Verheyen W, Jarvis JUM, Bennett NC (2004) Phylogeographical patterns of genetic divergence and speciation in African mole-rats. Mol Ecol 13: 613–629.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson-Smith MA, Yang F, O’Brien PCM (1998) Comparative mapping using chromosome sorting and painting. ILAR J 39: 68–76.

    PubMed  Google Scholar 

  • Fredga K (1972) Comparative chromosome studies in mongooses (Carnivora, Voverridae). I. Idiograms of 12 species and karyotype evolution in Herpestinae. Hereditas 71: 1–74.

    Article  PubMed  CAS  Google Scholar 

  • Gartler SM, Riggs AD (1983) Mammalian X-chromosome inactivation. Annu Rev Genet 17: 155–190.

    Article  PubMed  CAS  Google Scholar 

  • Graves JAM (1995) The origin and function of the mammalian Y chromosome and Y-borne genes: an evolving understanding. Bioessays 17: 311–320.

    Article  PubMed  CAS  Google Scholar 

  • Graves JAM, Foster JW (1994) Evolution of mammalian sex chromosomes and sex-determining genes. Int Rev Cytol 154.

  • Graves JAM, Watson JM (1991) Mammalian sex chromosomes: evolution of organization and function. Chromosoma 101: 63–68.

    Article  PubMed  CAS  Google Scholar 

  • Honeycutt RL, Allard MW, Edwards SV (1991) Systematics and evolution of the family Bathyergidae. In: Sherman JUMJ, Sherman RDAPW, eds, The Biology of the Naked Mole-Rat. Princeton, NJ: Princeton University Press, pp. 45–65.

    Google Scholar 

  • Ingram CM, Burda H, Honeycutt RL (2004) Molecular phylogenetics and taxonomy of the African mole-rats, genus Cryptomys and the new genus Coetomys Gray, 1864. Mol Phylogenet Evol 31: 997–1014.

    Article  PubMed  CAS  Google Scholar 

  • Kawalika M, Burda H, Bruggert D (2001) Was Zambia a cradle of the genus Cryptomys (Bathyergidae, Rodentia)? African Small Mammals. Paris: IRD Editions, pp. 253–261.

    Google Scholar 

  • Korenberg JR, Rykowsky MC (1988) Human genome organization: Alu, Lines, and the molecular structure of metaphase chromosome bands. Cell 53: 391–400.

    Article  PubMed  CAS  Google Scholar 

  • Lee MR, Elder FFB (1980) Yeast stimulation of bone marrow mitosis for cytogenetic investigations. Cytogenet Cell Genet 26: 36–40.

    PubMed  CAS  Google Scholar 

  • Lyon MF (1961) Gene action in the X-chromosome of the mouse (Mus musculus L). Nature 190: 372–373.

    Article  PubMed  CAS  Google Scholar 

  • Lyon MF (1998) X-Chromosome inactivation: a repat hypothesis. Cytogenet Cell Genet 80: 133–137.

    Article  PubMed  CAS  Google Scholar 

  • Macholan M, Burda H, Zima J, Misek I, Kawalika M (1993) Karyotype of the giant mole-rat, Cryptomys mechowi (Rodentia, Bathyergidae). Cytogenet Cell Genet 64: 261–263.

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1967) Sex Chromosomes and Sex Linked Genes. New York: Springer, 1967.

    Google Scholar 

  • Ohno S, Kaplan WD, Kinosita R (1959) Formation of the sex chromatin by a single X-chromosome in liver cells of Rattus norvegicus. Exp Cell Res 18: 415–418.

    Article  PubMed  CAS  Google Scholar 

  • Pack SD, Borodin PM, Serov OL, Searle JB (1993) The X-autosome translocation in the common shrew (Sorex araneus L.): late replication in female somatic cells and pairing in male meiosis. Chromosoma 102: 355–360.

    Article  PubMed  CAS  Google Scholar 

  • Parish DA, Vise P, Wichman HA, Bull JJ, Baker RJ (2002) Distribution of LINEs and other repetitive elements in the karyotype of the bar Carollia: implications for X-chromosome inactivation. Cytogenet Genome Res 96: 191–197.

    Article  PubMed  CAS  Google Scholar 

  • Priest JH, Heady JE, Priest RE (1967) Delayed onset of replication of human X chromosomes. J Cell Biol 35: 483–487.

    Article  PubMed  CAS  Google Scholar 

  • Ratomponirina C, Viegas-Pequignot E, Dutrillaux B, Petter F, Rumpler Y (1986) Synaptonemal complexes in Gerbillidae: probable role of intercalated heterochromatin in gonosome–autosome translocations. Cytogenet Cell Genet 43: 161–167.

    PubMed  CAS  Google Scholar 

  • Ross MT, Grafham DV, Coffey AJ (2005) The DNA sequence of the human X chromosome. Nature 434: 325–337.

    Article  PubMed  CAS  Google Scholar 

  • Russell LB, Bangham JW (1961) Variegated-type position effects in the mouse. Genetics 46: 509–525.

    PubMed  CAS  Google Scholar 

  • Takagi N (1974) Differentiation of the X chromosome in early female mouse embryos. Exp Cell Res 86: 127–135.

    Article  PubMed  CAS  Google Scholar 

  • Telenius H, Pelmear AH, Tunnacliffe A et al. (1992) Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow sorted chromosomes. Genes Chromosomes Cancer 4: 257–263.

    PubMed  CAS  Google Scholar 

  • Tucker PK (1986) Sex chromosome–autosome translocations in the leaf-nosed bats, family Phyllostomidae. I. Mitotic analyses of the subfamilies Stenodermatinae and Phyllostominae. Cytogenet Cell Genet 43: 19–27.

    PubMed  CAS  Google Scholar 

  • Van Daele PAAG, Dammann P, Meier JL et al. (2004) Chromosomal diversity in mole-rats of the genus Cryptomys (Rodentia: Bathyergidae) from the Zambezian region: with descriptions of new karyotypes. J Zool Lond 264: 317–326.

    Google Scholar 

  • Vassart M, Seguela A, Hayes H (1995) Chromosomal evolution in gazelles. J Hered 86: 158–167.

    Google Scholar 

  • Veyrunes F, Catalan J, Sicard B et al. (2004) Autosome and sex chromosome diversity among the African pygmy mice, subgenus Nannomys (Murinae; Mus). Chromosome Res 12: 369–382.

    Article  PubMed  CAS  Google Scholar 

  • Viegas-Pequignot E, Benazzou T, Dutrillaux B, Petter F (1982) Complex evolution of sex chromosomes in Gerbillidae (Rodentia). Cytogenet Cell Genet 34: 158–167.

    PubMed  CAS  Google Scholar 

  • Waters PD, Dobigny G, Pardini AT, Robinson TJ (2004) LINE-1 distribution in Afrotheria and Xenarthra: implications for understanding the evolution of LINE-1 in eutherian genomes. Chromosoma 113: 137–144.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Carter NP, Shi L, Ferguson-Smith MA (1995) A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103: 642–652.

    PubMed  CAS  Google Scholar 

  • Yang F, Muller S, Just R, Ferguson-Smith MA (1997a) Comparative chromosome painting in mammals: human and the Indian muntjac (Muntiacus muntjak vaginalis). Genomics 39: 396–401.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, O’Brien PCM, Wienberg J, Ferguson-Smith MA (1997b) A reappraisal of the tandem fusion theory of karyotype evolution in the Indian muntjac using chromosome painting. Chromosome Res 5: 109–117.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Evolutionary Genetics Group, Department of Botany and Zoology, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa

    J. L. Deuve & T. J. Robinson

  2. Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa

    N. C. Bennett

  3. Centre for Veterinary Science, University of Cambridge, Cambridge, UK

    P. C. M. O’Brien & M. A. Ferguson-Smith

  4. School of Biological and Chemical Sciences, Queen Mary, University of London, London, UK

    C. G. Faulkes

  5. Institut des Sciences de l’Evolution (UMR5554), Génétique & Environnement, Université Montpellier II, Montpellier, France

    J. Britton-Davidian

Authors
  1. J. L. Deuve
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. C. Bennett
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. C. M. O’Brien
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. A. Ferguson-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. G. Faulkes
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. Britton-Davidian
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. T. J. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. J. Robinson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Deuve, J.L., Bennett, N.C., O’Brien, P.C.M. et al. Complex evolution of X and Y autosomal translocations in the giant mole-rat, Cryptomys mechowi (Bathyergidae). Chromosome Res 14, 681–691 (2006). https://doi.org/10.1007/s10577-006-1080-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-006-1080-3

Key words

Search

Navigation