Skip to main content
SpringerLink
Log in

Autosome and Sex Chromosome Diversity Among the African Pygmy Mice, Subgenus Nannomys (Murinae; Mus)

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

The African pygmy mice, subgenus Nannomys, constitute the most speciose lineage of the genus Mus with 19 recognized species. Although morphologically very similar, they exhibit considerable chromosomal diversity which is here confirmed and extended by the G-banding analysis of 65 mice from West and South Africa. On the basis of their karyotype and distribution area, the specimens were assigned to at least five species. Extensive differentiation both within and between species was observed that involved almost exclusively Robertsonian translocations, 23 of which are newly described. Two of the rearrangements were sex chromosome-autosome translocations, associated in some cases with partial deletions of the X or Y chromosomes. Several authors have predicted that the highly deleterious effect of this rearrangement would be reduced if the sex and autosomal segments were insulated by a block of centromeric heterochromatin. The C-banding analyses performed showed that among the species carrying X-autosome translocations, one followed the expected pattern, while the other did not. In this case, functional isolation of the sex and autosome compartments must involve other repetitive sequences or genomic traits that require further molecular characterization. Such studies will provide insight into the causes and consequences of the high diversity of sex chromosome rearrangements in this subgenus.

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

  • Aniskin VM, Lavrenchenko LA, Varshavskii AA, Milishnikov AN (1998) Karyotypes and cytogenetic differentiation of two african mouse species of genus Mus (Rodentia, Muridae). Russ J Genet 34: 80–85.

    CAS  Google Scholar 

  • Arakawa Y, Nishida-Umehara C, Matsuda Y, Sutou S, Suzuki H (2002) X-chromosomal localization of mammalian Y-linked genes in two XO species of the Ryukyu spiny rat. Cytogenet Genome Res 99: 303–309.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bailey JA, Carrel L, Chakravarti A, Eichler EE (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 

  • Banaszek A, Fedyk S, Szalaj KA, Chetnicki W (2000) A comparison of spermatogenesis in homozygotes, simple Robertsonian heterozygotes and complex heterozygotes of the common shrew (Sorex araneus L.). Heredity 84: 570–577.

    Article  PubMed  Google Scholar 

  • Bianchi NO (2002) Akodon sex reversed females: the never ending story. Cytogenet Genome Res 96: 60–65.

    Article  PubMed  CAS  Google Scholar 

  • Britton-Davidian J, Catalan J, Ramalhinho MDG et al. (2000) Rapid chromosomal evolution in island mice. Nature 403: 158.

    Article  PubMed  CAS  Google Scholar 

  • Bronner GN, Hoffmann M, Taylor PJ et al. (2003) A revised systematic checklist of the extant mammals of the southern African subregion. Durban Museum Novitates 28: 56–106.

    Google Scholar 

  • Castiglia R, Capanna E (2000) Contact zone between chromosomal races of Mus musculus domesticus. 2. Fertility and segregation in laboratory-reared and wild mice heterozygous for multiple Robertsonian rearrangements. Hereditas 85: 147–156.

    Article  Google Scholar 

  • Castiglia R, Gormung E, Corti M (2002) Cytogenetic analyses of chromosomal rearrangements in Mus minuto?des/ musculo?des from North-West Zambia through mapping of the telomeric sequence (TTAGGG)n and banding techniques. Chromosome Res 10: 399–406.

    Article  PubMed  CAS  Google Scholar 

  • Catzeflis F, Denys C (1992) The African Nannomys (Muridae): an early offshoot from the Mus lineage. Evidence from scnDNA hybridization experiments and compared morphology. Israel J Zool 38: 219–231.

    Google Scholar 

  • Delneri D, Colson I, Grammenoudi S, Roberts IN, Louis EJ, Oliver SG (2003) Engineering evolution to study speciation in yeasts. Nature 422: 68–72.

    Article  PubMed  CAS  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, Volobouev V (submitted) Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study.

  • Evans EP, Breckon G, Ford CE (1964) An air-drying method for meiotic preparations from mammalian testes. Cytogenetics 3: 289–294.

    Google Scholar 

  • Fredga K (1965) A new sex determining in a mammal. Chromosomes of Indian mongoose (Herpestes auropunctatus). Hereditas 52: 411–420.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Garagna S, Redi CA, Zuccoti M, Britton-Davidian J, Winking H (1990) Kinetics of oogenesis in mice heterozygous for Robertsonian translocations. Differentiation 42: 167–171.

    PubMed  CAS  Google Scholar 

  • Garagna S, Marziliano N, Zuccotti M, Searle J, Capanna E, Redi CA (2001) Pericentromeric organization at the fusion point of mouse Robertsonian translocation chromosomes. Proc Natl Acad Sci USA 98: 171–175.

    Article  PubMed  CAS  Google Scholar 

  • Grant PR (1981) Speciation and the adaptive radiation of the Darwin's Finches. Am Sci 69: 653–663.

    Google Scholar 

  • Gropp A, Winking H, Redi C (1982) Consequences of Robertsonian heterozygosity: segregational impairment of fertility versus male-limited sterility. In: Crosignani PG, Rubin BL, eds. Serono Clinical Colloquia on Reproduction N o 3. New York: Academic Press/Grune and Stratton 3: 115–134.

    Google Scholar 

  • Hauffe HC, Searle JB (1998) Chromosomal heterozygosity and fertility in house mice (Mus musculus domesticus) from Northern Italy. Genetics 150: 1143–1154.

    PubMed  CAS  Google Scholar 

  • Jaafar H, Gabriel-Robez O, Rumpler Y (1993) Chromosomal anomalies and disturbance of transcriptional activity at the pachytene stage of meiosis: relationship to male sterility. Cytogenet Cell Genet 64: 273–280.

    PubMed  CAS  Google Scholar 

  • Jotterand M (1970) Un nouveau système polymorphe robertsonien chez une nouvelle espèce de 'Leggada' (Mus goundae Petter). Experientia 26: 1360–1361.

    Article  PubMed  CAS  Google Scholar 

  • Jotterand M (1972) Le polymorphisme chromosomique des Mus (Leggadas) africains. Cytogénétique, zoogéographie, évolution. Rev Suisse Zool 79: 287–359.

    PubMed  CAS  Google Scholar 

  • Jotterand-Bellomo M (1984) L'analyse cytogénétique de deux espèces de Muridae africains, Mus oubanguii et Mus minutoides/musculoides: polymorphisme chromosomique et ébauche d'une phylogénie. Cytogenet Cell Genet 38: 182–188.

    Google Scholar 

  • Jotterand-Bellomo M (1986) Le genre Mus africain, un exemple d'homogénéité caryotypique: étude cytogénétique de Mus minutoides/musculoides (Cô te d'Ivoire), de M. setulosus (République Centrafricaine), et de M. mattheyi (Burkina Faso). Cytogenet Cell Genet 42: 99–104.

    Google Scholar 

  • Jotterand-Bellomo M (1988) Chromosome analysis of five specimens of Mus bufo-triton (Muridae) from Burundi (Africa): three cytogenetic entities, a special type of chromosomal sex determination, taxonomy, and phylogeny. Cytogenet Cell Genet 48: 88–91.

    Google Scholar 

  • Just W, Rau W, Vogel W et al. (1995) Absence of SRY in species of the vole Ellobius. Nature Genet 11: 117–118.

    Article  PubMed  CAS  Google Scholar 

  • Just W, Baumstark A, Hameister H et al. (2002) The sex determination in Ellobius lutescens remains bizarre. Cytogenet Genome Res 96: 146–153.

    Article  PubMed  CAS  Google Scholar 

  • King M (1993) Species evolution. The role of chromosome change. Cambridge: Cambridge University Press.

    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 

  • Losos JB, Jackman TR, Larson A, de Queiroz Q, Rodriguez-Schettino L (1998) Contingency and determinism in replicated adaptive radiations of island lizards. Science 279: 2115–2118.

    Article  PubMed  CAS  Google Scholar 

  • Macholan M (2001) Multivariate analysis of morphometric variation in Asian Mus and sub-saharan Nannomys (Rodentia: Muridae). Zool Anz 240: 7–14.

    Google Scholar 

  • Marshall JT (1981) Taxonomy. In: Foster HL, Small JD, Fox JG, eds. The mouse in biomedical research, volume 1. New York: Academic Press, pp 17–26.

    Google Scholar 

  • Matthey R (1952) Chromosomes de Muridae (Microtinae et Cricetinae). Chromosoma 5: 113–138.

    Article  PubMed  CAS  Google Scholar 

  • Matthey R (1959) Formules chromosomiques de Muridae et Spalacidae. La question du polymorphisme chromosomique chez les mammifères. Rev Suisse Zool 66: 175–209.

    Google Scholar 

  • Matthey R (1964) Evolution chromosomique et spéciation chez les Mus du sous-genre Leggada. Experientia 20: 657–665.

    Article  PubMed  CAS  Google Scholar 

  • Matthey R (1965) Etudes de cytogénétique sur les Murinae africains appartenant aux genres Arvicanthis, Praomys, Acomys et Mastomys (Rodentia). Mammalia 29: 228–249.

    Google Scholar 

  • Matthey R (1966) Le polymorphisme chromosomique des Mus africains du sous-genre Leggada. Révision générale portant sur l'analyse de 213 individus. Rev Suisse Zool 73: 585–607.

    Google Scholar 

  • Matthey R (1967) Cytogénétique des Leggada: (1) la formule chromosomique de Mus (Leggada) bufo, (2) Nouvelles données sur la délétion portant sur le bras court d'un X chez Mus (Leggada) triton. Experientia 23: 133–134.

    Article  PubMed  CAS  Google Scholar 

  • Matthey R (1970) Nouvelles données sur la cytogénétique et la spéciation des Leggada (Mammalia-Rodentia-Muridae). Experientia 26: 102–103.

    Article  PubMed  CAS  Google Scholar 

  • Mercer SJ, Wallace BMN, Searle JB (1992) Male common shrews (Sorex araneus) with long chain configurations can be fertile: implications for chromosomal models of speciation. Cytogenet Cell Genet 60: 68–73.

    PubMed  CAS  Google Scholar 

  • Metcalfe CJ, Eldridge MDB, Toder R, Johnston PG (1998) Mapping the distribution of the telomeric sequence (T2AG3)n in the Macropodoidea (Marsupialia), by fluorescence in situ hybridization. I. The swamp wallaby, Wallabia bicolor. Chromosome Res 6: 603–610.

    Article  PubMed  CAS  Google Scholar 

  • Musser GG, Carleton MD (1993) Family Muridae. In: Wilson DE, Reeder DM, eds. Mammal species of the world. A taxonomic and geographic reference. Washington and London: Smithsonian Institution Press, pp 501–755.

    Google Scholar 

  • Neitzel H (1987) Chromosome evolution of Cervidae: karyotypic and molecular aspects. In: Obe G, Basler A, eds. Cytogenetics. Berlin, Heidelberg: Springer-Verlag, pp 90–112.

    Google Scholar 

  • Pack SD, Borodin PM, Serov OL, Searle JB (1993) The Xautosome 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 others repetitive elements in the karyotype of the bat Carollia: implications for X-chromosome inactivation. Cytogenet Genome Res 96: 191–197.

    Article  PubMed  CAS  Google Scholar 

  • Petter F (1963) Contribution à la connaissance des souris africaines. Mammalia 27: 602–607.

    Google Scholar 

  • Petter F (1981) Les souris africaines du groupe sorella (Rongeurs, Muridés). Mammalia 45: 313–320

    Article  Google Scholar 

  • Pialek J, Hauffe HC, Rodriguez-Clark KM, Searle JB (2001) Raciation and speciation in house mice from the Alps: the role of chromosomes. Mol Ecol 10: 613–625.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Redi CA, Capanna E (1988) Robertsonian heterozygotes in the house mouse and the fate of their germ cells. In: Daniel A, eds. The cytogenetics of mammalian autosomal rearrangements. New York: Alan R. Liss, Inc., pp 315–359.

    Google Scholar 

  • Redi CA, Garagna S, Capanna E (1990) Nature's experiment with in situ hybridization? A hypothesis for the mechanism of Rb fusion. J Evol Biol 3: 133–137.

    Article  Google Scholar 

  • Rieseberg LH (2001) Chromosomal rearrangements and speciation. Trends Ecol Evol 16: 351–358.

    Article  PubMed  Google Scholar 

  • Rodrigues Noronha RC, Nagamachi CY, Pieczarka JC, Marques-Aguiar S, De Souza Barros RM (2001) Sex-autosome translocations: meiotic behaviour suggests an inactivation block with permanence of autosomal gene activity in Phyllostomids bats. Caryologia 54: 267–277.

    Google Scholar 

  • Rokas A, Holland PWH (2000) Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15: 454–459.

    Article  PubMed  Google Scholar 

  • Sa?d K, Saad A, Auffray JC, Britton-Davidian J (1993) Fertility estimates in the Tunisian all-acrocentric and Robertsonian populations of the house mouse and their chromosomal hybrids. Heredity 71: 532–538.

    Google Scholar 

  • Sato A, O'hUigin C, Figueroa F et al. (1999) Phylogeny of Darwin's finches as revealed by mtDNA sequences. Proc Natl Acad Sci USA 96: 5101–5106.

    Article  PubMed  CAS  Google Scholar 

  • Seabright J (1971) A rapid technique for human chromosomes. Lancet II: 971–972.

    Article  Google Scholar 

  • Searle JB (1993) Chromosomal hybrid zones in eutherian mammals. In: Harrison RG, eds. Hybrid zones and the evolutionary process. Oxford: Oxford University Press, pp 309–353.

    Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75: 304–306.

    Article  PubMed  CAS  Google Scholar 

  • Sutou S, Mitsui Y, Tsuchiya K (2001) Sex determination without the Y chromosome in two Japanese rodents Tokudaia osimensis osimensis and Tokudaia osimensis spp. Mamm Genome 12: 17–21.

    Article  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 

  • Vassart M, Seguela A, Hayes H (1995) Chromosomal evolution in Gazelles. J Hered 86: 216–227.

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Volobouev V, Granjon L (1996) A finding of the XX/XY1Y2 sex-chromosome system in Taterillus arenarius (Gerbillinae, Rodentia) and its phylogenetic implications. Cytogenet Cell Genet 75: 45–48.

    PubMed  CAS  Google Scholar 

  • Yang F, O'Brien PCM, Wienberg J, Ferguson-Smith MA (1997) 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. Institut des Sciences de l'Evolution (UMR5554), Génétique & Environnement, Université Montpellier II, Montpellier, France; Tel

    Frédéric Veyrunes, Josette Catalan & Janice Britton-Davidian

  2. Laboratoire de Mammalogie (CBGP, UMR022), Institut de Recherche pour le Développement, Bamako, Mali

    Bruno Sicard & Laurent Granjon

  3. Department of Zoology, University of Stellenbosch, South Africa

    Terence J. Robinson & Gauthier Dobigny

  4. Laboratoire de Mammalogie (CBGP, UMR022), Institut de Recherche pour le Développement, Dakar, Senegal

    Jean-Marc Duplantier

  5. Laboratoire de Zoologie Mammifères et Oiseaux, Muséum National d'Histoire Naturelle, Paris, France

    Laurent Granjon & Gauthier Dobigny

Authors
  1. Frédéric Veyrunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Josette Catalan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruno Sicard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Terence J. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jean-Marc Duplantier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Laurent Granjon
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gauthier Dobigny
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Janice Britton-Davidian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frédéric Veyrunes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Veyrunes, F., Catalan, J., Sicard, B. et al. Autosome and Sex Chromosome Diversity Among the African Pygmy Mice, Subgenus Nannomys (Murinae; Mus). Chromosome Res 12, 369–382 (2004). https://doi.org/10.1023/B:CHRO.0000034098.09885.e6

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:CHRO.0000034098.09885.e6

Search

Navigation