Skip to main content
Log in

Karyotype evolution and phylogenetic relationships of hamsters (Cricetidae, Muroidea, Rodentia) inferred from chromosomal painting and banding comparison

  • Published:
Chromosome Research Aims and scope Submit manuscript

Abstract

The evolutionary success of rodents of the superfamily Muroidea makes this taxon the most interesting for evolution studies, including study at the chromosomal level. Chromosome-specific painting probes from the Chinese hamster and the Syrian (golden) hamster were used to delimit homologous chromosomal segments among 15 hamster species from eight genera: Allocricetulus, Calomyscus, Cricetulus, Cricetus, Mesocricetus, Peromyscus, Phodopus and Tscherskia (Cricetidae, Muroidea, Rodentia). Based on results of chromosome painting and G-banding, comparative maps between 20 rodent species have been established. The integrated maps demonstrate a high level of karyotype conservation among species in the Cricetus group (Cricetus, Cricetulus, Allocricetulus) with Tscherskia as its sister group. Species within the genera Mesocricetus and Phodopus also show a high degree of chromosomal conservation. Our results substantiate many of the conclusions suggested by other data and strengthen the topology of the Muroidea phylogenetic tree through the inclusion of genome-wide chromosome rearrangements. The derivation of the muroids karyotypes from the putative ancestral state involved centric fusions, fissions, addition of heterochromatic arms and a great number of inversions. Our results provide further insights into the karyotype relationships of all species investigated.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adkins RM, Walton AH, Honeycutt RL (2002) Higher-level systematics of rodents and divergence time estimates based on two congruent nuclear genes. Mol Phylogenet Evol 26: 409–420.

    Article  Google Scholar 

  • Aniskin VM, Benazzou T, Biltueva L, Dobigny G, Granjon L, Volobouev V (2006) Unusually extensive karyotype reorganization in four congeneric Gerbillus species (Muridae: Gerbillinae). Cytogenet Genome Res 112: 131–140.

    Article  PubMed  CAS  Google Scholar 

  • Carleton MD, Musser GG (2005) Order Rodentia. In Wilson E, Reeder D-AM, eds., Mammal Species of the World: a Taxonomic and Geographic Reference. Baltimore: Johns Hopkins University Press, pp. 926–930, 1039–1186.

    Google Scholar 

  • Cavagna P, Stone G, Stanyon R (2002) Black rat (Rattus rattus) genomic variability characterized by chromosome painting. Mamm Genome 13: 157–163.

    PubMed  CAS  Google Scholar 

  • Dobigny G, Ducroz JF, Robinson TJ, Volobouev V (2004) Cytogenetics and cladistics. Syst Biol 53: 470–484.

    Article  PubMed  Google Scholar 

  • Engelbrecht A, Dobigny G, Robinson TJ (2006) Further insights into the ancestral murine karyotype: the contribution of the Otomys–Mus comparison using chromosome painting. Cytogenet Genome Res 112: 126–130.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Froenicke L, Caldes MG, Graphodatsky A et al. (2006) Are molecular cytogenetics and bioinformatics suggesting diverging models of ancestral mammalian genomes? Genome Res 16: 306–310.

    Article  PubMed  CAS  Google Scholar 

  • Gamperl R, Vistorin G, Rosenkranz W (1978) Comparison of chromosome banding patterns in five members of Cricetinae with comments on possible relationships. Caryologia 31: 343–353.

    Google Scholar 

  • Graphodatsky AS (1989) Conserved and variable elements of mammalian chromosomes. In Halnan CRE, ed., Cytogenetics of Animals. Oxford: CAB International Press, pp. 95–123.

    Google Scholar 

  • Graphodatsky AS, Sablina OV, Meyer MN et al. (2000) Comparative cytogenetics of hamsters of the genus Calomyscus. Cytogenet Cell Genet 88: 296–304.

    Article  PubMed  CAS  Google Scholar 

  • Graphodatsky AS, Yang F, O’Brien PCM et al. (2001) Phylogenetic implications of the 38 putative ancestral chromosome segments for four canid species. Cytogenet Cell Genet 92: 243–247.

    Article  PubMed  CAS  Google Scholar 

  • Guilly M-N, Dano L, de Chamisso P, Fouchet P, Dutrillaux B, Chevillard S (2001) Comparative karyotype using bidirectional chromosome painting: how and why? Methods Cell Sci 23: 163–170.

    Article  PubMed  CAS  Google Scholar 

  • Guilly M-N, Fouchet P, de Chamisso P, Schmitz A, Dutrillaux B (1999) Comparative karyotype of rat and mouse using bidirectional chromosome painting. Chromosome Res 7: 213–221.

    Article  PubMed  CAS  Google Scholar 

  • Jansa SA, Weksler M (2004) Phylogeny of muroid rodents: relationships within and among major lineages as determined by IRBP gene sequences. Mol Phylogenet Evol 31: 256–276.

    Article  PubMed  CAS  Google Scholar 

  • Li T, O’Brien PC, Biltueva L et al. (2004) Evolution of genome organizations of squirrels (Sciuridae) revealed by cross-species chromosome painting. Chromosome Res 12: 317–335.

    Article  PubMed  Google Scholar 

  • Li T, Wang J, Su W, Nie W, Yang F (2006a) Karyotypic evolution of the family Sciuridae: inferences from the genome organizations of ground squirrels. Cytogenet Genome Res 112: 270–276.

    Article  PubMed  CAS  Google Scholar 

  • Li T, Wang J, Su W, Yang F (2006b) Chromosomal mechanisms underlying the karyotype evolution of the oriental voles (Muridae, Eothenomys). Cytogenet Genome Res 114: 50–55.

    Article  PubMed  CAS  Google Scholar 

  • Matsubara K, Nishuda-Umehara C, Tsuchiya K, Nukaya D, Matsuda Y (2004) Karyotypic evolution of Apodemus (Muridae, Rodentia) inferred from comparative FISH analyses. Chromosome Res 12: 383–395.

    Article  PubMed  CAS  Google Scholar 

  • Matsubara K, Nishida-Umehara C, Kuriowa A, Tsuchiya K, Matsuda Y (2003) Identification of chromosome rearrangements between the laboratory mouse (Mus musculus) and the Indian spiny mouse (Mus platythrix) by comparative FISH analysis. Chromosome Res 11: 57–64.

    Article  PubMed  CAS  Google Scholar 

  • Michaux J, Reyes A, Catzeftis F (2001) Evolutionary history of the most specious mammals: molecular phylogeny of muroid rodents. Mol Biol Evol 18: 2017–2031.

    PubMed  CAS  Google Scholar 

  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O’Brien SJ (2001a) Molecular phylogenetics and the origins of placental mammals. Nature 409: 614–618.

    Article  PubMed  CAS  Google Scholar 

  • Murphy WJ, Larkin DM, Everts-van der Wind A et al. (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309: 613–617.

    Article  PubMed  CAS  Google Scholar 

  • Murphy WJ, Stanyon, O’Brien SJ (2001b) Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biol 2: 1–8.

    Article  Google Scholar 

  • Neumann K, Michaux J, Lebedev V et al. (2006) Molecular phylogeny of the Cricetinae subfamily based on the mitochondrial cytochrome b and 12S rRNA genes and the nuclear vWF gene. Mol Phylogenet Evol 39: 135–148.

    Article  PubMed  CAS  Google Scholar 

  • Radjabli SI (1975) The karyotypic differentiation of Palaearctic hamsters (Rodentia, Cricetidae). Reports of AS of USSR 225: 697–700.

    Google Scholar 

  • Radjabli SI, Sablina OV, Graphodatsky AS (2006) Selected karyotypes. In O’Brien SJ, Nash WG, Menninger JC, eds., ATLAS of Mammalian Karyotypes. Chichester: John Wiley, pp. 188, 200–221.

    Google Scholar 

  • Rambau RV, Robinson TJ (2003) Chromosome painting in the African four-striped mouse Rhabdomys pumilio: detection of possible murid specific contiguous segment combination. Chromosome Res 11: 91–98.

    Article  PubMed  CAS  Google Scholar 

  • Richard F, Messaoudi C, Bonnet-Gamier A, Lombard M, Dutrillaux B (2003) Highly conserved chromosomes in an Asian squirrel (Menetes berdmorei, Rodentia: Sciuridae) as demonstrated by ZOO-FISH with human probes. Chromosome Res 11: 597–603.

    Article  PubMed  CAS  Google Scholar 

  • Romanenko SA, Perelman PL, Serdukova NA et al. (2006) Reciprocal chromosome painting between three laboratory rodent species. Mamm Genome 17: 1183–1192.

    Article  PubMed  Google Scholar 

  • Schmid M, Haaf T, Weis H, Schempp W (1986) Chromosomal homoeologies in hamster species of the genus Phodopus (Rodentia, Cricetinae). Cytogenet Cell Genet 43: 168–173.

    PubMed  CAS  Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet 2: 971–972.

    Article  PubMed  CAS  Google Scholar 

  • Stanyon R, Stone G, Garcia M, Froenicke L (2003) Reciprocal chromosome painting shows that squirrels, unlike murid rodents, have a highly conserved genome organization. Genomics 82: 245–249.

    Article  PubMed  CAS  Google Scholar 

  • Stanyon R, Yang F, Cavagna P et al. (1999) Reciprocal chromosome painting shows that genomic rearrangement between rat and mouse proceeds ten times faster than between humans and cats. Cytogenet Cell Genet 84: 150–155.

    Article  PubMed  CAS  Google Scholar 

  • Stanyon R, Yang F, Morescalchi AM, Galleni L (2004) Chromosome painting in the long-tailed field mouse provides insights into the ancestral murid karyotype. Cytogenet Genome Res 105: 406–411.

    Article  PubMed  CAS  Google Scholar 

  • Steppan SJ, Adkins RM, Anderson J (2004) Phylogeny and divergence-data estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst Biol 53: 533–553.

    Article  PubMed  Google Scholar 

  • Swofford DL (1998) PAUP: Phylogenetic Analysis Using Parcimony, version 4.0. Sinauer Associates, Sunderland, MA.

  • Veyrunes F, Dobigny G, Yang F et al. (2006) Phylogenomics of the genus Mus (Rodentia; Muridae): extensive genome repatterning is not restricted to the house mouse. Proc R Soc B 273: 2925–2934.

    Article  PubMed  Google Scholar 

  • Viegas-Pequignot E, Petit D, Benazzou T et al. (1986) Chromosomal evolution in rodents. Mammalia 50: 164–202.

    Google Scholar 

  • Volobouev VT, Gallardo MH, Graphodatsky AS (2006) Rodents cytogenetics. In O’Brien J, Nash WG, Menninger JC, eds., ATLAS of Mammalian Karyotypes. Chichester: John Wiley, pp. 173–176.

    Google Scholar 

  • Vorontzov NN, Potapova EG (1979) Taxonomy of the genus Calomyscus: status of the Calomyscus in the system of Cricetidae. Zool J 58: 1391–1397 [Rusian].

    Google Scholar 

  • Yang F, Fu B, O’Brien PC, Robinson TJ, Ryder OA, Ferguson-Smith MA (2003) Karyotypic relationships of horses and zebras: results of cross-species chromosome painting. Cytogenet Genome Res 102: 235–243.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, O’Brien PC, Milne BS (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62: 189–202.

    Article  PubMed  CAS  Google Scholar 

  • Yang F, O’Brien PCM, Ferguson-Smith MA (2000) Comparative chromosome map of the laboratory mouse and Chinese hamster defined by reciprocal chromosome painting. Chromosome Res 8: 219–227.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander S. Graphodatsky.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Romanenko, S.A., Volobouev, V.T., Perelman, P.L. et al. Karyotype evolution and phylogenetic relationships of hamsters (Cricetidae, Muroidea, Rodentia) inferred from chromosomal painting and banding comparison. Chromosome Res 15, 283–298 (2007). https://doi.org/10.1007/s10577-007-1124-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10577-007-1124-3

Key words

Navigation