Skip to main content
SpringerLink
Log in

Phylogenetic relationship and time of divergence of Mus terricolor with reference to other Mus species

  • RESEARCH ARTICLE
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Mitochondrial DNA control region of Mus terricolor, three aboriginal species M. spretus, M. macedonicus, M. spicilegus; the Asian lineage M. caroli, M. cervicolor, M. cookii; and the two house mice, M. musculus domesticus and M. m. castaneus were analysed to estimate the substitution rate, phylogenetic relationship and the probable time of divergence. Results showed that M. spretus, M. caroli and M. terricolor are highly diverged from each other (caroli/terricolor = 0.146, caroli/spretus = 0.147 and terricolor/spretus = 0.122), whereas M. spretus showed less divergence with two house mice species (0.070 and 0.071). Sequence divergence between M. terricolor and the Palearctic group were found to be ranging from 0.121 to 0.134. Phylogenetic analysis by minimum evolution, neighbour-joining, unweighed pair group method with arithmetic mean and maximum parsimony showed almost similar topology. Two major clusters were found, one included the Asian lineage, M. caroli, M. cookii and M. cervicolor and the other included the house mice M. m. domesticus, M. m. castaneus and the aboriginal mice M. macedonicus and M. spicilegus along with M. spretus, forming the Palearctic clade. M. terricolor was positioned between the Palearctic and Asian clades. Results showed that Palearctic-terricolor and the Asian lineages diverged 5.47 million years ago (Mya), while M. terricolor had split around 4.63 Mya from their ancestor. M. cervicolor, M. cookii and M. caroli diverged between 4.70 and 3.36 Mya, which indicates that M. terricolor and the Asian lineages evolved simultaneously. M. spretus is expected to have diverged nearly 2.9 Mya from their most recent common ancestor.

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • Auffray J.-C., Orth A., Catalan J., Gonzalez J.-P., Desmarias E. and Bonhomme F. 2003 Phylogenetic position and description of a new species of subgenus Mus (Rodentia, Mammalia) from Thailand. Zool. Scr. 32, 119–127.

    Article  Google Scholar 

  • Baker R. J., Haiduk M. W., Robbins L. W., Cadena A. and Koop B. F. 1982 Chromosomal studies of south American bats and their systematic implications. In Mammalian biology in south (ed. M. A. Mares and H. H. Genoways), pp. 303–327. Pymatuning Lab Ecol., University Pittsburgh, Pittsburgh.

  • Benton M. J. and Donoghue P. 2007 Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24, 26–53.

    Article  CAS  PubMed  Google Scholar 

  • Benveniste R. E., Callahan R., Sherr C. J., Chapman V. and Todaro G. J. 1977 Two distinct endogenous type C viruses isolated from the Asian rodent Mus cervicolor: conservation of virogene sequences in related rodent species. J. Virol. 21, 849–862.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bonhomme F., Martin S. and Thaler L. 1978 Hybridization between Mus musculus L. and Mus spretus Lataste under laboratory conditions. Experientia 34, 1140–1141.

    Article  CAS  PubMed  Google Scholar 

  • Bonhomme F., Catalan J., Guerassimov S., Orsini P. and Thaler L. 1983 Le complexe d’espèces du genre en Europe Centrale et Orientale. 1. Genetique. Z. Saugetierkd. 48, 78–85.

    Google Scholar 

  • Bonhomme F., Orth A., Cucchi T., Rajabi-Maham H., Catalan J., Boursot P. et al. 2011 Genetic differentiation of the house mouse around the Mediterranean basin: matrilineal footprints of early and late colonization. Proc. R. Soc. B 278, 1034–1043.

    Article  PubMed  Google Scholar 

  • Boursot P., Auffray J. C., Britton-Davidian J. and Bonhomme F. 1993 The evolution of house mice. Annu. Rev. Ecol. Evol. Syst. 24, 119–152.

    Article  Google Scholar 

  • Boursot P., Din W., Anand R., Darviche D., Dod B., Von-Deimling F. et al. 1996 Origin and radiation of the house mouse: mitochondrial DNA phylogeny. J. Evol. Biol. 9, 391–415.

    Article  CAS  Google Scholar 

  • Britten R. J. 1986 Rates of DNA sequence evolution differ between taxonomic groups. Science 231, 1393–l398.

    Article  CAS  PubMed  Google Scholar 

  • Brownell E. 1983 DNA/DNA hybridization studies of muroid rodents: symmetry and rates of molecular evolution. Evolution 37, 1034–1051.

    Article  CAS  Google Scholar 

  • Chatterjee B. and Rao G. R. 1984 A simple method for purification of mtDNA. Indian J. Biochem. Biophys. 21, 378–380.

    CAS  PubMed  Google Scholar 

  • Chatterjee B., Bahadur M. and Sharma T. 1994 Mitochondrial DNA restriction maps of Mus booduga, Mus terricolor and Mus musculus tytleri. J. Genet. 73, 57–64.

    Article  CAS  Google Scholar 

  • Chevret P., Veyrunes F. and Britton-Davidian J. 2005 Molecular phylogeny of the genus Mus (Rodentia: Murinae) based on mitochondrial and nuclear data. Biol. J. Linn. Soc. 84, 417–427.

    Article  Google Scholar 

  • Din W., Anand R., Boursot P., Darviche D., Dod B., Jouvin-Marche E. et al. 1996 Origin and radiation of the house mouse: clues from nuclear genes. J. Evol. Biol. 9, 519–539.

    Article  CAS  Google Scholar 

  • Felsenstein J. 1985 Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.

    Article  Google Scholar 

  • Flynn L. J., Jacobs L. L. and Lindsay E. H. 1985 Problems in muroid phylogeny: relationships to other rodents and origin of major groups. In Evolutionary relationships among rodents: a multidisciplinary analysis (ed. W. P. Luckett and J. L. Hartenberger), pp. 589–616. Plenum Press, New York, USA.

  • Fort P., Bonhomme F., Darlu P., Piechaczyk M., Jeanteur P. and Thaler L. 1985 Clonal divergence of mitochondrial DNA versus populational evolution of nuclear genome. Evol. Theor. 7, 81–90.

    Google Scholar 

  • Galewski T., Tilak M., Sanchez S., Chevret P., Paradis E. and Douzery E. 2006 The evolutionary radiation of Arvicoline rodents (voles and lemming): relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evol. Biol. 6, 80.

    Article  PubMed  PubMed Central  Google Scholar 

  • Geraldes A., Basset P., Gibson B., Smith K., Harr B., Yu H. T. et al. 2008 Inferring the history of speciation in house mice from autosomal, X-linked, Y-linked and mitochondrial genes. Mol. Ecol. 17, 5349–5363.

    Article  PubMed  PubMed Central  Google Scholar 

  • Guénet J. L. and Bonhomme F. 2003 Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet. 19, 24–31.

    Article  PubMed  Google Scholar 

  • Hasegawa M., Cao Y. and Yang Z. 1998 Preponderance of slightly deleterious polymorphism in mitochondrial DNA: nonsynonymous/synonymous rate ratio is much higher within species than between species. Mol. Biol. Evol. 15, 1499–1505.

    Article  CAS  PubMed  Google Scholar 

  • Huchon D., Catzeflis F. M. and Douzery E. J. P. 2000 Variance of molecular datings, evolution of rodents, and the phylogenetic affinities between Ctenodactylidae and Hystricognathi. Proc. R. Soc. Lon. B 267, 393–402.

    Article  CAS  Google Scholar 

  • Ingman M., Kaessmann H., Pabbo S. and Gyllensten U. 2000 Mitochondrial genome variation and the origin of modern humans. Nature 408, 708–713.

    Article  CAS  PubMed  Google Scholar 

  • Jacobs L. L. 1978 Fossil rodents (Rhyzomyidae and Muridae) from Neogene Siwalik deposits, Pakistan. Mus. Nort. Arizona Press Bull. Ser. 52, 1–103.

    Google Scholar 

  • Jacobs L. L. and Pilbeam D. 1980 Of mice and men: fossil based divergence dates and molecular “clocks”. J. Hum. Evol. 9, 551–555.

    Article  Google Scholar 

  • Jacobs L. L. and Downs W. R. 1994 The evolution of murine rodents in Asia. In Rodent and lagomorph families of Asian origin and diversification (ed. Y. Tomida, D. Li and T. Setoguchi), pp. 149–156. Monograph, National Science Museum, Tokyo.

  • Lee M. R. and Elder F. F. B. 1980 Yeast stimulation of bone marrow mitoses for cytogenetic investigations. Cytogenet. Cell Genet. 26, 36–40.

    Article  CAS  PubMed  Google Scholar 

  • Lundrigan B. L., Jansa S. A. and Tucker P. K. 2002 Phylogenetic relationships in the genus Mus, based on paternally, maternally, and biparentally inherited characters. Syst. Biol. 51, 410–431.

    Article  PubMed  Google Scholar 

  • Macholan M., Mrkvicova V. M., Bejcek V. and Stastny K. 2012 Mitochondrial DNA sequence variation and evolution of world house mice (Mus musculus). Folia Zool. 61, 284–307.

    Google Scholar 

  • Mahler K. L., Fleming J. L., Dworkin A. M., Gladman N., Cho H.-Y., Mao J.-H. et al. 2008 Sequence divergence of Mus spretus and Mus musculus across a skin cancer susceptibility locus. BMC Genomics 9, 626.

    Article  PubMed  PubMed Central  Google Scholar 

  • Manjunatha K. A. and Aswathanarayana N. V. 1979 Studies on chromosomes of the genus Mus: autosomal polymorphism in the Indian pygmy mouse Mus dunni (Wroughton). Curr. Sci. 48, 657–659.

    Google Scholar 

  • Markvong A., Marshall T., Pathak S. and Hsu T. C. 1975 Chromosomes and DNA of Mus: the karyotype of Mus flavidiventris and Mus dunni. Cytogenet. Cell Genet. 14, 116–125.

    Article  CAS  PubMed  Google Scholar 

  • Matthey R. and Petter F. 1968 Existence de deux especes distinctes, l’une chromosomiquement polymorphe chez der Mus indiens der groups booduga. Etude cytogenetique et taxonomique. Rev. Suisse Zool. 75, 461–498.

    CAS  Google Scholar 

  • Musser G. G. and Carleton M. D. 1993 Family Muridae. In Mammal species of the world: a taxonomic and geographic reference, 2nd edition (ed. D. E. Wilson and D. M. Reeder), pp. 501–756. Smithsonian Institution, Washington, USA.

  • Musser G. G. and Carleton M. D. 2005 Superfamily Muroidea. In Mammal species of the world a taxonomic and geographic reference (ed. D. E. Wilson and D. M. Reeder), pp. 894–1531. Johns Hopkins University Press, Baltimore, USA.

  • Nei M. and Kumar S. 2000 Molecular evolution and phylogenetics. Oxford University Press, New York, USA.

    Google Scholar 

  • Phifer-Rixey M., Bonhomme F., Boursot P., Churchill G. A., Pialek J., Tucker P. K. and Nachman M. W. 2012 Adaptive evolution and effective population size in wild house mice. Mol. Biol. Evol. 29, 2949–2955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prager E. M., Tichy M. H. and Sage R. D. 1996 Mitochondrial DNA sequence variation in the eastern house mouse, Mus musculus: comparison with other house mice and report of a 75-bp tandem repeat. Genetics 143, 427–446.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prager E. M., Orrego C. and Sage R. D. 1998 Genetic variation and phylogeography of central Asian and other house mice, including a major new mitochondrial lineage in Yemen. Genetics 150, 835–861.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rice N. R. 1971 Differences in the DNA of closely related rodents. Year B. Carnegie Inst. Wash. 70, 366–369.

    Google Scholar 

  • Rudra M. and Bahadur M. 2013 Heterochromatin variation among the populations of Mus terricolor Blyth, 1851 (Rodentia, Muridae) chromosome type I. Comp. Cytogen. 7, 139–151.

    Article  Google Scholar 

  • Rzhetsky A. and Nei M. 1992 A simple method for estimating and testing minimum evolution trees. Mol. Biol. Evol. 9, 945–967.

    CAS  Google Scholar 

  • Sage R. D. 1981 Wild mice. In The mouse in biomedical research, vol. 1. History, genetics and wild mice (ed. H. L. Foster, J. D. Small and J. G. Fox), pp. 39–90. Academic Press, New York, USA.

  • Sage R. D., Atchley W. R. and Capanna E. 1993 House mice as a model in systematic biology. Syst. Biol. 42, 523–561.

    Article  Google Scholar 

  • Saitou N. and Nei M. 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.

    CAS  PubMed  Google Scholar 

  • Sen S. and Sharma T. 1983 Role of constitutive heterochromatin in evolutionary divergence: results of chromosome banding and condensation inhibition studies in Mus musculus, Mus booduga and Mus dunni. Evolution 37, 628–636.

    Article  Google Scholar 

  • Sharma T. 1996 Chromosomal and molecular divergence in the Indian pygmy field mice Mus booduga–terricolor lineage of the subgenus Mus. Genetica 97, 331–338.

    Article  CAS  PubMed  Google Scholar 

  • Sharma T. and Garg G. S. 1975 Constitutive heterochromatin and karyotype variation in Indian pygmy mouse, Mus dunni. Genet. Res. 25, 189–191.

    Article  CAS  PubMed  Google Scholar 

  • Sharma T., Cheong N., Sen P. and Sen S. 1986 Constitutive heterochromatin and evolutionary divergence of Mus dunni, Mus booduga and Mus musculus. Curr. Top. Microbiol. Immunol. 127, 35–44.

    CAS  PubMed  Google Scholar 

  • Sharma T., Balajee A. S. and Cheong N. 1990 Chromosomal speciation: constitutive heterochromatin and evolutionary differentiation of the Indian pygmy field mice. In Trends in chromosome research (ed. T. Sharma), pp. 265–283. Springer-Verlag and Narosa Publishing House, New Delhi, India.

  • She J. X., Bonhomme F., Boursot P., Thaler L. and Catzeflis F. 1990 Molecular phylogenies in the genus Mus – comparative analysis of electrophoretic, scnDNA hybridization, and mtDNA RFLP data. Biol. J. Linn. Soc. 41, 83–103.

    Article  Google Scholar 

  • Smith M. F. and Patton J. L. 1999 Phylogenetic relationships and the radiation of sigmodontine rodents in south America: evidence from cytochrome b. J. Mamm. Evol. 6, 89–128.

    Article  Google Scholar 

  • Sneath P. H. A. and Sokal R. R. 1973 Numerical taxonomy. Freeman, San Francisco, USA.

    Google Scholar 

  • Spradling T., Hafner M. and Demastes J. 2001 Differences in rate of cytochrome-b evolution among species of rodents. J. Mammal 82, 65–80.

    Article  Google Scholar 

  • Stoneking M., Sherry S. T., Redd A. J. and Vigilant L. 1992 New approaches to dating suggest a recent age for the human mtDNA ancestor. Phil. Trans. R. Soc. Lon. B 337, 167–175.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H., Shimada T., Terashima M., Tsuchiya K. and Aplin K. 2004 Temporal, spatial, and ecological modes of evolution of Eurasian Mus based on mitochondrial and nuclear gene sequences. Mol. Phylogenet. Evol. 33, 626–646.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H., Nunome M., Inoshita G., Aplin K. P., Vogel P., Kryukov A. P. et al. 2013 Evolutionary and dispersal history of Eurasian house mice Mus musculus clarified by more extensive geographic sampling of mitochondrial DNA. Heredity 111, 375–390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F. 1993 Simple methods for testing molecular clock hypothesis. Genetics 135, 599–607.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K. and Nei M. 1993 Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526.

    CAS  PubMed  Google Scholar 

  • Tamura K., Nei M. and Kumar S. 2004 Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc. Natl. Acad. Sci. USA 101, 11030–11035.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K., Dudley J., Nei M. and Kumar S. 2007 MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.

    Article  CAS  PubMed  Google Scholar 

  • Tamura K., Peterson D., Peterson N., Stecher G., Nei M. and Kumar S. 2011 MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson J. D., Higgins D. G. and Gibson T. J. 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alighnment through sequence weighing, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker P. K. 2007 Systematics of the genus Mus. In The mouse in Biomedical Research, 2nd edition (ed. J. G Fox, S. W. Barthold, M. T. Davisson, C. E. Newcomer, F. W. Quimby and A. L. Smith), pp. 13–23. American College of Laboratory, Animal Medicine Series, Elsevier Press, Boston.

  • Tucker P. K., Lee B. K. and Eicher E. M. 1989 Y chromosome evolution in the subgenus Mus (genus Mus). Genetics 122, 169–179.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker P. K., Sandstedt S. and Lundrigan B. L. 2005 Phylogenetic relationships in the genus Mus: examining gene trees and species trees. Biol. J. Linn. Soc. 84, 653–662.

    Article  Google Scholar 

  • Wu C.-I. and Li W. H. 1985 Evidence for higher rates of nucleotide substitution in rodents than in man. Proc. Natl. Acad. Sci. USA 2, 1741–1745.

    Article  Google Scholar 

  • Yonekawa H., Moriwaki K., Gotoh O., Hayashi J.-I., Watanabe J., Miyashita N. et al. 1981 Evolutionary relationships among five subspecies of Mus musculus based on restriction enzyme cleavage patterns of mitochondrial DNA. Genetics 98, 801–816.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yonekawa H., Sato J. J., Suzuki H. and Moriwaki K. 2012 Origin and genetic status of Mus musculus molossinus: a typical example of reticulate evolution in the genus Mus. In Evolution of the house mouse. Cambridge studies in morphology and molecules: new paradigms in evolutionary biology (ed. M. Macholán, S. J. E. Baird, P. Munclinger and L. Piálek), pp. 94–113. Cambridge University Press, Cambridge , UK.

Download references

Acknowledgements

The financial support received from the University of North Bengal, Rajarammohunpur, Siliguri 734013, West Bengal, India, routed through the Department of Zoology is sincerely acknowledged. The DNA of M. caroli and M. spretus received from the Jackson Laboratory is gratefully acknowledged. The authors gratefully acknowledge Prof Ananda Mukhopadhyay, Department of Zoology, University of North Bengal for editing the manuscript with valuable suggestions on language.

Author information

Authors and Affiliations

  1. Genetics and Molecular Biology Laboratory, Department of Zoology, University of North Bengal, Siliguri, 734 013, India

    MAHUA RUDRA & MIN BAHADUR

  2. Laboratory of Developmental Biology, National Heart Lung and Blood Institute, National Institutes of Health, Bethesda, MD, 20892, USA

    BISHWANATH CHATTERJEE

Authors
  1. MAHUA RUDRA
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. BISHWANATH CHATTERJEE
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. MIN BAHADUR
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to MIN BAHADUR.

Additional information

[Rudra M., Chatterjee B. and Bahadur M. 2016 Phylogenetic relationship and time of divergence of Mus terricolor with reference to other Mus species. J. Genet. 95, xx–xx]

Electronic supplementary material

Below is the link to the electronic supplementary material.

(PDF 2.40 MB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

RUDRA, M., CHATTERJEE, B. & BAHADUR, M. Phylogenetic relationship and time of divergence of Mus terricolor with reference to other Mus species. J Genet 95, 399–409 (2016). https://doi.org/10.1007/s12041-016-0654-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12041-016-0654-x

Keywords

Search

Navigation