Skip to main content
Log in

Increased geographic sampling reveals considerable new genetic diversity in the morphologically conservative African Pygmy Mice (Genus Mus; Subgenus Nannomys)

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

African endemic pygmy mice (Genus Mus; sub-genus Nannomys) have considerable economic and public health significance, and some species exhibit novel sex determination systems, making accurate knowledge of their phylogenetics and distribution limits important. This phylogenetic study was based on the mitochondrial control region and cytochrome b gene, for which a substantial body of published data was available. Study specimens were sourced from eight previously unsampled or poorly sampled countries, and include samples morphologically identified as Mus bufo, M. indutus, M. callewaerti, M. triton and M. neavei. These analyses increase the known genetic diversity of Nannomys from 65 to 102 haplotypes; at least 5 unassigned haplotypes are distinguished by potentially species-level cytochrome b genetic distances. The monophyly of Nannomys is supported. Mus musculoides, M. callewaerti, M. indutus, M. bufo, M. haussa, M. mattheyi, M. baoulei and M. sorella are supported as discrete species. The range of M. indutus is extended to include Botswana. M. setulosus and M. minutoides appear to be species complexes. A south and east African M. minutoides clade was defined and includes 8 new haplotypes out of 15. M. setulosus sensu lato includes M. setulosus sensu stricto and a strongly-supported M. bufo clade. Two samples, morphologically identified as M. triton and M. neavei, fall within the M. minutoides clade.

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

  • Aniskine, V.M., Lavrenchenko, LA., Milishnikov, A.N., Warshavsky, A.A., 1998. Karyotypes of small mammals (Insectivora, Rodentia) of the Bale mountains, Ethiopia. In: Sokolov, V.E., Rozhnov, V.V., Serbenyuk, M.A. (Eds.), Behaviour, Communication and Ecology of Mammals. Inst. Ecol. Evol. RAS, Moscow, pp. 217–236.

    Google Scholar 

  • Baker, R.J., Bradley, R.D., 2006. Speciation in mammals and the genetic species concept. J. Mammal. 87 (4), 643–662.

    Article  PubMed  Google Scholar 

  • Benton, M.J., Donoghue, P.C., 2007. Paleontological evidence to date the tree of life. Mol. Biol. Evol. 24 (3), 889–891.

    CAS  Google Scholar 

  • Britton-Davidian, J., Robinson, T.J., Veyrunes, F., 2012. Systematics and evolution of the African pygmy mice, subgenus Nannomys: a review. Acta Oecol. 42, 41–49.

    Article  Google Scholar 

  • Bronner, G.N., Hoffmann, M., Taylor, P.J., Chimimba, C.T., Best, P.B., Matthee, C.A., Robinson, T.J., 2003 November. A revised systematic checklist of the extant mammals of the southern African subregion. Durban Mus. 28, 56–106.

    Google Scholar 

  • Castiglia, R., Gornung, E., Corti, M., 2002. Cytogenetic analyses of chromosomal rear¬rangements in Mus minutoides/musculoides from North-West Zambia through mapping of the telomeric sequence (TTAGGG) and banding techniques. Chromosome Res. 10 (5), 399–406.

    Article  CAS  PubMed  Google Scholar 

  • Chevret, P., Veyrunes, F., Britton-Davidian, J., 2005. Molecular phylogenyof the genus Mus Rodentia: Murinae) based on mitochondrial and nuclear data. In: Britton-Davidian, J., Searle, J.B. (Eds.), The Genus Mus as a Model for Evolutionary Studies, 84. Biol. J. Linn. Soc, pp. 417–427.

    Google Scholar 

  • Chimimba, C.T., Bennett, N., 2005. Order: Rodentia. In: Skinner, J.D., Chimimba, C.T. (Eds.), The Mammals of the Southern African Subregion., 3rd ed. Cambridge University Press, pp. 77–209.

  • Cotterill, F.P.D., de Wit, M.J., 2011. Geoecodynamics and the kalahari epeirogeny: linking its genomic record, tree of life and palimpsest into a unified narrative of landscape evolution. S. Afr. J. Geol. 114, 489–514.

    Article  CAS  Google Scholar 

  • Crawford-Cabral, J., 1998. The Angolan rodents of the superfamily Muroidea: an account of their distribution. Instituto de InvestigaçãoCientífica Tropical, Estudos, Ensaios e Documentos, 161, 223. In: Musser, G.G., Carleton, M.D., Wilson, D.E., Reeder, D.M. (Eds.), Superfamily Muroidea 2005. Mammal Species of the WorldaTaxonomic and Geographic Referenc, 3rd ed. Johns Hopkins University Press, Baltimore, pp. 894–1531.

    Google Scholar 

  • de Graaff, G., 1997. Order rodentia. In: Mills, G., Hes, L. (Eds.), The Complete Book of Southern African Mammals. Struik Winchester, Capetown, pp. 120–164.

    Google Scholar 

  • Dieterlen, F., Agwanda, B., 2008. Mus triton In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.1 (downloaded on 24th May 2010) www.iucnredlist.org

  • Drummond, A.J., Rambaut, A., 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Happold, D.C.D., 2013. Mus callewaerti Callewart’s pygmy mouse. In: Hpaaold, D.C.D. (Ed.), Mammals of Africa, II. Bloomsbury Publishing, London, pp. 478–479.

    Google Scholar 

  • Happold, D.C.D., Veyrunes, F., 2013. Genus Mus Old World mice and pygmy mice. In: Happold, D.C.D. (Ed.), Mammals of Africa, II. Bloomsbury Publishing, London, pp. 473–476.

    Google Scholar 

  • Honeycutt, R.L., Frabotta, L.J., Rowe, D.L., 2007. Rodent evolution, phylogenetics and biogeography. In: Wolff, J.O., Sherman, P.W. (Eds.), Rodent Societies: An Ecological & Evolutionary Perspective. The University of Chicago Press, London, pp. 8–23.

    Google Scholar 

  • Huson, D.H., 1998. SplitsTree: a program for analyzing and visualizing evolutionary data. Bioinformatics 14, 68–73.

    Article  CAS  PubMed  Google Scholar 

  • Jansa, S.A., Barker, F.K., Heaney, L.R., 2006. The pattern and timing of diversification of Philippine endemic rodents: evidence from mitochondrial and nuclear gene sequences. Syst. Biol. 55 (1), 73–88.

    Article  PubMed  Google Scholar 

  • Jotterand-Bellomo, M., 1988. Chromosome analysis of five specimens of Mus bufotriton (Muridae) from Burundi (Africa): three cytogenetic entities, a special type of chromosomal sex determination, taxonomy, and phylogeny. Cytogenet. Cell Genet. 48 (88), e91.

    Google Scholar 

  • Kan Kouassi, S.K., Nicolas, V., Aniskine, V., Lalis, A., Cruaud, C, Couloux, A., Colyn, M., Dosso, M., Koivogui, L., Verheyen, E., Akoua, C, 2008. Taxonomy and biogeography of the African Pygmy mice, Subgenus Nannomys (Rodentia, Murinae Mus) in Ivory Coast and Guinea (West Africa). Mammalia 72, 237–252.

    Google Scholar 

  • Lamb, J.M., Ralph, T.M.C., Naidoo, T., Taylor, P., Ratrimonanarivo, F., Stanley, W., Goodman, S.M., 2011. Towards a molecular phylogeny for the Molossidae (Chiroptera) of the Afro-Malagasy region. Acta Chiropterol. 13 (1), 1–16.

    Article  Google Scholar 

  • Lecompte, E., terMeulen, J., Emonet, S., Daffis, S., Charrel, R.N., 2007. Genetic identifications of Kodoko virus, a novel arenavirus of the African pygmy mouse (Mus Nannomys minutoides) in West Africa. Virology 364, 178–183.

    Article  CAS  PubMed  Google Scholar 

  • Lecompte, E., Aplin, K., Denys, C, Catzeflis, F., Chades, M., Chevret, P., 2008a. Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily. BMC Evol. Biol. 8, 199.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lecompte, E., Denys, C, Granjon, L., 2008b. Confrontation of morphological and molecular data: the Praomys group (Rodentia Murinae) as a case of adaptive convergences and morphological status. Mol. Phylogenet. Evol. 37, 899–919.

    Article  CAS  Google Scholar 

  • Mboumba, J.F., Deleporte, P., Colyn, M., Nicolas, V., 2011. Phylogeography of Mus (Nannomys) minutoides (Rodentia, Muridae) in West Central African savannahs: singular vicariance in neighbouring populations.J. Zool. Syst. Evol. Res. 49 (1), 77–85.

    Article  Google Scholar 

  • Meester, J., Rautenbach, I.L., Dippenaar, N.J., Baker, CM., 1986. Classification of southern African mammals. Transvaal Museum Monograph. 5, 1–359.

    Google Scholar 

  • Michaux, J., Catzeflis, F., 2000. The bushlike radiation of muroid rodents is exemplified by the molecular phylogeny of the LCAT nuclear gene. Mol. Phylogenet. Evol. 17 (2), 280–293.

    Article  CAS  PubMed  Google Scholar 

  • Michaux, J.R., Libois, R., Filippucci, M.G., 2005. So close and so different: comparative phylogeography of two small mammal species, the Yellownecked field mouse (Apodemus flavicollis) and the Woodmouse(Apodemus sylvaticus), in the Western Palearctic region. Heredity 94, 52–63.

    Article  CAS  PubMed  Google Scholar 

  • Monadjem, A., 2008. Mus minutoides. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.1 (downloaded on 25th May 2010) www.iucnredlist.org

  • Musser, G.G., Carleton, M.D., 1993. Family Muridae. In: Wilson, D.N., Reeder, D.M. (Eds.), Mammal Species of the World: ATaxonomic and Geographical Reference. , 2nd ed. Smithsonian Institution, Washington, DC.

    Google Scholar 

  • Musser, G.G., Carleton, M.D., 2005. Superfamily Muroidea. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species ofthe World aTaxonomic and Geographic Reference. , 3rd ed. Johns Hopkins University Press, Baltimore, pp. 894–1531.

    Google Scholar 

  • Petter, F., Matthey, R., 1975. Genus Mus Part 6.7. In: Meester, J., Setzer, H.W. (Eds.), The Mammals of Africa: An Identification Manual. Smithsonian Institution Press, Washington, DC, pp. 1–4.

    Google Scholar 

  • Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C, Sundberg, P., Thollesson, M., 2008. Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol. Phylogenet. Evol. 48, 369–371.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D., 2008. jModelTest : phylogenetic model averaging. Mol. Phylogenet. Evol. 25, 1253–1256.

    Article  CAS  Google Scholar 

  • Rambaut, A., 2009. FigTree, ver. 1.3.1 [Online] 5th January 2013, http://tree.bio.ed.ac.uk/software/figtree/

  • Robbins, L.W., Baker, R.J., 1978. Karyotypic data for African mammals, with a description of an in vivo bone marrow technique. Bull. Carnegie Mus. Nat. Hist. 6, 188–210.

    Google Scholar 

  • Rozas, J., Sanchez-Del Barrio, J.C., Messeguer, X., Rozas, R., 2003. DnaSP, DNA, polymorphism, analysis by the coalescent and other methods. Bioinformatics 19, 2496–2497.

    Article  CAS  PubMed  Google Scholar 

  • Skinner, J.D., Chimimba, C.T., 2005. The Mammals of the Southern African Subregion, 3rd ed. Cambridge University Press.

  • Skinner, J.D., Smithers, R.H.N., 1990. The Mammals of the Southern African Subregion. University of Pretoria Press, Pretoria.

    Google Scholar 

  • Swofford, D.L., 2000. PAUP*: phylogenetic analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Inc. Publishers, Sunderland, Massachusetts.

    Google Scholar 

  • Taylor, P.J., Maree, S., van Sandwyk, J., Kerbis Peterhans, J.C., Stanley, W.T., Verheyen, E., Kaliba, P., Verheyen, W., Kaleme, P., Bennett, N.C., 2009. Speciation mirrors geomorphology and palaeoclimatic history in African laminate-toothed rats (Muridae: Otomyini) of the Otomys denti and O. lacustris species-complexes in the “Montane Circle” of East Africa. Biol. J. Linn. Soc. 96, 913–941.

    Google Scholar 

  • Taylor, P.J., Lavrenchenko, L.A., Carleton, M.D., Verheyen, E., Bennett, N., Oosthuisen, C, Maree, S., 2011. Specific limits and emerging diversity patterns in east African populations of laminate-toothed rats, genus Otomys (Muridae: Murinae: Otomyini) : revision of the Otomys typus complex. Zootaxa 3024, 1–66.

    Article  Google Scholar 

  • Taylor, P.J., Stoffberg, S., Monadjem, A., Schoeman, M.C., Bayliss, J., Cotterill, F.P.D., 2012. Four new bat species (Rhinolophus hildebrandtii complex) reflect Plio-Pleistocene divergence of dwarfs and giants across an Afromontane Archipelago. PLoS ONE 7 (9), e41744, https://doi.org/10.1371/journal.pone.0041744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veyrunes, F., Catalan, J., Sicard, B., Robinson, T.J., Duplantier, J.M., Granjon, L., Dobigny, G., 2004. Autosome and sex chromosome diversity among the African pygmy mice, subgenus Nannomys (Murinae; Mus). Chromosome Res. 12 (4), 369–382.

    Article  CAS  PubMed  Google Scholar 

  • Veyrunes, F., Britton-Davidian, J., Robinson, T.J., Calvet, E., Denys, C, Chevret, P., 2005. Molecular phylogeny ofthe African pygmy mice, subgenus Nannomys (Rodentia Murinae, Mus): implications for chromosomal evolution. Mol. Phylogenet. Evol. 36 (2), 358–369.

    Article  CAS  PubMed  Google Scholar 

  • Veyrunes, F., Chevret, P., Catalan, J., Castiglia, R., Watson, J., Dobigny, G., Robinson, T.J., Britton-Davidian, J., 2010a. A novel sex determination system in a close relative ofthe house mouse. Proc. R. Soc. B 277 (1049), e1056.

    Google Scholar 

  • Veyrunes, F., Catalan, J., Tatard, C, Cellier-Holzem, E., Watson, J., Chevret, P., Robinson, T.J., 2010b. Mitochondrial and chromosomal insights into karyotypic evolution of the pygmy mouse Mus minutoides, in South Africa. Chromosome Res. 18 (5), 563–574.

    Article  CAS  PubMed  Google Scholar 

  • Winkler, A.J., 2002. Neogene paleobiogeography and East African paleoenvironments: contributions from the Tungen Hills rodents and lagomorphs. J. Human Evol. 42 (1/2), 237–256.

    Article  Google Scholar 

  • Zachos, F.E., Appolonio, M., Bärmann, E., Festa-Bianchet, M., Gölich, U., Habel, J.C., Haring, E., Krukenhauser, L., Lovari, S., McDevitt, A.D., Pertoldi, C, Rössner, G.E., Sánchez-Villagra, M., Scandura, M., Suchentrunk, F., 2013. Species inflation and taxonomic artefacts – a critical comment on recent trends in mammalian classification. Mamm. Biol. 78, 1–6.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jennifer Lamb.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lamb, J., Downs, S., Eiseb, S. et al. Increased geographic sampling reveals considerable new genetic diversity in the morphologically conservative African Pygmy Mice (Genus Mus; Subgenus Nannomys). Mamm Biol 79, 24–35 (2014). https://doi.org/10.1016/j.mambio.2013.08.010

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2013.08.010

Keywords

Navigation