Skip to main content
Log in

Revision of the Mouse Lemurs (Microcebus) of Eastern Madagascar

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Phylogenetic analysis of ca. 4500 base pairs of mitochondrial DNA sequence data reveals further genetic diversity in mouse lemurs (Microcebus) on the eastern and western coasts of Madagascar. Molecular data and phylogenetic analyses revise the previously monotypic species of eastern Madagascar, Microcebus rufus, with the description of 3 new species. Three additional Microcebus species are proposed in eastern Madagascar, along with another Microcebus species in western Madagascar. Correlating the molecular data with previously generated sequence data, we present a tentative pattern of distribution along the east coast. We show that the general distribution of Microcebus is based on a traditional eastern/western division. The preliminary model appears strongly influenced by both rivers and altitudinal differences acting independently as barriers.

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.

Fig. 1.
Fig. 1(C).
Fig. 2.
Fig. 2 (B).
Fig. 3.
Fig. 3 (B).
Fig. 4.
Fig. 5.
Fig. 6 (A).
Fig. 6 (B).
Fig. 6 (C).
Fig. 6 (D).
Fig. 7.

Similar content being viewed by others

REFERENCES

  • Adkins, R. M., and Honeycutt, R. L. (1994). Evolution of the primate cytochrome c oxidase subunit II gene. J. Mol. Evol. 38: 215–231.

    Article  PubMed  CAS  Google Scholar 

  • Amato, G., Gatesy, J., and Brazaitis, P. (1998). PCR assays of variable nucleotide sites for identification of conservation units. In DeSalle, R., and Schierwater, B. (eds.), Molecular Approaches to Ecology and Evolution: An Example from Caiman, Birkhauser, Basel, pp. 177–190.

    Google Scholar 

  • Baker, C. S., Perry, A., Bannister, J. L., Weinrich, M. T., Abernethy, R. B., Calambokidis, J., Lien, R. H., Lambersen, J. U., Ramirez, O., Vasquez, P. Clapham, J., Alling, A., O’Brien, S. J., and Palumbi, S. R. (1993). Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc. Natl. Acad. Sci. USA 90: 8239–8243.

    Article  PubMed  CAS  Google Scholar 

  • Barrowclough, G. F., and Flesness, N. R. (1996). Species, subspecies, and races: The problem of units of management in conservation. In Kleiman, G. G., Allen, M., and Harris, H. (eds.), Wild Mammals in Captivity, The University of Chicago Press, Chicago, pp. 247–254.

    Google Scholar 

  • Cracraft, J. (1983). Species concepts and speciation analysis. In Johnston, R. F. (ed.), Current Ornithology, Vol. 1, Plenum Press, New York, pp. 159–187.

    Google Scholar 

  • Davis, J. I., and Nixon, K. C. (1992). Populations, genetic variation, and the delimitation of phylogenetic species. Syst. Biol. 41: 421–435.

    Article  Google Scholar 

  • Ganzhorn, J. U. (1998). Nested patterns of species composition and their implications for lemur biogeography in Madagascar. Folia Primatol. 69: 332–341.

    Article  Google Scholar 

  • Groves, C. P. (2000). The genus Cheirogaleus: Unrecognized biodiversity in dwarf lemurs. Int. J. Primatol. 21: 943–961.

    Article  Google Scholar 

  • Groves, C. P. (2001). Primate Taxonomy, Smithsonian Institution, Washington, DC, pp. 26–53; 68–70.

    Google Scholar 

  • Hasegawa, M., Kishino, H., and Yano, T.-A. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22: 160–174.

    Article  PubMed  CAS  Google Scholar 

  • Hedges, S. B. (1994). Molecular evidence for the origin of birds. Proc. Natl. Acad. Sci. USA 91: 2621–2624.

    Article  PubMed  CAS  Google Scholar 

  • Hey, J. (2001). The mind of the species problem. TRENDS Ecol. Evol. 16: 326–329.

    Article  PubMed  Google Scholar 

  • IUCN Conservation Monitoring Unit. (1984). In Jenkins, M. (ed.), An Environmental Profile of Madagascar, IUCN, Cambridge, UK, pp. 44.

  • IUCN/SSC Criteria Review Working Group. (1999). IUCN Red List Criteria review provisional report: draft of the proposed changes and recommendations. Species 31–32: 43–57.

    Google Scholar 

  • Jernvall, J., and Wright, P. C. (1998). Diversity components of impending primate extinctions. Proc. Natl. Acad. Sci. USA 95: 11279–11283.

    Article  PubMed  CAS  Google Scholar 

  • Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, S., Tamura, K., and Nei, M. (1993). MEGA Molecular Evolutionary Genetics Analysis, Version, 2.1, The Pennsylvania State University. University Park Press, Baltimore, MD.

  • Lesson, R. P. (1840). Species des mammiferes bimanes et quadrumanes, J. B. Baillière, Paris.

  • Longmire, J. L., Gee, G. F., Hardekoff, C. L., and Mark, G. A. (1992). Establishing paternity in whooping cranes (Grus americana) by DNA analysis. The Auk 109: 522–529.

    Google Scholar 

  • Maddison, W. P., and Maddison, D. R. (1992). MacClade: Analysis of Phylogeny and Character Evolution, Sinauer Associates, Sunderland, MA.

    Google Scholar 

  • Martin, R. D. (1972a) Adaptive radiation and behaviour of the Malagasy lemurs. Philos. Trans. Roy. Soc. (Lond.) B 264: 295–352.

    Article  CAS  Google Scholar 

  • Martin, R. D. (1972b). A preliminary field-study of the lesser mouse lemur (Microcebus murinus, J. F. Miller 1777). Z. Tierpsychol. Beiheft. 9: 43–89.

    Google Scholar 

  • Martin, R. D. (1995). Prosimians: From obscurity to extinction? In Alterman, L., Doyle, G. A., and Izard, M. K. (eds.), Creatures of the Dark: The Nocturnal Prosimians, Plenum Press, New York, pp. 535–563.

    Google Scholar 

  • Mayden, R. L. (1997). A hierarchy of species concepts: The denouement in the saga of the species problem. In Claridge, M. A., Dawah, H. A., and Wilson, M. R. (eds.), Species: The Units of Diversity, Chapman and Hall, London, pp. 381–424.

    Google Scholar 

  • Mayor, M. I., Sommer, J. A., Houck, M. L., Zaonarivelo, J. R., Wright, P. C., Ingram, C., Engel, S. R., and Louis, E. E., Jr. (2004). Specific status of Propithecus spp. Int. J. Primatol. 25: 875–900.

    Article  Google Scholar 

  • Mayr, E. (1942). Systematics and the Origin of Species from the Viewpoint of a Zoologist, Columbia University Press, New York.

    Google Scholar 

  • Miadana Harisoa, F., Rabesihanaka, S., Hawkins, F., Katz, A., Byers, O., and Seal, U. (eds.). (2002). Evaluation et Plans de Gestion pour la Conservation (CAMP) de la Faune de Madagascar: Lémuriens, Autres Mammifères, Reptiles et Amphibiens, Poissons d’eau douce et Evaluation de la Viabilité des Populations et de Habitats de Hypogeomys antimena (Vositse). Resume Executif. Version Finale. Conservation Breeding Specialist Group (SSC/IUCN), pp. 229–256.

  • Miller, J. F. (1777). Icones Animalium, Miller's Illustration of Linnaeus, 1776–1785. London.

  • Mittermeier, R. A., Tattersall, I., Konstant, W. R., Meyers, D. M., and Mast, R. B. (1994). Lemurs of Madagascar, Conservation International, Washington, DC, pp. 83–94.

  • Myers, N. (2000). Biodiversity hotspots for conservation priorities. Nature 403: 853–858.

    Article  PubMed  CAS  Google Scholar 

  • Pastorini, J., Forstner, M. R. J., and Martin, R. D. (2000). Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 16: 418–429.

    Article  PubMed  CAS  Google Scholar 

  • Pastorini, J., Forstner, M. R. J., and Martin, R. D. (2002). Phylogenetic relationships among Lemuridae (Primates): evidence from mtDNA. J. Hum. Evol. 43: 463–478.

    PubMed  Google Scholar 

  • Pastorini, J., Martin, R. D., Ehresmann, P., Zimmermann, E., and Forstner, M. R. J. (2001). Molecular phylogeny of the lemur family Cheirogaleidae (primates) based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. 19: 45–56.

    Article  PubMed  CAS  Google Scholar 

  • Pastorini, J., Thalmann, U., and Martin, R. D. (2003). A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc. Natl. Acad. Sci. USA 100: 5879–5884.

    Article  PubMed  CAS  Google Scholar 

  • Petter, J.-J., Albignac, R., and Rumpler, Y. (1977). Faune de Madagascar 44: Mammiferes Lémuriens (Primates, Prosimiens), ORSTOM/CNRS, Paris.

  • Rasoloarison, R. M., Goodman, S. M., and Ganzhorn, J. U. (2000). Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int. J. Primatol. 21: 963–1019.

    Article  Google Scholar 

  • Ravaoarimanana, B., Tiedemann, R., Montagnon, D., and Rumpler, Y. (2004). Molecular and cytogenetic evidence for cryptic speciation within a rare endemic Malagasy lemur, the northern sportive lemur (Lepilemur septentrionalis). Mol. Phylogenet. Evol. 31: 440–448.

    Article  PubMed  CAS  Google Scholar 

  • Reed, D. H. (2004). Extinction risk in fragmented habitats. Anim. Conserv. 7: 181–191.

    Article  Google Scholar 

  • Sambrook, J., Fritch, E. F., and Maniatus, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed, Cold Spring Harbor Laboratory Press, Cole Spring Harbor, New York.

    Google Scholar 

  • Schwarz, E. (1931). A revision of the genera and species of Madagascar Lemuridae. Proc. Zool. Soc. Lond. 1931: 399–428.

    Google Scholar 

  • Smith, R. J., and Jungers, W. L. (1997). Body mass in comparative primatology. J. Hum. Evol. 32: 523–559.

    Article  PubMed  CAS  Google Scholar 

  • Soltis, P. S., and Gitzendanner, M. A. (1999). Molecular systematics and the conservation of rare species. Conserv. Biol. 13: 471–483.

    Article  Google Scholar 

  • Swofford, D. L. (2001) PAUP *. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4.0b5, Sinauer Associates, Sunderland, MA.

    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 chimpanzee. Mol. Biol. Evol. 10: 512–526.

    PubMed  CAS  Google Scholar 

  • Telenius, H., Carter, N. P., Bebb, C. E., Nordenskjöb, M., Ponder, A. J., and Tunnacliffe, A. (1992). Degenerate oligonucleotide-primed PCR: General amplification of target DNA by a single degenerate primer. Genomics 13: 718–725.

    Article  PubMed  CAS  Google Scholar 

  • Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997). The ClustalX-Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 25: 4876–4882.

    Article  PubMed  CAS  Google Scholar 

  • Wheeler, Q. D., and Platnick, N. I. (2000). The phylogenetic species concept (sensu Wheeler and Platnick). In Wheeler, Q. D., and Meier, R. (eds.), Species Concepts and Phylogenetic Theory: A Debate, Columbia University Press, New York, pp. 230.

    Google Scholar 

  • Wyner, Y. M., Amato, G., and DeSalle, R. (1999). Captive breeding, reintroduction, and the conservation genetics of black and white ruffed lemurs, Varecia variegata variegata. Mol. Ecol. 8: S107–S115.

    Article  PubMed  CAS  Google Scholar 

  • Yoder, A. D., Rasoloarison, R. M., Goodman, S. M., Irwin, J. A., Atsalis, S., Ravosa, M. J., and Ganzhorn, J. U. (2000). Remarkable species diversity of Malagasy mouse lemurs (Primates, Microcebus). Proc. Natl. Acad. Sci. USA 97: 11325–11330.

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann, E., Cepok, S., Rakotoarison, M., Zietemann, V., and Radespiel, U. (1998). Sympatric mouse lemurs in northwest Madagascar: A new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatol. 69: 106–114.

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann, E., Ehresmann, P., Zietemann, V., Radespiel, U., Randrianambinina, B., and Rakotoasrison, N. (1997). Poster 5—a new primate species in north-western Madagascar: The golden-brown mouse lemur (Microcebus ravelobensis). Primate Eye 63: 26–27.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

A grant from the Committee for Research and Exploration of the National Geographic Society (6613.99) supported in part the work described here. The project would not have been possible without the support of the guides, staff, and drivers of the Institute for Conservation of Tropical Environments, Madagascar (ICTE-MICET), as well as the Association Nationale pour la Gestion des Aires Protégées (ANGAP), Parc Botanique et Zoologique de Tsimbazaza, the Ministère des Eaux et Forêt of Madagascar, and U.S. Fish and Wildlife. We acknowledge the generosity of Bill and Berniece Grewcock for their support at Henry Doorly Zoo. Generous equipment support from the Ahmanson Foundation and the Theodore F. and Claire M. Hubbard Family Foundation further sustained our research. Although the mouse lemur is considered the smallest primate in the world, its diminutive size is no reflection on the contribution to wildlife conservation by the 3 individuals for which the new Microcebus species are named in their honor.

We are thankful for the creative genius Stephen Nash who has prepared amazingly detailed and accurate illustrations of Microcebus spp.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edward E. Louis Jr..

Rights and permissions

Reprints and permissions

About this article

Cite this article

Louis, E.E., Coles, M.S., Andriantompohavana, R. et al. Revision of the Mouse Lemurs (Microcebus) of Eastern Madagascar. Int J Primatol 27, 347–389 (2006). https://doi.org/10.1007/s10764-006-9036-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-006-9036-1

KEY WORDS

Navigation