International Journal of Primatology

, Volume 27, Issue 2, pp 347–389 | Cite as

Revision of the Mouse Lemurs (Microcebus) of Eastern Madagascar

  • Edward E. LouisJr.
  • Melissa S. Coles
  • Rambinintsoa Andriantompohavana
  • Julie A. Sommer
  • Shannon E. Engberg
  • John R. Zaonarivelo
  • Mireya I. Mayor
  • Rick A. Brenneman

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.


Control region Madagascar Microcebus mouse lemur prosimian system-atics 



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.


  1. Adkins, R. M., and Honeycutt, R. L. (1994). Evolution of the primate cytochrome c oxidase subunit II gene. J. Mol. Evol. 38: 215–231.PubMedCrossRefGoogle Scholar
  2. 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
  3. 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.PubMedCrossRefGoogle Scholar
  4. 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
  5. 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
  6. Davis, J. I., and Nixon, K. C. (1992). Populations, genetic variation, and the delimitation of phylogenetic species. Syst. Biol. 41: 421–435.CrossRefGoogle Scholar
  7. Ganzhorn, J. U. (1998). Nested patterns of species composition and their implications for lemur biogeography in Madagascar. Folia Primatol. 69: 332–341.CrossRefGoogle Scholar
  8. Groves, C. P. (2000). The genus Cheirogaleus: Unrecognized biodiversity in dwarf lemurs. Int. J. Primatol. 21: 943–961.CrossRefGoogle Scholar
  9. Groves, C. P. (2001). Primate Taxonomy, Smithsonian Institution, Washington, DC, pp. 26–53; 68–70.Google Scholar
  10. 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.PubMedCrossRefGoogle Scholar
  11. Hedges, S. B. (1994). Molecular evidence for the origin of birds. Proc. Natl. Acad. Sci. USA 91: 2621–2624.PubMedCrossRefGoogle Scholar
  12. Hey, J. (2001). The mind of the species problem. TRENDS Ecol. Evol. 16: 326–329.PubMedCrossRefGoogle Scholar
  13. IUCN Conservation Monitoring Unit. (1984). In Jenkins, M. (ed.), An Environmental Profile of Madagascar, IUCN, Cambridge, UK, pp. 44.Google Scholar
  14. 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
  15. Jernvall, J., and Wright, P. C. (1998). Diversity components of impending primate extinctions. Proc. Natl. Acad. Sci. USA 95: 11279–11283.PubMedCrossRefGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.Google Scholar
  18. Lesson, R. P. (1840). Species des mammiferes bimanes et quadrumanes, J. B. Baillière, Paris.Google Scholar
  19. 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
  20. Maddison, W. P., and Maddison, D. R. (1992). MacClade: Analysis of Phylogeny and Character Evolution, Sinauer Associates, Sunderland, MA.Google Scholar
  21. Martin, R. D. (1972a) Adaptive radiation and behaviour of the Malagasy lemurs. Philos. Trans. Roy. Soc. (Lond.) B 264: 295–352.CrossRefGoogle Scholar
  22. 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
  23. 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
  24. 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
  25. 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.CrossRefGoogle Scholar
  26. Mayr, E. (1942). Systematics and the Origin of Species from the Viewpoint of a Zoologist, Columbia University Press, New York.Google Scholar
  27. 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.Google Scholar
  28. Miller, J. F. (1777). Icones Animalium, Miller's Illustration of Linnaeus, 1776–1785. London.Google Scholar
  29. 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.Google Scholar
  30. Myers, N. (2000). Biodiversity hotspots for conservation priorities. Nature 403: 853–858.PubMedCrossRefGoogle Scholar
  31. 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.PubMedCrossRefGoogle Scholar
  32. 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.PubMedGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. Petter, J.-J., Albignac, R., and Rumpler, Y. (1977). Faune de Madagascar 44: Mammiferes Lémuriens (Primates, Prosimiens), ORSTOM/CNRS, Paris.Google Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.PubMedCrossRefGoogle Scholar
  38. Reed, D. H. (2004). Extinction risk in fragmented habitats. Anim. Conserv. 7: 181–191.CrossRefGoogle Scholar
  39. 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
  40. Schwarz, E. (1931). A revision of the genera and species of Madagascar Lemuridae. Proc. Zool. Soc. Lond. 1931: 399–428.Google Scholar
  41. Smith, R. J., and Jungers, W. L. (1997). Body mass in comparative primatology. J. Hum. Evol. 32: 523–559.PubMedCrossRefGoogle Scholar
  42. Soltis, P. S., and Gitzendanner, M. A. (1999). Molecular systematics and the conservation of rare species. Conserv. Biol. 13: 471–483.CrossRefGoogle Scholar
  43. Swofford, D. L. (2001) PAUP *. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4.0b5, Sinauer Associates, Sunderland, MA.Google Scholar
  44. 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.PubMedGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. 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.PubMedCrossRefGoogle Scholar
  47. 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
  48. 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.PubMedCrossRefGoogle Scholar
  49. 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.PubMedCrossRefGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. 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

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Edward E. LouisJr.
    • 1
  • Melissa S. Coles
    • 2
  • Rambinintsoa Andriantompohavana
    • 3
  • Julie A. Sommer
    • 1
  • Shannon E. Engberg
    • 1
  • John R. Zaonarivelo
    • 3
  • Mireya I. Mayor
    • 4
  • Rick A. Brenneman
    • 1
  1. 1.Center for Conservation and ResearchHenry Doorly ZooOmahaUSA
  2. 2.Department of BiologyUniversity of NebraskaOmahaUSA
  3. 3.University of AntananarivoAntananarivo 101AntananarivoMadagascar
  4. 4.Department of AnthropologyState University of New YorkStony BrookUSA

Personalised recommendations