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Two New Species of Mouse Lemurs (Cheirogaleidae: Microcebus) from Eastern Madagascar

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Abstract

The number of newly discovered Malagasy vertebrate taxa has multiplied in recent years, emphasizing the importance of complete taxon sampling for phylogenetics, biogeography, functional ecology, and conservation biology, especially in such a biodiversity hotspot. In particular, the diversity of extant lemurs is much higher than previously thought, and we have yet to comprehend fully the full extent of lemuriform biodiversity. A recent genetic analysis of mtDNA and nDNA sequence data in Malagasy mouse lemurs revealed the existence of several novel mtDNA clades based on new field sampling. These geographically defined and previously unrecognized mtDNA clades corresponded precisely to patterns of population structure revealed in the analysis of the nDNA data, thus confirming their evolutionary divergence from other mouse lemur clades. Two of these independently evolving lineages correspond to specimens that were collected by us in the Marolambo and Manantantely/Ivorona regions. Here we summarize the genetic evidence and report on the morphometric and external characteristics of these animals, formally describing them as new species. This report thus brings the number of currently recognized and described mouse lemur species to 20. The forests in which these mouse lemurs were discovered have been heavily degraded in the past decade, prompting the classification of one of the new species as Endangered by the IUCN, even before its formal description. As with several other newly described lemur species, immediate field studies and appropriate conservation actions are therefore urgent.

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References

  • Ali, J. R., & Huber, M. (2010). Mammalian biodiversity on Madagascar controlled by ocean currents. Nature, 463, 653–656.

    Article  PubMed  CAS  Google Scholar 

  • Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., et al. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22, 148–155.

    Article  Google Scholar 

  • Cuozzo, F. P., Rasoazanabary, E., Godfrey, L. R., Sauther, M. L., Youssouf, I. A., & LaFleur, M. M. (2013). Biological variation in a large sample of mouse lemurs from Amboasary, Madagascar: implications for interpreting variation in primate biology and paleobiology. Journal of Human Evolution, 64, 1–20.

    Article  PubMed  Google Scholar 

  • de Queiroz, K. (1998). The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In D. J. Howard & S. H. Berlocher (Eds.), Endless forms: Species and speciation (pp. 57–75). Oxford: Oxford University Press.

    Google Scholar 

  • Fujita, M. K., & Leaché, A. D. (2011). A coalescent perspective on delimiting and naming species: a reply to Bauer et al. Proceedings of the Royal Society B: Biological Sciences, 278, 493–495.

    Article  Google Scholar 

  • Gligor, M., Ganzhorn, J. U., Rakotondravony, D., Ramilijaona, O. R., Razafimahatratra, E., Zischler, H., et al. (2009). Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar. Molecular Ecology, 18, 520–533.

    Article  PubMed  CAS  Google Scholar 

  • Groeneveld, L. F., Weisrock, D. W., Rasoloarison, R. M., Yoder, A. D., & Kappeler, P. M. (2009). Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evolutionary Biology, 9, e30. doi:10.1186/1471-2148-9-30.

    Article  Google Scholar 

  • Hapke, A., Gligor, M., Rakotondranary, S. J., Rosenkranz, D., & Zupke, O. (2011). Hybridization of mouse lemurs: different patterns under different ecological conditions. BMC Evolutionary Biology, 11, e297. doi:10.1186/1471-2148-11-297.

    Article  Google Scholar 

  • Hapke, A., Andrianaivo, T. B. D., Gligor, M., & Razafimahatratra, E. (2013). Range shifts of mouse lemurs in south-eastern Madagascar: Evidence from mitochondrial genetic data. In J. Masters, M. Gamba, & F. Génin (Eds.), Leaping ahead (pp. 71–77). New York: Springer.

    Google Scholar 

  • Heckman, K., Rasoazanabary, E., Machlin, E., Godfrey, L., & Yoder, A. (2006). Incongruence between genetic and morphological diversity in Microcebus griseorufus of Beza Mahafaly. BMC Evolutionary Biology, 6, 98.

    Article  PubMed  Google Scholar 

  • Kappeler, P. M. (2000). Lemur origins: rafting by groups of hibernators? Folia Primatologica, 71, 422–425.

    Article  CAS  Google Scholar 

  • Kappeler, P. M., Rasoloarison, R. M., Razafimanantsoa, L., Walter, L., & Roos, C. (2005). Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1870, with description of a new species. Primate Report, 71, 3–26.

    Google Scholar 

  • Louis, E. E., Jr., Coles, M. S., Andriantompohavana, R., Sommer, J. A., Engberg, S. E., Zaonarivelo, J. R., et al. (2006). Revision of the mouse lemurs (Microcebus) of eastern Madagascar. International Journal of Primatology, 27, 347–389.

    Article  Google Scholar 

  • Louis, E. E., Jr., Engberg, S. E., McGuire, S. M., McCormick, M. J., Randriamampionona, R., Ranaivoarisoa, J. F., et al. (2008). Revision of the mouse lemurs, Microcebus (Primates, Lemuriformes), of northern and northwestern Madagascar with descriptions of two new species at Montagne d’Ambre National Park and Antafondro Classified Forest. Primate Conservation, 23, 19–38.

    Article  Google Scholar 

  • Mallet, J. (2008). Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2971–2986.

    Article  Google Scholar 

  • Markolf, M., Brameier, M., & Kappeler, P. M. (2011). On species delimitation: yet another lemur species or just genetic variation? BMC Evolutionary Biology, 11, e216. doi:10.1186/1471-2148-11-216.

    Article  Google Scholar 

  • Mittermeier, R. A., Tattersall, I., Konstant, W. R., Meyers, D. M., & Mast, R. B. (1994). Lemurs of Madagascar (1st ed.). Washington: Conservation International.

    Google Scholar 

  • Mittermeier, R. A., Louis, E. E., Jr., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A. B., et al. (2011). Lemurs of Madagascar (3rd ed.). Arlington: Conservation International.

    Google Scholar 

  • Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., & Kent, J. P. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.

    Article  PubMed  CAS  Google Scholar 

  • Nagy, Z. T., Sonet, G., Glaw, F., & Vences, M. (2012). First large-scale DNA barcoding assessment of reptiles in the biodiversity hotspot of Madagascar, based on newly designed COI primers. PLoS One, 7, e3. doi:10.1371/journal.pone.0034506.

    Google Scholar 

  • Padial, J. M., Miralles, A., De la Riva, I., & Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7, e16. doi:10.1186/1742-9994-7-16.

    Article  Google Scholar 

  • Pearson, R. G., & Raxworthy, C. J. (2009). The evolution of local endemism in Madagascar: watershed versus climatic gradient hypotheses evaluated by null biogeographic models. Evolution, 63, 959–967.

    Article  PubMed  Google Scholar 

  • Poux, C., Madsen, O., Marquard, E., Vieites, D. R., DeJong, W. W., & Vences, M. (2005). Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Systematic Biology, 54, 719–730.

    Article  PubMed  Google Scholar 

  • Radespiel, U., Ratsimbazafy, J. H., Rasoloharijaona, S., Raveloson, H., Andriaholinirina, N., Rakotondravony, R., et al. (2012). First indications of a highland specialist among mouse lemurs (Microcebus spp.) and evidence for a new mouse lemur species from eastern Madagascar. Primates, 53, 157–170.

    Article  PubMed  Google Scholar 

  • Rakotondranary, S. J., Hapke, A., & Ganzhorn, J. U. (2011). Distribution and morphological variation of Microcebus spp. along an environmental gradient in southeastern Madagascar. International Journal of Primatology, 32, 1037–1057.

    Article  Google Scholar 

  • Ramasindrazana, B., Goodman, S. M., Schoeman, M. C., & Appleton, B. (2011). Identification of cryptic species of Miniopterus bats (Chiroptera: Miniopteridae) from Madagascar and the Comoros using bioacoustics overlaid on molecular genetic and morphological characters. Biological Journal of the Linnean Society, 104, 284–302.

    Article  Google Scholar 

  • Rasoloarison, R. M., Goodman, S. M., & Ganzhorn, J. U. (2000). Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. International Journal of Primatology, 21, 963–1019.

    Article  Google Scholar 

  • Samonds, K. E., Godfrey, L. R., Ali, J. R., Goodmand, S. M., Vences, M., Sutherland, M. R., et al. (2012). Spatial and temporal arrival patterns of Madagascar’s vertebrate fauna explained by distance, ocean currents, and ancestor type. Proceedings of the National Academy of Sciences of the United States of America, 109, 5352–5357.

    Article  PubMed  CAS  Google Scholar 

  • Schmid, J., & Kappeler, P. M. (1994). Sympatric mouse lemurs (Microcebus ssp.) in western Madagascar. Folia Primatologica, 63, 162–170.

    Article  CAS  Google Scholar 

  • Smithe, F. B. (1975). Naturalist’s color guide. Part 1. New York: American Museum of Natural History.

    Google Scholar 

  • Solano, E., Gilbert, C., Richards, L., Taylor, P. J., Soarimalala, V., Engelbrecht, A., et al. (2011). First karyotypic descriptions of Malagasy rodents (Nesomyinae, Muridae) reveal variation at multiple taxonomic levels. Journal of Zoology (London), 285, 110–118.

    Article  Google Scholar 

  • Springer, M. S., Meredith, R. W., Gatesy, J., Emerling, C. A., Park, J., Rabosky, D. L., et al. (2012). Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PLoS One, 7, e49521.

    Article  PubMed  CAS  Google Scholar 

  • Stankiewicz, J., Thiart, C., Masters, J. C., & de Wit, M. J. (2006). Did lemurs have sweepstake tickets? an exploration of Simpson’s model for the colonization of Madagascar by mammals. Journal of Biogeography, 33, 221–235.

    Article  Google Scholar 

  • Tattersall, I. (2007). Madagascar’s lemurs: cryptic diversity or taxonomic inflation? Evolutionary Anthropology, 16, 12–23.

    Article  Google Scholar 

  • Vences, M., Wollenberg, K. C., Vieites, D. R., & Lees, D. C. (2009). Madagascar as a model region of species diversification. Trends in Ecology & Evolution, 24, 456–465.

    Article  Google Scholar 

  • Vieites, D. R., Wollenberg, K. C., Andreone, F., Köhler, J., Glawe, F., & Vences, M. (2009). Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences of the United States of America, 106, 8267–8272.

    Article  PubMed  CAS  Google Scholar 

  • Weisrock, D. W., Rasoloarison, R. M., Fiorentino, I., Ralison, J. M., Goodman, S. M., Kappeler, P. M., et al. (2010). Delimiting species without nuclear monophyly in Madagascar’s mouse lemurs. PLoS One, 5, e9883. doi:10.1371/journal.pone.0009883.

    Article  PubMed  Google Scholar 

  • Weisrock, D. W., Smith, S. D., Chan, L. M., Biebouw, K., Kappeler, P. M., Yoder, A. D. (2012). Concatenation and concordance in the reconstruction of mouse lemur phylogeny: an empirical demonstration of the effect of allele sampling in phylogenetics. Molecular Biology and Evolution, 29, 1615–1630.

    Google Scholar 

  • Wilmé, L., Goodman, S. M., & Ganzhorn, J. U. (2006). Biogeographic evolution of Madagascar’s microendemic biota. Science, 312, 1063–1065.

    Article  PubMed  Google Scholar 

  • Yang, Z., & Yoder, A. D. (2003). Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Systematic Biology, 52, 705–716.

    Article  PubMed  Google Scholar 

  • Yoder, A. D., & Nowak, M. (2006). Has vicariance or dispersal been the predominant biogeographic force in Madagascar? only time will tell. Annual Review of Ecology, Evolution, and Systematics, 37, 405–431.

    Article  Google Scholar 

  • Yoder, A. D., Rasoloarison, R. M., Goodman, S. M., Irwin, J. A., Atsalis, S., Ravosa, M. J., et al. (2000). Remarkable species diversity in Malagasy mouse lemurs (Primates, Microcebus). Proceedings of the National Academy of Sciences of the United States of America, 97, 11325–11330.

    Article  PubMed  CAS  Google Scholar 

  • Yoder, A. D., Burns, M. M., Zehr, S., Delefosse, T., Veron, G., Goodman, S. M., et al. (2003). Single origin of Malagasy carnivora from an African ancestor. Nature, 421, 734–737.

    Article  PubMed  CAS  Google Scholar 

  • Yoder, A. D., Olson, L. E., Hanley, C., Heckman, K. L., Rasoloarison, R. M., Russell, A. L., et al. (2005). A multidimensional approach for detecting species patterns in Malagasy vertebrates. Proceedings of the National Academy of Sciences of the United States of America, 102, 6587–6594.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the Malagasy authorities (Committee CAFF/CORE of the Ministry of Water, Forests and Environment), and especially our colleagues at the Département de Biologie Animale, Université d’Antananarivo for their authorization and support of this study. All field procedures adhered to the laws of Madagascar and were approved by the Ministry of Water, Forests and Environment. We thank Joanna Setchell and three anonymous reviewers for excellent comments, Bellarmin Ramahefasoa (Durrell Wildlife Conservation Trust Marolambo) for taking the photos depicted in Fig. 3, and H. Lahmann for preparing Fig. 1. This research was funded by a grant of the Deutsche Forschungsgemeinschaft to P. M. Kappeler (DFG, KA 1082/8-1&2).

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Authors and Affiliations

  1. Département de Biologie Animale, Université d’Antananarivo, BP 906, Antananarivo (101), Madagascar

    Rodin M. Rasoloarison & Daniel Rakotondravony

  2. Behavioral Ecology and Sociobiology Unit, German Primate Center (DPZ), 37077, Göttingen, Germany

    Rodin M. Rasoloarison & Peter M. Kappeler

  3. Department of Biology, University of Kentucky, Lexington, KY, 40506, USA

    David W. Weisrock

  4. Department of Biology, Duke University, Durham, NC, 27708, USA

    Anne D. Yoder

  5. Duke Lemur Center, Duke University, Durham, NC, 27705, USA

    Anne D. Yoder

  6. Department of Sociobiology/Anthropology, University of Göttingen, 37077, Göttingen, Germany

    Peter M. Kappeler

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  1. Rodin M. Rasoloarison
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  2. David W. Weisrock
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  3. Anne D. Yoder
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  4. Daniel Rakotondravony
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  5. Peter M. Kappeler
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Correspondence to Peter M. Kappeler.

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Rasoloarison, R.M., Weisrock, D.W., Yoder, A.D. et al. Two New Species of Mouse Lemurs (Cheirogaleidae: Microcebus) from Eastern Madagascar. Int J Primatol 34, 455–469 (2013). https://doi.org/10.1007/s10764-013-9672-1

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