First indications of a highland specialist among mouse lemurs (Microcebus spp.) and evidence for a new mouse lemur species from eastern Madagascar

Primates

Volumn 53, Issue 2, 2012, Pages 157-170

  Radespiel, Ute ^a,b   Ratsimbazafy, Jonah H ^b,c   Rasoloharijaona, Solofonirina ^b,d   Raveloson, Herimalala ^b,d   Andriaholinirina, Nicole ^b,d   Rakotondravony, Romule ^b,d   Randrianarison, Rose M ^b   Randrianambinina, Blanchard ^b,d  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b Groupe d'Etude et de Recherche sur les Primates de Madagascar (GERP)   (Madagascar)

^c DURRELL WILDLIFE CONSERVATION TRUST   (United Kingdom)

^d Campus Universitaire d'Ambondrona   (Madagascar)

Author keywords

Conservation; Evolution; Morphometry; Phylogeny; Primates; Taxonomy

Indexed keywords

CONSERVATION STATUS; FAUNA; GEOGRAPHICAL DISTRIBUTION; MORPHOMETRY; NEW SPECIES; PHYLOGENETICS; PHYLOGENY; PRIMATE; TAXONOMY;

ANIMAL; ARTICLE; CHEIROGALEIDAE; CLASSIFICATION; DEMOGRAPHY; ECOSYSTEM; ENVIRONMENTAL PROTECTION; GENETICS; HAPLOTYPE; MADAGASCAR; PHYLOGENY; PHYSIOLOGY; SPECIES DIFFERENCE; TREE;

ANIMALS; CHEIROGALEIDAE; CONSERVATION OF NATURAL RESOURCES; DEMOGRAPHY; ECOSYSTEM; HAPLOTYPES; MADAGASCAR; PHYLOGENY; SPECIES SPECIFICITY; TREES;

MADAGASCAR; MANTADIA NATIONAL PARK; TOAMASINA;

LEMUR; LEMURIDAE; MICROCEBUS; MICROCEBUS LEHILAHYTSARA; PRIMATES;

EID: 84859568036     PISSN: 00328332     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10329-011-0290-2     Document Type: Article

References (43)

1. Andriantompohavana R, Zaonarivelo JR, Engberg SW, Randriamampionona R, McGuire SM, Shore GD, Rakotonomenjanahary R, Brenneman RA, Louis EE Jr (2006) Mouse lemurs of northwestern Madagascar with a description of a new species at Lokobe Special Reserve. Occas Pap Tex Tech Univ Mus 259: 1-23.
2. Atsalis S (1999) Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemurs, Microcebus rufus. Int J Prim 20: 883-910.
3. Atsalis S, Schmid J, Kappeler PM (1996) Metrical comparisons of three species of mouse lemur. J Hum Evol 31: 61-68.
4. Cracraft J (1983) Species concepts and speciation analysis. Curr Ornithol 1: 159-187.
5. Craul M, Zimmermann E, Rasoloharijaona S, Randrianambinina B, Radespiel U (2007) Unexpected species diversity of Malagasy primates (Lepilemur spp.) in the same biogeographical zone: a morphological and molecular approach with the description of two new species. BMC Evol Biol 7. doi: 10. 1186/1471-2148-7-83.
6. Dammhahn M, Kappeler PM (2005) Social system of Microcebus berthae, the world's smallest primate. Int J Prim 26: 407-435.
7. Génin F (2008) Life in unpredictable environments: first investigation of the natural history of Microcebus griseorufus. Int J Prim 29: 303-321.
8. Goodman SM, Ganzhorn JU (2004) Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers. J Biogeogr 31: 47-55.
9. Green GM, Sussman RW (1990) Deforestation history of the eastern rain forests of Madagascar from satellite images. Science 248: 212-215.
10. Groeneveld LF, Weisrock DW, Rasoloarison RM, Yoder AD, Kappeler PM (2009) Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evol Biol 9: 30.
11. Groeneveld LF, Rasoloarison RM, Kappeler PM (2011) Morphometrics confirm taxonomic deflation in dwarf lemurs (Primates: Cheirogaleidae), as suggested by genetics. Zool J Linn Soc 161: 229-244.
12. Guschanski K, Olivieri G, Funk SM, Radespiel U (2007) MtDNA reveals strong genetic differentiation among geographically isolated populations of the golden brown mouse lemur, Microcebus ravelobensis. Conserv Genet 8: 809-821.
13. Hafen T, Neveu H, Rumpler Y, Wilden I, Zimmermann E (1998) Acoustically dimorphic advertisement calls separate morphologically and genetically homogenous populations of the grey mouse lemur (Microcebus murinus). Folia Primatol 69(Suppl 1): 342-356.
14. Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Env Cons 34: 1-9.
15. Kamilar JM, Muldoon KM (2010) The climatic niche diversity of Malagasy primates: a phylogenetic perspective. PLoS ONE 5: e11073.
16. Kappeler PM, Rasoloarison RM, 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 Rep 71: 3-26.
17. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163.
18. Louis EE Jr, Coles MS, Andriantompohavana R, Sommer JA, Engberg SE, Zaonarivelo JR, Mayor MI, Brenneman RA (2006) Revision of the mouse lemurs (Microcebus) of Eastern Madagascar. Int J Primatol 27: 347-389.
19. Louis EE Jr, Engberg SE, McGuire SM, McCormick MJ, Randriamampionona R, Ranaivoarisoa JF, Bailey CA, Mittermeier RA, Lei R (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 Conserv 23: 19-38.
20. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor.
21. Mittermeier RA, Ganzhorn JU, Konstant WR, Glander K, Tattersall I, Groves CP, Rylands AB, Hapke A, Ratsimbazafy J, Mayor MI, Louis EE Jr, Rumpler Y, Schwitzer C, Rasoloarison RM (2008) Lemur diversity in Madagascar. Int J Primatol 29: 1607-1656.
22. Mittermeier RA, Louis EE Jr, Richardson M, Schwitzer C, Langrand O, Rylands AB, Hawkins F, Rajaobelina S, Ratsimbazafy J, Rasoloarison R, Roos C, Kappeler PM, Mackinnon J (2010) Lemurs of Madagascar, 3rd edn. Conservation International, Arlington.
23. Muldoon KM, Goodman SM (2010) Ecological biogeography of Malagasy non-volant mammals: community structure is correlated with habitat. J Biogeogr 37: 1144-1159.
24. Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, Radespiel U (2007) The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol Phylogenet Evol 43: 309-327.
25. Olivieri GL, Sousa V, Chikhi L, Radespiel U (2008) From genetic diversity and structure to conservation: genetic signature of recent population declines in three mouse lemur species (Microcebus spp.). Biol Conserv 141: 1257-1271.
26. Padial JM, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zool 7: 16. doi: 10. 1186/1742-9994-7-16.
27. Pearson RG, Raxworthy CJ (2009) The evolution of local endemism in Madagascar: watershed versus climatic gradient hypotheses evaluated by null biogeographic models. Evolution 63: 959-967.
28. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.
29. Radespiel U, Olivieri G, Rasolofoson DW, Rakotondratsimba G, Rakotonirainy O, Rasoloharijaona S, Randrianambinina B, Ratsimbazafy JH, Ratelolahy F, Randriamboavonjy T, Rasolofoharivelo T, Craul M, Rakotozafy L, Randrianarison RM (2008) Exceptional diversity of mouse lemurs (Microcebus spp.) in the Makira region with the description of one new species. Am J Primatol 70: 1033-1046.
30. Randrianambinina B (2001) Contribution à l'étude comparative de l'écoéthologie de deux microcèbes rouges de Madagascar: Microcebus ravelobensis (Zimmermann et al., 1998) Microcebus rufus (Lesson, 1840) (doctoral thesis). University of Antananarivo, Madagascar.
31. Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primatol 21: 963-1019.
32. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
33. Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analysis. Can J Zool 69: 82-90.
34. Silvestro D, Michalak (2010) raxmlGUI: a graphical front-end for RAxML. http://sourceforge. net/projects/raxmlgui/.
35. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
36. Tattersall I (2007) Madagascar's lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol 16: 12-23.
37. Thalmann O, Hebler J, Poinar HN, Pääbo S, Vigilant L (2004) Unreliable mtDNA data due to nuclear insertions: a cautionary tale from analysis of humans and other great apes. Mol Ecol 13: 321-335.
38. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
39. Vences M, Wollenberg KC, Vieites DR, Lees DC (2009) Madagascar as a model region of species diversification. Trends Ecol Evol 24: 456-465.
40. Weisrock DW, Rasoloarison RM, Fiorentino L, Ralison JM, Goodman SM, Kappeler PM, Yoder AD (2010) Delimiting species without nuclear monophyly in Madagascar's mouse lemurs. PLoS ONE 5: e9883. doi: 10. 1371/journal. pone. 0009883.
41. Wilmé L, Goodman SM, Ganzhorn JU (2006) Biogeographic evolution of Madagascar's microendemic biota. Science 312: 1063-1065.
42. Yoder AD, Rasoloarison RM, Goodman SM, Irwin JA, Atsalis S, Ravosa MJ, Ganzhorn JU (2000) Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus). Proc Natl Acad Sci USA 97: 11325-11330.
43. Zimmermann E, Cepok S, Rakotoarison N, Zietemann V, Radespiel U (1998) Sympatric mouse lemurs in North-West Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatol 69: 106-114.