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MtDNA reveals strong genetic differentiation among geographically isolated populations of the golden brown mouse lemur, Microcebus ravelobensis

Abstract

Microcebus ravelobensis is an endangered nocturnal primate endemic to northwestern Madagascar. This part of the island is subject to extensive human intervention leading to massive habitat destruction and fragmentation. We investigated the degree of genetic differentiation among remaining populations using mitochondrial control region sequences (479–482 bases). Nine populations were sampled from the hypothesized geographic range. The region is composed of three inter-river systems (IRSs). Samples were collected in three areas of continuous forests (CFs) and six isolated forest fragments (IFFs) of different sizes. We identified 27 haplotypes in 114 animals, with CFs and IFFs harbouring 5–6 and 1–3 haplotypes, respectively. All IFFs were significantly differentiated from each other with high ΦST values and sets of unique haplotypes. The rivers constitute significant dispersal barriers with over 82% of the molecular variation being attributed to the divergence among the IRSs. The data suggest a deep and so far unknown split within the rufous mouse lemurs of northwestern Madagascar. The limited data base and the lack of ecological and morphological data do not allow definite taxonomic classification at this stage. However, the results clearly indicate that M. ravelobensis consists of three evolutionary significant units, possibly cryptic species, which warrant urgent and separate conservation efforts.

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Acknowledgements

We would like to thank the following institutions and persons for their support and the permissions to conduct the necessary fieldwork in Madagascar: Le Ministère des Eaux et Forêts, Chantal Andrianarivo (ANGAP), University of Antananarivo (Olga Ramilijaona and Daniel Rakotondravony), and the late Berthe Rakotosamimanana. For help and assistance in the field, we thank Mathias Craul, Jean-Aimé Rakotonirina, Todisoa Razafimamonjy. Many thanks go to all students and colleagues who helped collecting samples over the course of the last 4 years and especially to Pia Braune, Nicole Hagenah, Kathrin Marquart, Romule Rakotondravony, Blanchard Randrianambinina, Solofo Rasoloharijaona, and Andrea Weidt. We are very grateful to Elke Zimmermann for her constant support during the course of the work. We thank Lounès Chikhi and Mike Bruford for the helpful comments on the analyses and the manuscript. K.G. thanks Heike Pröhl for valuable discussions. Thanks go to the Institute of Zoology, Zoological Society of London, UK, for providing molecular facilities for part of the study. The manuscript was greatly improved by the comments of two anonymous reviewers. The study was financially supported by DFG (Ra 502/7-1) and Conservation International. We also gratefully acknowledge the Scholarship of the German National Academic Foundation for the financial support of K.G. throughout the study and especially during the fieldwork in Madagascar.

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Correspondence to U. Radespiel.

Appendix

Appendix

Summary list of samples used in this study. The source population, the respective IRS, year of sampling, sex and haplotype assignment as well as the sampler of each individual are provided. The sample ID is composed of the individual number, followed by the year of sampling and by an abbreviation for the population. All sequences have been deposited in GenBank under the Accession numbers EF065272–EF065385.

Sample ID Population IRS Year Sex Haplotype Samplera
012y00jbb JBB I 2000 m H11 UR, P. Braune
014y00jbb JBB I 2000 f H13 UR, P. Braune
008y00jbb JBB I 2000 f H15 UR, P. Braune
011y00jbb JBB I 2000 f H18 UR, P. Braune
005y00jbb JBB I 2000 m H11 UR, P. Braune
016y00jbb JBB I 2000 f H15 UR, P. Braune
021y00jbb JBB I 2000 m H11 UR, P. Braune
007y00jbb JBB I 2000 f H21 UR, P. Braune
006y00jbb JBB I 2000 m H11 UR, P. Braune
002y00jbb JBB I 2000 m H18 UR, P. Braune
004y00jbb JBB I 2000 f H18 UR, P. Braune
010y00jbb JBB I 2000 f H18 UR, P. Braune
013y00jbb JBB I 2000 m H11 UR, P. Braune
015y00jbb JBB I 2000 f H11 UR, P. Braune
078y00bev Bevazaha I 2003 m H16 R. Rakotondravony
095y00bev Bevazaha I 2003 m H16 R. Rakotondravony
001y00bev Bevazaha I 2000 f H12 UR
089y03bev Bevazaha I 2000 f H12 UR
098y03bev Bevazaha I 2003 f H13 R. Rakotondravony
088y03bev Bevazaha I 2003 m H16 R. Rakotondravony
084y03bev Bevazaha I 2003 m H16 R. Rakotondravony
085y03bev Bevazaha I 2003 f H16 R. Rakotondravony
079y03bev Bevazaha I 2003 f H16 R. Rakotondravony
116y03bev Bevazaha I 2003 f H23 R. Rakotondravony
005y00bev Bevazaha I 2000 m H12 UR
006y00bev Bevazaha I 2000 f H12 UR
080y03bev Bevazaha I 2003 m H22 R. Rakotondravony
003y00bev Bevazaha I 2000 f H17 UR
004y00bev Bevazaha I 2000 m H17 UR
002y00bev Bevazaha I 2000 f H17 UR
022y01stm Ste.Marie I 2001 f H14 UR, KG, K. Marquart
028y01stm Ste.Marie I 2001 f H14 UR, KG, K. Marquart
012y01stm Ste.Marie I 2001 m H24 UR, KG, K. Marquart
020y01stm Ste.Marie I 2001 f H14 UR, KG, K. Marquart
003y01stm Ste. Marie I 2001 f H14 UR, KG, K. Marquart
006y01stm Ste. Marie I 2001 m H14 UR, KG, K. Marquart
011y01stm Ste. Marie I 2001 m H14 UR, KG, K. Marquart
021y01stm Ste. Marie I 2001 m H14 UR, KG, K. Marquart
016y01stm Ste. Marie I 2001 f H14 UR, KG, K. Marquart
027y01stm Ste. Marie I 2001 m H14 UR, KG, K. Marquart
005y01stm Ste. Marie I 2001 m H14 UR, KG, K. Marquart
004y01stm Ste. Marie I 2001 f H14 UR, KG, K. Marquart
002y01stm Ste. Marie I 2001 f H14 UR, KG, K. Marquart
014y01stm Ste. Marie I 2001 f H14 UR, KG, K. Marquart
013y01stm Ste. Marie I 2001 f H14 UR, KG, K. Marquart
019y01stm Ste. Marie I 2001 m H14 UR, KG, K. Marquart
008y01stm Ste. Marie I 2001 f H14 UR, KG, K. Marquart
018y01stm Ste. Marie I 2001 m H14 UR, KG, K. Marquart
103y03mari Mariarano I 2003 f H20 GO
106y03mari Mariarano I 2003 m H10 GO
061y03mari Mariarano I 2003 f H10 GO
096y03mari Mariarano I 2003 f H10 GO
081y03mari Mariarano I 2003 f H20 GO
057y03mari Mariarano I 2003 f H25 GO
097y03mari Mariarano I 2003 f H10 GO
079y03mari Mariarano I 2003 f H20 GO
085y03mari Mariarano I 2003 f H10 GO
075y03mari Mariarano I 2003 m H20 GO
058y03mari Mariarano I 2003 m H20 GO
101y03mari Mariarano I 2003 f H10 GO
099y03mari Mariarano I 2003 f H10 GO
051y03mari Mariarano I 2003 f H20 GO
086y03mari Mariarano I 2003 f H10 GO
367y03tsia Tsiaramaso I 2003 f H19 GO, KG
359y03tsia Tsiaramaso I 2003 f H19 GO, KG
368y03tsia Tsiaramaso I 2003 f H19 GO, KG
358y03tsia Tsiaramaso I 2003 f H19 GO, KG
369y03tsia Tsiaramaso I 2003 f H19 GO, KG
365y03tsia Tsiaramaso I 2003 f H19 GO, KG
360y03tsia Tsiaramaso I 2003 m H19 GO, KG
371y03tsia Tsiaramaso I 2003 f H19 GO, KG
370y03tsia Tsiaramaso I 2003 f H19 GO, KG
364y03tsia Tsiaramaso I 2003 f H19 GO, KG
363y03tsia Tsiaramaso I 2003 f H19 GO, KG
366y03tsia Tsiaramaso I 2003 f H19 GO, KG
362y03tsia Tsiaramaso I 2003 m H19 GO, KG
361y03tsia Tsiaramaso I 2003 m H19 GO, KG
372y03tsia Tsiaramaso I 2003 f H19 GO, KG
340y03ata Maroakata II 2003 m H5 GO, KG
311y03ata Maroakata II 2003 m H5 GO, KG
308y03ata Maroakata II 2003 f H6 GO, KG
323y03ata Maroakata II 2003 f H6 GO, KG
345y03ata Maroakata II 2003 f H26 GO, KG
332y03ata Maroakata II 2003 m H5 GO, KG
312y03ata Maroakata II 2003 m H5 GO, KG
314y03ata Maroakata II 2003 f H5 GO, KG
326y03ata Maroakata II 2003 f H5 GO, KG
327y03ata Maroakata II 2003 f H5 GO, KG
301y03ata Maroakata II 2003 f H7 GO, KG
313y03ata Maroakata II 2003 m H7 GO, KG
347y03ata Maroakata II 2003 f H8 GO, KG
317y03ata Maroakata II 2003 m H8 GO, KG
339y03ata Maroakata II 2003 f H5 GO, KG
307y03ata Maroakata II 2003 f H6 GO, KG
318y03ata Maroakata II 2003 f H8 GO, KG
319y03ata Maroakata II 2003 f H8 GO, KG
151y03est Mahajamba-Est II 2003 m H9 UR, R. Rakotondravony
154y03est Mahajamba-Est II 2003 f H9 UR, R. Rakotondravony
153y03est Mahajamba-Est II 2003 f H9 UR, R. Rakotondravony
149y03est Mahajamba-Est II 2003 f H9 UR, R. Rakotondravony
152y03est Mahajamba-Est II 2003 f H9 UR, R. Rakotondravony
148y03est Mahajamba-Est II 2003 f H9 UR, R. Rakotondravony
357y03amb Ambongabe III 2003 f H2 GO, KG
356y03amb Ambongabe III 2003 f H2 GO, KG
349y03amb Ambongabe III 2003 m H2 GO, KG
352y03amb Ambongabe III 2003 m H2 GO, KG
355y03amb Ambongabe III 2003 f H1 GO, KG
348y03amb Ambongabe III 2003 f H3 GO, KG
353y03amb Ambongabe III 2003 f H3 GO, KG
354y03amb Ambongabe III 2003 m H3 GO, KG
350y03amb Ambongabe III 2003 f H1 GO, KG
003y02bora Bora III 2002 f H27 B. Randrianambinina, S. Rasoloharijaona
002y02bora Bora III 2002 m H4 B. Randrianambinina, S. Rasoloharijaona
001y02bora Bora III 2002 m H4 B. Randrianambinina, S. Rasoloharijaona
  1. aSampling authors are abbreviated with initials

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Guschanski, K., Olivieri, G., Funk, S.M. et al. MtDNA reveals strong genetic differentiation among geographically isolated populations of the golden brown mouse lemur, Microcebus ravelobensis . Conserv Genet 8, 809–821 (2007). https://doi.org/10.1007/s10592-006-9228-4

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  • DOI: https://doi.org/10.1007/s10592-006-9228-4

Keywords

  • Primates
  • Madagascar
  • Genetic diversity
  • Habitat fragmentation
  • Cryptic species