Skip to main content

Advertisement

Log in

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

  • Original Paper
  • Published:
Conservation Genetics Aims and scope Submit manuscript

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.

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. 2
Fig. 3

Similar content being viewed by others

References

  • Avise JC (2000) Phylogeography. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Barrett EM, Gurnell J, Malarky G, Deaville R, Bruford MW (1999) Genetic structure of fragmented populations of red squirrel (Sciurus vulgaris) in the UK. Mol Ecol 8:S55–S63

    Article  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Dewar RE (1997) Were people responsible for the extinction of Madagascar’s subfossils, and how will we ever know? In: Goodman SM, Petterson BD (eds.) Natural change and human impact in Madagascar. Smithsonian Institution Press, Washington, pp. 364–377

    Google Scholar 

  • Frazer DF, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752

    Google Scholar 

  • Fredsted T, Pertoldi C, Olesen JM, Eberle M, Kappeler PM (2004) Microgeographic heterogeneity in spatial distribution and mtDNA variability of gray mouse lemurs (Microcebus murinus, Primates: Cheirogaleidae). Behav Ecol Sociobiol 56:393–403

    Article  Google Scholar 

  • Gerloff U, Hartung B, Fruth B, Hohmann G, Tautz D (1999) Intracommunity relationships, dispersal pattern and paternity success in a wild living community of Bonobos (Pan paniscus) determined from DNA analysis of faecal samples. Proc R Soc Lond B 266:1189–1195

    Article  CAS  Google Scholar 

  • Hofreiter M, Siedel H, Van Neer W, Vigilant L (2003) Mitochondrial DNA sequence from an enigmatic gorilla population (Gorilla gorilla uellensis). Am J Phys Anthropol 121:361–368

    Article  PubMed  Google Scholar 

  • Jobling MA, Tyler-Smith C (2003) The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet 4:598–612

    Article  PubMed  CAS  Google Scholar 

  • Johnson JA, Bellinger MR, Toepfer JE, Dunn P (2004) Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Mol Ecol 13:2617–2630

    Article  PubMed  CAS  Google Scholar 

  • Kappeler PM, Rasoloarison RM, Razafimanantsoa L, Walter L, Roos C (2005) Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) gray, 1970, with description of a new species. Prim Report 71:3–26

    Google Scholar 

  • Louis EE, Coles ME, Andrintompohavana R, Sommer JA, Engberg SE, Zaonarivelo JR, Mayor MI, Brenneman RA (2006) Revision of the Mouse Lemurs (Microcebus) of Eastern Madagascar. Int J Primotol 27:347–389

    Article  Google Scholar 

  • Moritz C (1994) Defining “evolutionary significant units” for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  PubMed  CAS  Google Scholar 

  • Pastorini J, Martin RD, Ehresmann P, Zimmermann E, Forstner MR (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, Martin RD (2003) A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc Natl Acad Sci USA 100:5879–5884

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Radespiel U, Lutermann H, Schmelting B, Bruford MW, Zimmermann E (2003) Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus. Anim Behav 65:709–719

    Article  Google Scholar 

  • Radespiel U, Raveloson H (2001) Preliminary study on the lemur communities at three sites of dry deciduous forest in the Réserve Naturelle d’Ankarafantsika. Lemur News 6:22–24

    Google Scholar 

  • Radespiel U, Sarikaya Z, Zimmermann E (2001) Sociogenetic structure in a free-living nocturnal primate population: sex-specific differences in the grey mouse lemur (Microcebus murinus). Behav Ecol Sociobiol 50:493–502

    Article  Google Scholar 

  • Randrianambinina B, Rasoloharijaona S, Rakotosamimanana B (2003) Inventaires des communautés lémuriennes dans la réserve spéciale de Bora au nord-ouest et la forêt domaniale de Mahilaka-Maromandia au nord de Madagascar. Lemur News 8:15–18

    Google Scholar 

  • Rakotoarisoa J-A (1997) A cultural history of Madagascar: evolution and interpretation of the archeological evidence. In: Goodman SM, Petterson BD (eds.) Natural change and human impact in Madagascar. Smithsonian Institution Press, Washington, pp. 331–341

    Google Scholar 

  • Rasoloarison RM, Goodman SM, Ganzhorn JU (2000) Taxonomic revision of mouse lemurs (Microcebus) in the western portions of Madagascar. Int J Primotol 21:963–1019

    Article  Google Scholar 

  • Rendigs A, Radespiel U, Wrogemann D, Zimmermann E (2003) Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. Int J Primatol 24:47–64

    Article  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messenguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetics data analysis

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    Article  CAS  Google Scholar 

  • Smith AP (1997) Deforestation, fragmentation, and reserve design in western Madagascar. In: Laurance WF, Bierregard RO Jr (eds.) Tropical forest remnants: ecology, management, and conservation of fragmented communities. University of Chicago Press, Chicago, pp. 415–441

    Google Scholar 

  • Swofford DL (1998) PAUP*, Phylogenetic Analysis Using Parsimony (*and Other Methods). Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Tallman DA, Draheim HM, Mills LS, Allendorf FW (2002) Insights into recently fragmented vole populations from combined genetic and demographic data. Mol Ecol 11:699–709

    Article  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Thalmann O, Hebler J, Poinar HN, Paabo 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

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Weidt A, Hagenah N, Randrianambinina B, Radespiel U, Zimmermann E (2004) Social organization of the golden brown mouse lemur (Microcebus ravelobensis). Am J Phys Anthropol 123:40–51

    Article  PubMed  Google Scholar 

  • Wimmer B, Tautz D, Kappeler PM (2002) The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behav Ecol Sociobiol 52:166–175

    Article  Google Scholar 

  • Wright HT, Rakotoarisoa J-A (1997) Cultural transformations and the impacts on the environments of Madagascar. In: Goodman SM, Petterson BD (eds.) Natural change and human impact in Madagascar. Smithsonian Institution Press, Washington, pp. 309–330

    Google Scholar 

  • Yoder AD, Cartmill M, Ruvolo M, Smith K, Vilgalys R (1996) Ancient single origin for Malagasy primates. Proc Natl Acad Sci USA 93:5122–5126

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yoder AD, Yang Z (2000) Estimation of primate speciation dates using local molecular clocks. Mol Biol Evol 17:1081–1090

    PubMed  CAS  Google Scholar 

  • Yoder AD, Yang Z (2004) Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Mol Ecol 13:757–773

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

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

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

Keywords

Navigation