Skip to main content

Advertisement

SpringerLink
Log in

Genetic architecture of two red ruffed lemur (Varecia rubra) populations of Masoala National Park

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

The current range of the red ruffed lemur (Varecia rubra) population is primarily restricted to forests of the Masoala Peninsula on the northeastern coast of Madagascar. Whereas much of the peninsula is protected as Masoala National Park, parts of the forest are at risk from anthropogenic pressures and habitat fragmentation. We sampled 32 individual red ruffed lemur from two sites: Ambatoledama (DAMA), a narrow forest corridor across an area of degraded habitat connecting larger blocks of forest in the northwestern reaches of the park, and Masiaposa (MAS) forest, a largely pristine forest on the lower western side of the peninsula. Population genetic parameters were estimated for these two populations employing 15 microsatellite loci derived from the V. variegata genome. We found that by exceeding the expected heterozygosity at mutation-drift equilibrium, the DAMA population has undergone a recent population bottleneck. Population structure analysis detected individuals harboring genotypic admixture of the DAMA genetic cluster in the MAS population, suggesting a possibility of unilateral gene flow or movement between these populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allnutt TF, Powell GVN, Ferrier S, Ricketts TH, Steininger MK, Manion G (2004) Quantifying biodiversity loss in Madagascar using biological inventories, environmental data and a 50-year record of deforestation. Society for Conservation Biology Meetings, New York, 30 July–22 August 2004

  • Balko EA (1998) A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata in Ranomafana national park, Madagascar. PhD dissertation, Syracuse University

  • Balko EA, Underwood HB (2005) Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. Am J Primatol 66(1):45–70

    Article  PubMed  Google Scholar 

  • Balloux F (2004) Heterozygote excess in small populations and the heterozygote-excess effective population size. Evolution 58(9):1891–1900

    PubMed  Google Scholar 

  • Banks MA, Eichert W (2000) WHICHRUN (version 3.2) a computer program for population assignment of individuals based on multilocus genotype data. J Hered 91:87–89

    Article  CAS  PubMed  Google Scholar 

  • Callen DF, Thompson AD, Shen Y, Phillips HA, Richards RI, Mulley JC, Sutherland GR (1993) Incidence and origin of “null” alleles in the (AC)n microsatellite markers. Am J Hum Genet 52:922–927

    CAS  PubMed  Google Scholar 

  • Chakraborty R, Fuerst PA, Nei M (1980) Statistical studies on protein polymorphism in natural populations. III. Distribution of allele frequencies and the number of alleles per locus. Genetics 94:1039–1063

    PubMed  CAS  Google Scholar 

  • Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3):621–631

    Article  CAS  PubMed  Google Scholar 

  • Conservation Breeding Specialist Group (SSC/IUCN) (2002) Evaluation et Plans de Gestion pour la Conservation (CAMP) de la Fauna de Madagascar: Lémuriens, Autre Mammifères, Reptiles et Amphibiens, Poissons d’eau douce et Evaluation de la Viabilitiédes Populations et des Habitats de Hypogeomys antimena (Vositse). CBSG, Apple Valley

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed  Google Scholar 

  • Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multi-locus genotypes to select and exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdez AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170

    Article  CAS  PubMed  Google Scholar 

  • Dieringer D, Schlötterer C (2002) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 1(3):167–169

    Google Scholar 

  • Dutton CJ, Junge RE, Louis EE (2008) Biomedical evaluation of free-ranging red ruffed lemurs (Varecia rubra) within Masoala National Park, Madagascar. J Zool Wildl Med 39(1):76–85

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Frankham R, Ballou JA, Briscoe DA (2004) Introduction to conservation genetics. Cambridge University Press, Cambridge, p 536

    Google Scholar 

  • Garza JC, Williamson E (2001) Detection and reduction population size using data from microsatellite DNA. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Geoffroy-Saint Hilare E (1812) Notes sur trios dessins de Commerçon représentant des Quadrumanes d’un genre inconnu. Ann Mus Hist Nat Paris 19:171–175

    Google Scholar 

  • Gligor M, Ganzhorn JU, Radotondravony D, Ramilijaona OR, Razafimhatratra E, Zischler H, Hapke A (2009) Hybridization between mouse lemur species in an ecological transition zone in southern Madagascar. Mol Ecol 18:520–533

    Article  CAS  PubMed  Google Scholar 

  • Goodman SM, Ganzhorn JU (2004) Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers. J Biogeogr 31(1):47–55

    Article  Google Scholar 

  • Goudet J (1995) FSTAT, a computer program to test F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet 1995

  • Goudet J, Perrin N, Wasser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11:1103–1114

    Article  CAS  PubMed  Google Scholar 

  • Green C, Sussman RW (1990) Deforestation history of the eastern rain forests of Madagascar from satellites images. Science 248:212–215

    Article  PubMed  CAS  Google Scholar 

  • Hannah L, Rakotosamimanana B, Ganzhorn J, Mittermeier RA, Olivieri S, Iyer L, Rajaobelina S, Hough J, Andramialisoa F, Bowles I, Tilkin G (1998) Participatory planning, scientific priorities and landscape conservation in Madagascar. Environ Conserv 25:30–36

    Article  Google Scholar 

  • Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34(4):1–9

    Google Scholar 

  • Hekkala ER, Rakotondratsima M, Vasey N (2007) Habitat and distribution of the ruffed lemur, Varecia, north of the Bay of Antongil in northwestern Madagascar. Primate Conserv 22:89–95

    Article  Google Scholar 

  • Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  • Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for parental exclusion. Mol Ecol 14:599–612

    Article  CAS  PubMed  Google Scholar 

  • Holloway L (2000) Catalysing rainforest restoration in Madagascar. In: Lorenço WR, Goodman SM (eds) Diversité et Endémisme à Madagascar. Mémoires, Société de Biogéographie, Paris, pp 115–124

    Google Scholar 

  • Jenkins MD (ed) (1990) Madagascar: an environmental profile. IUCN Conservation Monitoring Centre, Gland

    Google Scholar 

  • Lawler R (2008) Testing for a historical bottleneck in wild Verreaux’s sifaka (Propithecus verreauxi verreauxi) using microsatellite data. Am J Primatol 70:990–994

    Article  PubMed  Google Scholar 

  • Louis EE Jr, Ratsimbazafy JH, Razakamaharavo VR, Pierson DJ, Barber RC, Brenneman RA (2005) Conservation genetics of black and white ruffed lemurs (Varecia variegata variegata) from Southeastern Madagascar. Anim Conserv 8:105–111

    Article  Google Scholar 

  • Luikart G, Cornuet J-M (1999) Estimating the effective number of breeders from heterozygote excess progeny. Genetics 151:1211–1216

    CAS  PubMed  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  PubMed  Google Scholar 

  • Markolf M, Roos C, Kappeler P (2008) Genetic and demographic consequences of a rapid reduction in population size in a solitary lemur (Mirza coquereli). Open Conserv Biol J 2:21–29

    Article  CAS  Google Scholar 

  • Merenlender A, Kremen C, Rakotondratsima M, Weiss A (1998) Monitoring impacts of natural resource extraction on lemurs of the Masoala peninsula, Madagascar. Conserv Ecol 2(2):5

    Google Scholar 

  • Mittermeier RA, Langrand O, Lowry PP II, Schatz G, Gerlasch J, Goodman SM, Steininger M, Hawkins F, Raminosoa N, Ramilijaona OAL, Andriamaro O, Randrianasolo H, Rabarison H, Rakotobe ZL (2004) Hotspots revisited: earth’s biologically richest and most endangered terrestrial ecosystems. CEMEX, USA

    Google Scholar 

  • Morin PA, Leduc RG, Archer FI, Martien KK, Huebinger R, Bickham JW, Taylor BL (2009) Significant deviations from Hardy–Weinberg equilibrium caused by low levels of microsatellite genotyping errors. Mol Ecol Res 9:498–504

    Article  Google Scholar 

  • Morland HS (1991) Social organization and ecology of black and white ruffed lemurs (Varecia variegata variegata) in lowland rain forest, Nosy Mangabe, Eastern Madagascar. Folia Primatol 56:253–265

    Article  Google Scholar 

  • Myers N (1988) Threatened biotas: “hotspots” in tropical forests. Environmentalist 8:1–12

    Article  Google Scholar 

  • Myers N (1998) Lifting the veil on perverse subsidies. Nature 392:327–328

    Article  CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Conserv Biol 12:516–520

    Google Scholar 

  • Nei M, Maryuama T, Chakraborty R (1975) The bottleneck effect and genetic variability in population size using data from microsatellite DNA. Mol Ecol 10:305–318

    Google Scholar 

  • Nelson R, Horning N (1993) Cover forest/non-forest classification of Madagascar from AVHRR data. Int J Remote Sens 14(8):1445–1446

    Article  Google Scholar 

  • Nicoll ME, Lagrand O (1993) AVHRR-LAC estimates of forested area in Madagascar, 1990. Int J Remote Sens 14(8):1463–1475

    Article  Google Scholar 

  • Olivieri GI, 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

    Article  Google Scholar 

  • Paetkau DW, Calvert W, Stirling I, Strombeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  CAS  PubMed  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Direct real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Patel E, Andrianandrasana LH (2008) Low elevation silky sifakas (Propithecus candidus) in the Makira Conservation Site at Andaparaty-Rabeson: ranging, demography, and possible sympatry with red ruffed lemurs (Varecia rubra). Lemur News 13:18–22

    Google Scholar 

  • Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size, version 1.3. Queensland Government, Department of Primary Industries and Fisheries

  • Petter JJ, Albignac R, Rumpler Y (1977) Faunne de Madagascar 44: Mammifères lémuriens (Primates prosimiens). ORSTOM/CNRS, Paris

    Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first generation migrants detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  • Pollack E (1987) On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117:353–360

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess progeny. Genetics 144:383–387

    CAS  PubMed  Google Scholar 

  • Quéméré E, Louis EE Jr, Ribéron L, Chikhi L, Crouau-Roy B (2009) Non-invasive conservation genetics of the critically endangered golden-crowned sifaka (Propithecus tattersalli): high diversity and significant genetic differentiation over a small range. Conserv Genet. doi:10.1007/s10592-009-9837-9

  • Radespiel U, Rakotondravony R, Chikhi L (2008) Natural and anthropogenic determinants of genetic structure in the largest remaining population of the endangered golden-brown mouse lemur, Microcebus ravelobensis. Am J Primatol 70:860–870

    Article  PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  CAS  PubMed  Google Scholar 

  • Ratsimbazafy JH (2002) On the brink of extinction and the process of recovery: responses of black and white ruffed lemurs (Varecia variegata variegata) to disturbances in Manombo. PhD dissertation, State University of New York, Stony Brook

  • Raymond M, Rousset F (1995) GENEPOP (Version3.1): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rigamonti MM (1993) Home range and diet in red ruffed lemurs (Varecia variegata rubra) on the Masoala peninsula, Madagascar. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum Press, New York, pp 25–39

    Google Scholar 

  • Simons HJ, Lindsay NB (1987) Survey work on ruffed lemurs (Varecia variegata) and other primates in the northeastern rainforests of Madagascar. Primate Conserv 8:88–91

    Google Scholar 

  • Slate J, Marshall TC, Pemberton JM (2000) A retrospective assessment of the accuracy of the paternity inference program CERVUS. Mol Ecol 9(6):801–808

    Article  CAS  PubMed  Google Scholar 

  • Tattersall I (1977) Distribution of Malagasy lemurs. Part 1: the lemurs of northern Madagascar. Annal N Y Acad Sci 293:160–169

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  CAS  Google Scholar 

  • Vasey N (1997a) Community ecology and behavior of Varecia variegata rubra and Lemur fulvus albifrons on the Masoala Peninsula, Madagascar. PhD dissertation, Washington University, St. Louis

  • Vasey N (1997b) How many red ruffed lemurs are left? Int J Primatol 18(2):207–216

    Article  Google Scholar 

  • Vasey N (2002) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns. Am J Phys Anthropol 118(2):169–183

    Article  PubMed  Google Scholar 

  • Vasey N (2003) Varecia, ruffed lemurs. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1332–1336

    Google Scholar 

  • Vasey N (2006) Impact of seasonality and reproduction on social structure, ranging patterns, and fission–fusion social organization in red ruffed lemurs. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 275–304

    Google Scholar 

  • Vasey N, Tattersall I (2002) Do ruffed lemurs form a hybrid zone?: distribution and discovery of Varecia with systematic and conservation implications. Am Mus Novit 3376:1–26

    Article  Google Scholar 

  • Waples RS (1991) Genetic methods for estimating the effective size of Cetacean populations. In: Hoezel AR (ed) Genetic ecology of whales and dolphins, special issue 13. International Whaling Commission, London, pp 279–300

    Google Scholar 

  • Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358–1370

    Article  Google Scholar 

  • White FG (1991) Social organization, feeding ecology and reproductive strategy of ruffed lemurs (Varecia variegata). In: Ehara A, Takenaka O (eds) Primatology, proceedings of the XIII congress of the IPS, Iwamoto, Nagoya and Kyoto. Elsevier Science, Amsterdam

    Google Scholar 

Download references

Acknowledgments

This project would not have been possible without the support of the staff of the Institute for Conservation of Tropical Environments, Madagascar (ICTE-MICET), as well as, the National Parks Madagascar (NPM), US Fish and Wildlife Service, and the Ministère des Eaux et Forêts of Madagascar. We thank Bill and Berniece Grewcock for their support of student interns, the Ahmanson Foundation for their generous support of DNA sequencers and other laboratory components, and the Theodore F. and Claire M. Hubbard Family Foundation for supporting conservation projects undertaken by the HDZ Madagascar Biodiversity and Biogeography Project. We thank the late Prof. Randria Ravololonarivo Gisele for her support of graduate students and the Department of Anthropology and Paleontology at the University of Antananarivo. Finally, we thank the three reviewers whose helpful comments greatly improved the manuscript. No animals were injured in this study, and the research protocols were performed within the guidelines of the Primate Society of Japan, the HDZ-IACUC #97-001, and in compliance with the care and expectations of local, national, and international laws and standards.

Author information

Authors and Affiliations

  1. Department of Paleontology and Anthropology, University of Antananarivo, 101, Antananarivo, Madagascar

    Vololoniaina R. Razakamaharavo

  2. Omaha’s Henry Doorly Zoo, 3701 South 10th Street, Omaha, NE, 68107, USA

    Susie M. McGuire, Edward E. Louis Jr. & Rick A. Brenneman

  3. Department of Anthropology, Portland State University, P.O. Box 751, Portland, OR, 97207, USA

    Natalie Vasey

Authors
  1. Vololoniaina R. Razakamaharavo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susie M. McGuire
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natalie Vasey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edward E. Louis Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rick A. Brenneman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rick A. Brenneman.

About this article

Cite this article

Razakamaharavo, V.R., McGuire, S.M., Vasey, N. et al. Genetic architecture of two red ruffed lemur (Varecia rubra) populations of Masoala National Park. Primates 51, 53–61 (2010). https://doi.org/10.1007/s10329-009-0171-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-009-0171-0

Keywords

Search

Navigation