Skip to main content

Patch size and isolation influence genetic patterns in black-and-white ruffed lemur (Varecia variegata) populations

Abstract

Land use in Madagascar has resulted in extensive deforestation and forest fragmentation. Endemic species, such as the black-and-white ruffed lemur (Varecia variegata), may be vulnerable to habitat fragmentation due to patchy geographic distributions and sensitivities to forest disturbance. We tested for genetic differentiation among black-and-white ruffed lemur groups in two sites in a large forest patch and three sites in smaller patches. We also investigated the relationship between the genetic diversity of populations and patch configuration (size and isolation), as well as the presence or absence of past genetic bottlenecks. We collected blood (n = 22 individuals) or fecal (n = 33) samples from lemurs and genotyped the extracted DNA for 16 polymorphic microsatellites. Bayesian cluster analysis and FST assigned individuals to three populations: Ranomafana (two sites in continuous forest), Kianjavato (two fragments separated by 60 m of non-forest), and Vatovavy (a single fragment, more isolated in time and space). Vatovavy showed significantly lower allelic richness than Ranomafana. Kianjavato also appeared to have lower allelic richness than Ranomafana, though the difference was not significant. Vatovavy was also the only population with a genetic bottleneck indicated under more than one mutation model and a significant FIS value, showing excess heterozygosity. These results indicate that a small geographic separation may not be sufficient for genetic differentiation of black-and-white ruffed lemur populations and that patch size may influence the rapidity with which genetic diversity is lost following patch isolation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  • Andrainarivo C, Andriaholinirina V, Feistner A, Felix T, Ganzhorn J, Garbut N, Golden C, Konstant B, Louis EEJ, Meyers D, Mittermeier R, Perieras A, Princee F, Rabarivola J, Rakotosamimanana B, Rasamimanana H, Ratsimbazafy JH, Raveloarinoro G, Razafimanantsoa A, Rumpler Y, Schwitzer C, Thalmann U, Wilme L, Wright P (2008) Varecia variegata. IUCN. 2009. www.iucnredlist.org. 2009

  • Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71:355–366

    Article  Google Scholar 

  • Arroyo-Rodríguez V, Dias PAD (2010) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 72:1–16

    Article  PubMed  Google Scholar 

  • Baden AL, Brenneman RA, Louis EE Jr (2008) Morphometrics of wild black-and-white ruffed lemurs (Varecia variegata, Kerr 1792). Am J Primatol 70:1–14

    Article  Google Scholar 

  • Baden AL, Wright PC, Louis EE, Bradley BJ (in press) Communal care, kinship and maternal success in a social primate. Behav Ecol Sociobiol

  • Balko EA (1998) A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar. Dissertation, State University of New York College of Environmental Science and Forestry, New York

  • Bossart JL, Prowell DP (1998) Genetic estimates of population structure and gene flow: limitations, lessons and new directions. Trends Ecol Evol 13(5):202–205

    Article  PubMed  CAS  Google Scholar 

  • Brenneman RA, Johnson SE, Bailey CA, Ingraldi C, Delmore KE, Wyman TM, Andriamaharoa HE, Ralainasolo FB, Ratsimbazafy JH, Louis EE (2012) Population genetics and abundance of gray-headed lemurs (Eulemur cinereiceps): potential consequences of fragmentation and cyclones in an endangered primate. Oryx. doi:10.1017/S0030605311000159

    Google Scholar 

  • Brockman DK, Willis MS, Karesh WB (1987) Management and husbandry of ruffed lemurs, Varecia-variegata, at the San-Diego-zoo.2. Reproduction, pregnancy, parturition, litter size, infant care, and reintroduction of hand-raised infants. Zoo Biol 6(4):349–363

    Article  Google Scholar 

  • Busch JD, Waser PM, DeWoody JA (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16(12):2450–2462

    Article  PubMed  CAS  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4):2001–2014

    PubMed  CAS  Google Scholar 

  • Craul M, Chikhi L, Sousa V, Olivieri GL, Rabesandratana A, Zimmermann E, Radespiel U (2009) Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar. Biol Cons 142(12):2862–2871

    Article  Google Scholar 

  • Dellicour S, Frantz AC, Colyn M, Bertouille S, Chaumont F, Flamand MC (2011) Population structure and genetic diversity of red deer (Cervus elaphus) in forest fragments in north-western France. Conserv Genet 12(5):1287–1297

    Article  Google Scholar 

  • di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91(8):3166–3170

    Article  PubMed  Google Scholar 

  • Drees C, De Vries H, Hardtle W, Matern A, Persigehl M, Assmann T (2011) Genetic erosion in a stenotopic heathland ground beetle (Coleoptera: Carabidae): a matter of habitat size? Conserv Genet 12(1):105–117

    Article  Google Scholar 

  • Erhart EM, Overdorff DJ (2008) Rates of agonism by diurnal lemuroids: implications for female social relationships. Int J Primatol 29:1227–1247

    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  PubMed  CAS  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  • Foerg R (1982) Reproductive-behavior in Varecia-variegata. Folia Primatol 38(1–2):108–121

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10(6):1500–1508

    Article  Google Scholar 

  • Gerber BD (2010) Madagascar GIS: spatial information to aid research and conservation. http://filebox.vt.edu/users/bgerber/services.htm. Accessed 5 Mar 2012

  • Google Inc (2009) Google Earth. 5.1.3509.4636 edn. Google Inc

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86(6):485–486

    Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9.3. Available at http://www.unil.ch/popgen/softwares/fstat/htm. version 2.9.3 edn

  • Grativol AD, Ballou JD, Fleischer RC (2001) Microsatellite variation within and among recently fragmented populations of the golden lion tamarin (Leontopithecus rosalia). Conserv Genet 2:1–9

    Article  CAS  Google Scholar 

  • Harper G, Maclean N, Goulson D (2003) Microsatellite markers to assess the influence of population size, isolation and demographic change on the genetic structure of the UK butterfly Polyommatus bellargus. Mol Ecol 12:3349–3357

    Article  PubMed  CAS  Google Scholar 

  • Harper G, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34(4):325–333

    Article  Google Scholar 

  • IUCN 2011. IUCN red list of threatened species. Version 2011.2. <www.iucnredlist.org>. Downloaded on 16 Apr 2012

  • Jordan MA, Morris DA, Gibson SE (2009) The influence of historical landscape change on genetic variation and population structure of a terrestrial salamander (Plethodon cinereus). Conserv Genet 10(6):1647–1658

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17(5):230–241

    Article  Google Scholar 

  • Keyghobadi N, Roland J, Matter SF, Strobeck C (2005) Among-and within-patch components of genetic diversity respond at different rates to habitat fragmentation: an empirical demonstration. Proc R Soc B 272:553–560

    Article  PubMed  Google Scholar 

  • Knaepkens G, Bervoets L, Verheyen E, Eens M (2004) Relationship between population size and genetic diversity in endangered populations of the European bullhead (Cottus gobio): implications for conservation. Biol Cons 115:403–410

    Article  Google Scholar 

  • Lampila S, Kvist L, Wistbacka R, Orell M (2009) Genetic diversity and population differentiation in the endangered Siberian flying squirrel (Pteromys volans) in a fragmented landscape. Eur J Wildl Res 55:397–406

    Article  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11(11):2445–2449

    Article  PubMed  CAS  Google Scholar 

  • Liu ZJ, Ren BP, Wu RD, Zhao L, Hao YL, Wang BS, Wei FW, Long YC, Li M (2009) The effect of landscape features on population genetic structure in Yunnan snub-nosed monkeys (Rhinopithecus bieti) implies an anthropogenic genetic discontinuity. Mol Ecol 18(18):3831–3846

    Article  PubMed  CAS  Google Scholar 

  • Longmire JL, Gee GF, Hardekopf CL, Mark GA (1992) Establishing paternity in whooping cranes (Grus americana by DNA analysis. The Auk 109(3):522–529

    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, from Southeastern Madagascar. Anim Conserv 8:105–111

    Article  Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12(1):228–237

    Article  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89(3):238–247

    Article  PubMed  CAS  Google Scholar 

  • Mittermeier RA, Louis EEJ, 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. conservation international tropical field guide series, Arlington

    Google Scholar 

  • Morland HS (1991) Social organization and ecology of black and white ruffed lemurs (Variecia variegata) in lowland rain forest, Nosy Mangabe, Madagascar. Dissertation, Yale University

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403(6772):853–858

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70(12):3321–3323

    Article  PubMed  CAS  Google Scholar 

  • Oklander LI, Kowalewski MM, Corach D (2010) Genetic consequences of habitat fragmentation in black-and-gold howler (Alouatta caraya) populations from northern Argentina. Int J Primatol 31(5):813–832

    Article  Google Scholar 

  • 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 Cons 141(5):1257–1271

    Article  Google Scholar 

  • Pardini R, Marques de Souza S, Braga-Neto R, Metzger JP (2005) The role of forest structure, fragment size and corridors in maintaining small mammal abundance and diversity in an Atlantic forest landscape. Biol Cons 124:253–266

    Article  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S, Vásquez-Carrillo C, Pauli JN, Palsbøll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    Article  PubMed  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(4):502–503

    Article  Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6:847–859

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    PubMed  CAS  Google Scholar 

  • Quéméré E, Crouau-Roy B, Rabarivola C, Louis EE, Chikhi L (2010) Landscape genetics of an endangered lemur (Propithecus tattersalli) within its entire fragmented range. Mol Ecol 19(8):1606–1621

    Article  PubMed  Google Scholar 

  • 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(9):860–870

    Article  PubMed  Google Scholar 

  • Ratsimbazafy J (2002) On the brink of extinction and the process of recovery: responses of black-and-white ruffed lemurs (Varecia variegata) to disturbance in Manombo Forest, Madagascar. Dissertation, State University of New York at Stony Brook

  • Raymond M, Rousset F (1995) GENEPOP (Version-1.2)-population-genetics software for exact tests and ecumenicism. J Hered 86(3):248–249

    Google Scholar 

  • Razakamaharavo VR, McGuire SM, Vasey N, Louis EE, Brenneman RA (2010) Genetic architecture of two red ruffed lemur (Varecia rubra) populations of Masoala National Park. Primates 51(1):53–61

    Article  PubMed  Google Scholar 

  • Rousset F (2008) GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8(1):103–106

    Article  PubMed  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392(6675):491–494

    Article  CAS  Google Scholar 

  • Sambrook J, Fritch EF, Maniatus T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Press, New York

    Google Scholar 

  • Segelbacher G, Höglund J, Storch I (2003) From connectivity to isolation: genetic consequences of population fragmentation in capercaillie across Europe. Mol Ecol 12:1773–1780

    Article  PubMed  CAS  Google Scholar 

  • Stangel PW, Lennartz MR, Smith MH (1992) Genetic variation and population structure of red-cockaded woodpeckers. Conserv Biol 6(2):283–292

    Article  Google Scholar 

  • Vasey N (2005) New developments in the behavioral ecology and conservation of ruffed lemurs (Varecia). Am J Primatol 66:1–6

    Article  PubMed  Google Scholar 

  • Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • White FJ, Overdorff DJ, Balko EA, Wright PC (1995) Distribution of ruffed lemurs (Varecia-variegata) in Ranomafana National-Park, Madagascar. Folia Primatol 64(3):124–131

    Article  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST≠1/(4Nm+1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Wikberg EC, Sicotte P, Campos FA, Ting N (2012) Between-group variation in female dispersal, kin composition of groups, and proximity patterns in a black-and-white colobus monkey (Colobus vellerosus). PLoS One 7(11):e48740. doi:10.1371/journal.pone.0048740

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto S, Morita K, Koizumi I, Maekawa K (2004) Genetic differentiation of white-spotted charr (Salvelinus leucomaenis) populations after habitat fragmentation: spatial-temporal changes. Conserv Genet 5:529–538

    Google Scholar 

Download references

Acknowledgments

We would like to thank all of the local and foreign research assistants for sample collection in Madagascar (specifically F. Gordon, L.G. Razanajatovo, C. Razafindravelo, E.E. Rakotoson, and J.P. Marolahy for fecal sample collection), the staff at the Grewcock Center for Conservation and Research at Omaha’s Henry Doorly Zoo and Aquarium for help with genotyping, T. Wyman for help with maps, and M. Aylward for input regarding statistical analysis. Funding was provided by the Natural Sciences and Engineering Research Council of Canada (SMH), the government of Alberta (SMH), the University of Calgary (SMH, SEJ), the International Primatological Society (SMH), the Calgary Zoological Society (SMH), the National Science Foundation (ALB, DDIG BSC-0725975), J. William Fulbright Foundation (ALB), the L.S.B. Leakey Foundation (ALB), Stony Brook University (ALB), Conservation International and Margot Marsh Biodiversity Foundation’s Primate Action Fund (SMH, ALB, SEJ), and Primate Conservation, Inc. (SMH, ALB, SEJ).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sheila M. Holmes.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Holmes, S.M., Baden, A.L., Brenneman, R.A. et al. Patch size and isolation influence genetic patterns in black-and-white ruffed lemur (Varecia variegata) populations. Conserv Genet 14, 615–624 (2013). https://doi.org/10.1007/s10592-013-0455-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0455-1

Keywords

  • Forest fragmentation
  • Genetic differentiation
  • Diversity
  • Bottleneck
  • Madagascar