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Non-invasive conservation genetics of the critically endangered golden-crowned sifaka (Propithecus tattersalli): high diversity and significant genetic differentiation over a small range

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Abstract

The genetic structure of the golden-crowned sifaka (Propithecus tattersalli) was evaluated in three forest types in the Daraina region between the Loky and Manambato Rivers in northeastern Madagascar. This critically endangered lemur species, only found within this restricted region (~1,300 km2), comprises populations which survive in forest fragments of varying size. While this remote region is already affected by human deforestation, the scheduled paving of the national road can potentially bring significant changes in the near future. In 2006, sifakas feces from 82 putative individuals were collected immediately after defecation. DNA samples were genotyped at 13 microsatellite loci to characterize patterns of genetic diversity within and among three sets of forest fragments representing different ecological types. The recent 2CTAB/PCI extraction method and the ‘comparative’ genotype validation approach allowed us to significantly improve the efficiency of amplification procedures. We found that golden-crowned sifaka genetic diversity was surprisingly high despite its narrow distribution and the current level of habitat fragmentation. We used both spatial and non-spatial Bayesian clustering methods to determine if forest edges correlated with cryptic genetic clusters and found that it was overall the case. However, the results also indicate that migrations are possible between two of the three studied forest complexes despite the presence of the national road. This is probably due to remaining riparian and small forest patches between these two forest complexes. The third forest complex is more differentiated although some migrations/connections may still exist through non-sampled fragments. This strongly suggests that it is necessary to maintain corridors and small patches, and also to explore the genetic diversity of the fragments outside the protected area.

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References

  • Anderson EC, Dunham K (2008) The influence of family groups on inferences made with the program Structure. Mol Ecol Res 8:1219–1229

    Article  Google Scholar 

  • Banks SC, Lindenmayer DB, Ward SJ, Taylor AC (2005) The effects of habitat fragmentation via forestry plantation establishment on spatial genotypic structure in the small marsupial carnivore, Antechinus agilis. Mol Ecol 14:1667–1680. doi:10.1111/j.1365-294X.2005.02525.x

    Article  CAS  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996/2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171. Université de Montpellier II, Montpellier

    Google Scholar 

  • Bellemain E, Nawaz MA, Valentini A, Swenson JE, Taberlet P (2007) Genetic tracking of the brown bear in northern Pakistan and implications for conservation. Biol Conserv 134:537–547. doi:10.1016/j.biocon.2006.09.004

    Article  Google Scholar 

  • Bergl RA, Vigilant L (2007) Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli). Mol Ecol 16(3):501–516. doi:10.1111/j.1365-294X.2006.03159.x

    Article  PubMed  Google Scholar 

  • Beyer HL (2004) Hawth’s analysis tools for ARCGIS. Available at http://www.spatialecology.com/htools/

  • Broquet T, Petit E (2004) Quantifying genotyping errors in non-invasive population genetics. Mol Ecol 13:3601–3608. doi:10.1111/j.1365-294X.2004.02352.x

    Article  CAS  PubMed  Google Scholar 

  • Broquet T, Ménard N, Petit E (2007) Noninvasive population genetics: a review of sample source, diet, fragment length and microsatellite motif effects on amplification success and genotyping error rates. Conserv Genet 8:249–260. doi:10.1007/s10592-006-9146-5

    Article  Google Scholar 

  • Burney DA (1999) Rates, patterns, and processes of landscape transformation and extinction in Madagascar. In: MacPhee A (ed) Extinctions in near time: causes, contexts and consequences. Kluwer Academic/Plenum Publishers, New York, pp 145–164

    Google Scholar 

  • Burney DA, Burney LP, Godfrey LR, Jungers WL, Goodman SM, Wright HT, Jull AJT (2004) A chronology for late prehistoric Madagascar. J Hum Evol 47:25–63. doi:10.1016/j.jhevol.2004.05.005

    Article  PubMed  Google Scholar 

  • Chen C, Durant E, Forbes F, François O (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Mol Ecol Notes 7(5):747–756. doi:10.1111/j.1471-8286.2007.01769.x

    Article  Google Scholar 

  • Chikhi L, Bruford MW (2005) Mammalian population genetics and genomics. In: Ruvinsky A, Marshall Graves J (eds) Mammalian genomics, chapter 21. CABI Publishers, UK, pp 539–583

    Chapter  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Coulon A, Fitzpatrick JW, Bowman R, Stith BM, Makarewich CA, Stenzler LM, Lovette IJ (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens). Mol Ecol 17:1685–1701. doi:10.1111/j.1365-294X.2008.03705.x

    Article  CAS  PubMed  Google Scholar 

  • Craul M, Chikhi L, Sousa V, Olivieri G, Rabesandratana A, Zimmermann E, Radespiel U (2009) Influence of forest fragmentation on endangered large-bodied lemurs in northwestern Madagascar-implications for conservation

  • Dewar RE (2003) Relationship between human ecological pressure and the vertebrate extinctions. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. The University of Chicago Press, Chicago, pp 119–122

    Google Scholar 

  • Dunham AE, Erhart EM, Overdorff DJ, Wright PC (2008) Evaluating effects of deforestation, hunting, and El Ninõ events on a threatened lemur. Biol Conserv 141:287–297. doi:10.1016/j.biocon.2007.10.006

    Article  Google Scholar 

  • Eriksson J, Hohmann G, Boesch C, Vigilant L (2004) Rivers influence the population genetic structure of bonobos (Pan paniscus). Mol Ecol 13:3425–3435. doi:10.1111/j.1365-294X.2004.02332.x

    Article  CAS  PubMed  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. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  Google Scholar 

  • François O, Blum MGB, Jakobsson M, Rosenberg NA (2008) Demographic history of European populations of Arabidopsis thaliana. PLoS Genet 4(5):e1000075. doi:10.1371/journal.pgen.1000075

    Article  PubMed  Google Scholar 

  • Frantz AC, Pope LC, Carpenter PJ, Roper TJ, Wilson GJ, Delahay RJ, Burke T (2003) Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Mol Ecol 12:1649–1661. doi:10.1046/j.1365-294X.2003.01848.x

    Article  CAS  PubMed  Google Scholar 

  • Ganzhorn JU, Goodman SM, Dehgan A (2003) Effects of forest fragmentation on small mammals and lemurs. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1228–1234

    Google Scholar 

  • Godfrey LR, Irwin MT (2007) The evolution of extinction risk: past and present anthropogenic impacts on the primate communities of Madagascar. Folia Primatol (Basel) 78:405–419. doi:10.1159/000105152

    Article  Google Scholar 

  • Goodman SM, Benstead JP (2003) The natural history of Madagascar. The University of Chicago Press, Chicago

    Google Scholar 

  • Goossens B, Chikhi L, Jalil MF, Ancrenaz M, Lackman-Ancrenaz I, Mohamed M, Andau P, Bruford MW (2005) Patterns of genetic diversity and migration in increasingly fragmented and declining orang-utan (Pongo pygmaeus) populations from Sabah, Malaysia. Mol Ecol 14(2):441–456. doi:10.1111/j.1365-294X.2004.02421.x

    Article  CAS  PubMed  Google Scholar 

  • Goossens B, Setchell JM, James SS, Funk SM, Chikhi L, Abulani A, Ancrenaz M, Lackman-Ancrenaz I, Bruford MW (2006) Philopatry and reproductive success in Bornean orang-utans (Pongo pygmaeus). Mol Ecol 15(9):2577–2588. doi:10.1111/j.1365-294X.2006.02952.x

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Avaible from http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet J (1995) FSTAT v-1.2: a computer program to calculate F statistics, J Hered 86, 485–486

  • Guillot G, Estoup A, Mortier F, Cosson J-F (2005a) A spatial statistical model for landscape genetics. Genetics 170(3):1261–1280. doi:10.1534/genetics.104.033803

    Article  CAS  PubMed  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005b) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5(3):708–711. doi:10.1111/j.1471-8286.2005.01031.x

    Article  Google Scholar 

  • Hansen H, Ben-David M, McDonald DB (2008) Effects of genotyping protocols on success and errors in identifying individual river otters (Lontra canadensis) from their faeces. Mol Ecol Resour 8(2):282–289. doi:10.1111/j.1471-8286.2007.01992.x

    Article  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDI: a versatile computer program to analyse spatial genetic structure at the individual and population levels. Mol Ecol Notes 2:618–620. doi:10.1046/j.1471-8286.2002.00305.x

    Article  Google Scholar 

  • He W, Lin L, Shen F, Zhang W, Zhang Z, King E, Yue B (2008) Genetic diversities of the giant panda (Ailuropoda melanoleuca) in wanglang and baoxing nature reserves. Conserv Genet 9:1541–1546. doi:10.1007/s10592-007-9493-x

    Article  Google Scholar 

  • Irwin MT (2006) Ecologically enigmatic lemurs: the sifakas of the eastern forests (Propithecus candidus, P. diadema, P. edwardsi, P. perrieri and P. tattersalli). In: Gould L, Sauther M (eds) Lemurs: ecology and adaptation. Springer, New York, pp 305–326

    Google Scholar 

  • Jalil MJ, Cable J, Sinyor J, Lackman-Ancrenaz I, Ancrenaz M, Bruford MW, Goosens B (2008) Riverine effects on mitochondrial structure of Bornean orang-utans (Pongo pygmaeus) at two spatial scales. Mol Ecol 17(12):2898–2909. doi:10.1111/j.1365-294X.2008.03793.x

    Article  CAS  PubMed  Google Scholar 

  • Lathuillière M, Ménard N, Gautier-Hion A, Crouau-Roy B (2001) Testing the reliability of non-invasive genetic sampling by comparing blood and feces samples in Barbary macaques (Macaca sylvanus). Am J Primatol 55:151–158. doi:10.1002/ajp.1048

    Article  PubMed  Google Scholar 

  • Lawler RR, Richard AF, Riley MA (2001) Isolation and screening of microsatellite loci in a wild lemur population (Propithecus verreauxi verreauxi). Am J Primatol 55:253–259. doi:10.1002/ajp.1058

    Article  CAS  PubMed  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Mayor MI, Sommer JA, Houck ML, Zaonarivelo JR, Wright PC, Ingram C, Engel SR, Louis EEJ (2004) Specific status of Propithecus spp. Int J Primatol 25:875–900. doi:10.1023/B:IJOP.0000029127.31190.e9

    Article  Google Scholar 

  • Meyers D (1993) The effects of resource seasonality on the behavior and reproduction of the golden-crowned Sifaka (Propithecus tattersalli, Simons, 1988) in three Malagasy forests. PhD Dissertation, Duke University, University microfilms, Ann Arbor

  • Miquel C, Bellemain E, Poillot C, Bessière J, Durant A, Taberlet P (2006) Quality indexes to assess the reliability of genotypes in studies using noninvasive sampling and multiple-tube approach. Mol Ecol Notes 6(4):985–988. doi:10.1111/j.1471-8286.2006.01413.x

    Article  Google Scholar 

  • Mittermeier RA, Konstant WR, Hawkins F, Louis EE, Langrand O, Ratsimbazafy J, Rasoloarison R, Ganzhorn JU, Rajaobelina S, Tattersall I, Meyers DM (2005) Lemurs of Madagascar, 2nd edn. Conservation International, Washington

    Google Scholar 

  • Morin PA, Chambers KE, Boesch C, Vigilant L (2001) Quantitative polymerase chain reaction analysis of DNA from noninvasive samples for accurate microsatellite genotyping of wild chimpanzees (Pan troglodytes verus). Mol Ecol 10(7):1835–1844. doi:10.1046/j.0962-1083.2001.01308.x

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evol Int J Org Evol 29:1–10. doi:10.2307/2407137

    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 Conserv 141:1257–1271. doi:10.1016/j.biocon.2008.02.025

    Article  Google Scholar 

  • Pritchard J, Wen W (2004) Documentation for STRUCTURE Software: version 2. Department of Human Genetics, University of Chicago, Chicago

    Google Scholar 

  • Quéméré E, Champeau J, Besolo A, Rasolondraibe E, Rabarivola CJ, Crouau-Roy B, Chikhi L (2009) Spatial variation in density and total size estimates in fragmented primate populations: the golden-crowned sifaka (Propithecus tattersalli)

  • 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. doi:10.1002/ajp.20574

    Article  PubMed  Google Scholar 

  • Rakotoarisoa G, Shore G, McGuire S, Engberg S, Louis EE, Brenneman RA (2006) Characterization of 20 microsatellite marker loci in Coquerel’s sifaka (Propithecus coquereli). Mol Ecol Notes 6(4):1119–1121. doi:10.1111/j.1471-8286.2006.01457.x

    Article  CAS  Google Scholar 

  • Razafindrakoto A, Quéméré E, Shore G, McGuire SM, Louis EE, Brenneman RA (2008) Characterization of 20 microsatellites marker loci in the golden-crowned sifaka (Propithecus tattersalli). Conserv Genet 9:1027–1031. doi:10.1007/s10592-007-9440-x

    Article  CAS  Google Scholar 

  • Riley SPD, Pollinger JP, Sauvajot RM, York EC, Bromley C, Fuller TL, Wayse RK (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741. doi:10.1111/j.1365-294X.2006.02907.x

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62. doi:10.1046/j.1420-9101.2000.00137.x

    Article  Google Scholar 

  • Scott DM, Brown D, Mahood S, Denton B, Silburn A, Rakotondraparany F (2006) The impacts of forest clearance on lizard, small mammal and bird communities in the arid spiny forest, southern Madagascar. Biol Conserv 127:72–87. doi:10.1016/j.biocon.2005.07.014

    Article  Google Scholar 

  • Simons EL (1988) A new species of Propithecus (Primates) from Northeast Madagascar. Folia Primatol (Basel) 50:148–151. doi:10.1159/000156340

    Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evol Int J Org Evol 47:264–279. doi:10.2307/2410134

    Google Scholar 

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

    Google Scholar 

  • Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Demelle E, Vierling L, Waits LP (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142. doi:10.1038/sj.hdy.6800917

    Article  CAS  PubMed  Google Scholar 

  • Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 2:3189–3194. doi:10.1093/nar/24.16.3189

    Article  Google Scholar 

  • Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327. doi:10.1016/S0169-5347(99)01637-7

    Article  PubMed  Google Scholar 

  • Vallet D, Petit EJ, Gatti S, Levréro S, Ménard N (2008) A new 2CTAB/PCI method improves DNA amplification success from faeces of Mediterranean (Barbary macaques) and tropical (lowland gorillas) primates. Conserv Genet 9(3):677–680. doi:10.1007/s10592-007-9361-8

    Article  CAS  Google Scholar 

  • Vargas A, Jiménez I, Palomeres F, Palacios MJ (2002) Distribution, status, and conservation needs of the golden-crowned sifaka (Propithecus tattersalli). Biol Conserv 108:325–334. doi:10.1016/S0006-3207(02)00117-9

    Article  Google Scholar 

  • Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254. doi:10.2307/2529947

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population-structure. Evol Int J Org Evol 38:1358–1370. doi:10.2307/2408641

    Google Scholar 

  • Wilmé L, Goodman SM, Ganzhorn JU (2006) Biogeographic evolution of Madagascar’s microendemic biota. Science 312(5776):1063–1065. doi:10.1126/science.1122806

    Article  PubMed  Google Scholar 

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Acknowledgments

Financial support for this study was provided by CNRS and the French ministry of Research core funding to UMR5174 CNRS Université Paul Sabatier EQ was funded by a MNRT (Ministère de l’Education Nationale, de la Recherche et de la Technologie) PhD grant. The field work was possible thanks to the support of the following associations and NGOs: IDEA WILD, CEPA (Conservation des Espèces et Populations Animales, notably J.-M. Lernould) and FANAMBY (in particular S. Rajaobelina, S. Wohlhauser, and McG. Ranaivo Arivelo). We warmly thank Daraina local communities for welcoming us, guides and research assistants for their precious help on the field. We thank CAFF/CORE, the “Direction générale des Eaux et Forêt” for giving us permission to conduct the fieldwork in Madagascar and for the authorizations to export the samples, and Prof. C. Rabarivola for his support. We also thank two anonymous referees, S. Wohlhauser, McG. Ranaivo Arivelo and M. Beaumont for useful and constructive comments which helped us improve the manuscript. The lab work was funded by European Commission (research contract QLRI-CT-2002-01325 INPRIMAT), the Center of Conservation and Research (CCR), Omaha’s Henry Doory Zoo (Nebraska, USA), where the microsatellites were isolated and the Institut Français de la Biodiversité, Programme Biodiversité de l’Océan Indien. This manuscript was partly written during a visit of EQ at the IGC funded by the Programme d’Actions Universitaires Intégrées Luso-françaises 2007/2008 to LC.

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  1. UMR5174 CNRS/UPS EDB, «Evolution et Diversité Biologique», Bâtiment 4R3 b2, Université Paul Sabatier, 118 route de Narbonne, 31062, Toulouse cedex 9, France

    Erwan Quéméré, Alexandre Ribéron, Lounès Chikhi & Brigitte Crouau-Roy

  2. Center for Conservation and Research, Henry Doorly Zoo, 3701 South 10th Street, Omaha, NE, 68107, USA

    Edward E. Louis Jr.

  3. Instituto Gulbenkian de Ciência, Rua da Quinta Grande, no. 6, 2780-156, Oeiras, Portugal

    Lounès Chikhi

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  1. Erwan Quéméré
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  4. Lounès Chikhi
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Quéméré, E., Louis, E.E., Ribéron, A. et al. 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 11, 675–687 (2010). https://doi.org/10.1007/s10592-009-9837-9

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