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Genetic Diversity, Population Size, and Conservation of the Critically Endangered Perrier’s Sifaka (Propithecus perrieri)

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Abstract

Genetic data can be combined with ecological data to study the demographic history of a species, identify landscape features that influence migration patterns, and guide conservation efforts. Perrier’s sifaka (Propithecus perrieri) is a Critically Endangered, rare, and elusive social lemur living in a very restricted, fragmented landscape. To assess the effect of habitat loss and fragmentation on the genetic diversity of the Perrier’s sifaka population we examined 24 microsatellite markers genotyped for 67 samples corresponding to 42 individuals. Perrier’s sifaka shows a low current effective population size (ca. 52–105) and a strong heterozygosity excess, suggesting a historically large but dwindling population. Moreover, we identified a pattern of isolation by distance, typical of continuous habitat, suggesting that sifakas were still able to cross the grasslands between forest fragments in the recent past. Our study calls for a unified conservation plan covering the two protected areas where the species is still present, if not the whole area of its past distribution. Further studies inferring the past demographic history of Perrier’s sifaka may confirm the population decline and shed light on its potential causes.

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References

  • Agudo, R., Rico, C., Vilà, C., Hiraldo, F., & Donázar, J. A. (2010). The role of humans in the diversification of a threatened island raptor. BMC Evolutionary Biology, 10(1), 384.

    Article  PubMed  PubMed Central  Google Scholar 

  • Allcock, A. L., & Strugnell, J. M. (2012). Southern Ocean diversity: new paradigms from molecular ecology. Trends in Ecology & Evolution, 27(9), 520–528.

    Article  Google Scholar 

  • Allentoft, M. E., Heller, R., Oskam, C. L., Lorenzen, E. D., Hale, M. L., Gilbert, M. T. P., et al. (2014). Extinct New Zealand megafauna were not in decline before human colonization. Proceedings of the National Academy of Sciences of the USA, 111(13), 4922–4927.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Allnutt, T. F., Ferrier, S., Manion, G., Powell, G. V., Ricketts, T. H., Fisher, B. L., et al. (2008). A method for quantifying biodiversity loss and its application to a 50-year record of deforestation across Madagascar. Conservation Letters, 1(4), 173–181.

    Article  Google Scholar 

  • Andren, H. (1994). Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suiTable habitat: a review. Oikos, 71(3), 355–366.

    Article  Google Scholar 

  • Asner, G. P., Rudel, T. K., Aide, T. M., Defries, R., & Emerson, R. (2009). A contemporary assessment of change in humid tropical forests. Conservation Biology, 23(6), 1386–1395.

    Article  PubMed  Google Scholar 

  • Baden, A. L., Holmes, S. M., Johnson, S. E., Engberg, S. E., Louis, E. E., & Bradley, B. J. (2014). Species-level view of population structure and gene flow for a critically endangered primate (Varecia variegata). Ecology and Evolution, 4(13), 2675–2692.

    Article  PubMed  PubMed Central  Google Scholar 

  • Banks, M. A. (2013). Determinants of abundance and the distribution of primates in northern Madagascar (Physical Anthropology). Ph.D. thesis, Stony Brook University.

  • Banks, M. A., Ellis, E. R., & Wright, P. C. (2007). Global population size of a critically endangered lemur, Perrier’s sifaka. Animal Conservation, 10(2), 254–262.

    Article  Google Scholar 

  • Barrett, M. A., Brown, J. L., Morikawa, M. K., Labat, J.-N., & Yoder, A. D. (2010). CITES designation for endangered rosewood in Madagascar. Science, 328(5982), 1109–1110.

    Article  PubMed  CAS  Google Scholar 

  • Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., & Catch, F. (2004). GENETIX 4. 0. 5. 2., Software under Windows™ for the genetics of the populations. Laboratory Genome, Populations, Interactions, CNRS UMR.

  • Berec, L., Angulo, E., & Courchamp, F. (2007). Multiple Allee effects and population management. Trends in Ecology & Evolution, 22(4), 185–191.

    Article  Google Scholar 

  • Brenneman, R. A., Johnson, S. E., Bailey, C. A., Ingraldi, C., Delmore, K. E., Wyman, T. M., et al. (2012). Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations. Oryx, 46(02), 298–307.

    Article  Google Scholar 

  • Buckland, S. T. (2001). Introduction to distance sampling: Estimating abundance of biological populations. New York: Oxford University Press.

    Google Scholar 

  • Buckland, S. T., Plumptre, A. J., Thomas, L., & Rexstad, E. A. (2010). Design and analysis of line transect surveys for primates. International Journal of Primatology, 31(5), 833–847.

    Article  Google Scholar 

  • Burivalova, Z. (2011). Remote sensing of vegetation in conservation: A case study from the dry and transitional forests of Andrafiamena, northern Madagascar. Master’s dissertation, Universite de Geneve and Conservatoire et Jardin botaniques de la Ville de Geneve, Genève.

  • Carret, J.-C. (2013). Madagascar - Country Environmental Analysis (CEA): Taking stock and moving forward (No. 77993, pp. 1–164). The World Bank. http://documents.worldbank.org/curated/en/2013/05/17759163/madagascar-country-environmental-analysis-cea-taking-stock-moving-forward. Accessed 7 Nov 2014.

  • Chikhi, L., Sousa, V. C., Luisi, P., Goossens, B., & Beaumont, M. A. (2010). The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics, 186(3), 983.

    Article  PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Craul, M., Chikhi, L., Sousa, V., Olivieri, G. L., Rabesandratana, A., Zimmermann, E., & Radespiel, U. (2009). Influence of forest fragmentation on an endangered large-bodied lemur in northwestern Madagascar. Biological Conservation, 142, 2862--2871.

  • Csilléry, K., Blum, M. G., Gaggiotti, O. E., & François, O. (2010). Approximate Bayesian computation (ABC) in practice. Trends in Ecology & Evolution, 25(7), 410–418.

    Article  Google Scholar 

  • Cushman, S. A., Wasserman, T. N., Landguth, E. L., & Shirk, A. J. (2013). Re-evaluating causal modeling with Mantel tests in landscape genetics. Diversity, 5(1), 51–72.

    Article  Google Scholar 

  • Dewar, R. E., Radimilahy, C., Wright, H. T., Jacobs, Z., Kelly, G. O., & Berna, F. (2013). Stone tools and foraging in northern Madagascar challenge Holocene extinction models. Proceedings of the National Academy of Sciences of the USA, 110(31), 12583–12588.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fahrig, L. (2003). Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution, and Systematics, 34, 487–515.

    Article  Google Scholar 

  • Falush, D., Stephens, M., & Pritchard, J. K. (2007). Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes, 7(4), 574–578.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Frankham, R., Briscoe, D. A., & Ballou, J. D. (2002). Introduction to conservation genetics (p. 619). Cambridge: Cambridge University Press.

  • Frankham, R., Bradshaw, C. J., & Brook, B. W. (2014). Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biological Conservation, 170, 56–63.

    Article  Google Scholar 

  • Franklin, I. R. (1980). Evolutionary change in small populations. Conservation biology: An evolutionary-ecological perspective (pp. 135–149). Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Frantz, A. C., Pope, L. C., Carpenter, P. J., Roper, T. J., Wilson, G. J., Delahay, R. J., & Burke, T. (2003). Reliable microsatellite genotyping of the Eurasian badger (Meles meles) using faecal DNA. Molecular Ecology, 12(6), 1649–1661.

    Article  PubMed  CAS  Google Scholar 

  • Ganzhorn, J. U., Lowry, P. P., Schatz, G. E., & Sommer, S. (2001). The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx, 35(4), 346–348.

    Article  Google Scholar 

  • Gibson, L., Lee, T. M., Koh, L. P., Brook, B. W., Gardner, T. A., Barlow, J., et al. (2011). Primary forests are irreplaceable for sustaining tropical biodiversity. Nature, 478(7369), 378–381.

    Article  PubMed  CAS  Google Scholar 

  • Global Witness. (2009). Investigation into the illegal felling, transport and export of precious wood in SAVA Region Madagascar. London: Environmental Investigation Agency.

  • Godfrey, L. R., Jungers, W. L., Simons, E. L., Chatrath, P. S., & Rakotosamimanana, B. (1996). Past and present distributions of lemurs in Madagascar. In New directions in lemur studies (pp. 19–53). New York: Springer-Verlag. 10.1007/978-1-4615-4705-1_2 Accessed 26 March 2015.

  • Gommery, D., Ramanivosoa, B., Faure, M., Guerin, C., Kerloc’h, P., Senegas, F., & Randrianantenaina, H. (2011). Oldest evidence of human activities in Madagascar on subfossil hippopotamus bones from Anjohibe (Mahajanga Province). Comptes Rendus Palevol, 10(4), 271–278.

    Article  Google Scholar 

  • Goodman, S. M., & Benstead, J. P. (2005). Updated estimates of biotic diversity and endemism for Madagascar. Oryx, 39(01), 73–77.

    Article  Google Scholar 

  • Goodman, S. M., & Wilmé, L. (2006a). Inventaires de la faune et de la flore du nord de Madagascar dans la région Loky-Manambato, Analamerana et Andavakoera. Recherche pour le Developement, 23, 238.

    Google Scholar 

  • Goodman, S. M., & Wilmé, L. (2006b). Introduction. Inventaires de la faune et de la flore du nord de Madagascar dans la région Loky-Manambato, Analamerana et Andavakoera. Recherche pour le Developement, 23, 1–36.

    Google Scholar 

  • Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation, 34(4), 325–333.

    Article  Google Scholar 

  • Hawkins, A. F. A., Chapman, P., Ganzhorn, J. U., Bloxam, Q. M. C., Barlow, S. C., & Tonge, S. J. (1990). Vertebrate conservation in Ankarana special reserve, northern Madagascar. Biological Conservation, 54(2), 83–110.

    Article  Google Scholar 

  • Heller, R., Chikhi, L., & Siegismund, H. R. (2013). The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS ONE, 8(5), e62992.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hewitt, G. (2000). The genetic legacy of the Quaternary ice ages. Nature, 405(6789), 907–913.

    Article  PubMed  CAS  Google Scholar 

  • Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 359(1442), 183–195.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hochachka, W. M., Martin, K., Doyle, F., & Krebs, C. J. (2000). Monitoring vertebrate populations using observational data. Canadian Journal of Zoology, 78(4), 521–529.

    Article  Google Scholar 

  • Humbert, H., Darne, G. C., & Besairie, H. (1965). Notice de la carte Madagascar. Institut Français de Pondichéry. http://library.wur.nl/WebQuery/clc/1939325. Accessed 6 Nov 2014.

  • Irwin, M. T., Johnson, S. E., & Wright, P. C. (2005). The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx, 39(2), 204–218.

    Article  Google Scholar 

  • IUCN, S. S. C. (2001). IUCN Red List categories and criteria: version 3.1. Prepared by the IUCN Species Survival Commission.

  • IUCN (2014). 2014 IUCN Red List of threatened species, version 2014.2. http://www.iucnredlist.org/. Accessed 26 Nov 2015.

  • Jacobson, B., & Peres-Neto, P. R. (2010). Quantifying and disentangling dispersal in metacommunities: how close have we come? How far is there to go? Landscape Ecology, 25(4), 495–507.

    Article  Google Scholar 

  • Jenkins, R. K. B., Keane, A., Rakotoarivelo, A. R., Rakotomboavonjy, V., Randrianandrianina, F. H., Razafimanahaka, H. J., et al. (2011). Analysis of patterns of bushmeat consumption reveals extensive exploitation of protected species in eastern Madagascar. PLoS ONE, 6(12), e27570.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jeppsson, T., & Forslund, P. (2012). Can life history predict the effect of demographic stochasticity on extinction risk? The American Naturalist, 179(6), 706–720.

    Article  PubMed  Google Scholar 

  • Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics, 27(21), 3070–3071.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jungers, W. L., Godfrey, L. R., Simons, E. L., & Chatrath, P. S. (1995). Subfossil Indri indri from the Ankarana Massif of northern Madagascar. American Journal of Physical Anthropology, 97(4), 357–366.

    Article  PubMed  CAS  Google Scholar 

  • Kalinowski, S. T. (2005). hp-rare 1.0: a computer program for performing rarefaction analysis on measures of allelic richness. Molecular Ecology Notes, 5(1), 187–189.

    Article  CAS  Google Scholar 

  • Kappeler, P. M., & Schäffler, L. (2008). The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behavioral Ecology and Sociobiology, 62(6), 1007–1015.

    Article  Google Scholar 

  • Keller, L. F., & Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology & Evolution, 17(5), 230–241.

    Article  Google Scholar 

  • Khasin, M., Meerson, B., Khain, E., & Sander, L. M. (2012). Minimizing the population extinction risk by migration. Physical Review Letters, 109(13), 138104.

    Article  PubMed  CAS  Google Scholar 

  • Kimura, M., & Ohta, T. (1969). The average number of generations until fixation of a mutant gene in a finite population. Genetics, 61(3), 763.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kliman, R., Sheehy, B., & Schultz, J. (2008). Genetic drift and effective population size. Nature Education, 1(3), 3.

    Google Scholar 

  • Kramer, A. M., Dennis, B., Liebhold, A. M., & Drake, J. M. (2009). The evidence for Allee effects. Population Ecology, 51(3), 341–354.

    Article  Google Scholar 

  • Kun-Rodrigues, C., Salmona, J., Besolo, A., Rasolondraibe, E., Rabarivola, C., Marques, T. A., & Chikhi, L. (2014). New density estimates of a threatened sifaka species (Propithecus coquereli) in Ankarafantsika National Park. American Journal of Primatology, 76(6), 515–528.

    Article  PubMed  Google Scholar 

  • Lande, R. (1993). Risks of population extinction from demographic and environmental stochasticity and random catastrophes. The American Naturalist, 142, 911–927.

  • Laurance, W. F., Useche, D. C., Rendeiro, J., Kalka, M., Bradshaw, C. J., Sloan, S. P., et al. (2012). Averting biodiversity collapse in tropical forest protected areas. Nature, 489(7415), 290–294.

    Article  PubMed  CAS  Google Scholar 

  • Lawler, R. R., Richard, A. F., & Riley, M. A. (2001). Characterization and screening of microsatellite loci in a wild lemur population (Propithecus verreauxi verreauxi). American Journal of Primatology, 55(4), 253–259.

    Article  PubMed  CAS  Google Scholar 

  • Lawler, R. R., Caswell, H., Richard, A. F., Ratsirarson, J., Dewar, R. E., & Schwartz, M. (2009). Demography of Verreaux’s sifaka in a stochastic rainfall environment. Oecologia, 161(3), 491–504.

    Article  PubMed  Google Scholar 

  • Lehman, S. M., & Mayor, M. (2004). Dietary patterns in Perrier’s sifakas (Propithecus diadema perrieri): a preliminary study. American Journal of Primatology, 62(2), 115–122.

    Article  PubMed  Google Scholar 

  • Lei, R., Day, S., Ramarokoto, R., Shore, G. D., Louis, J., Edward, E., & Brenneman, R. A. (2008). Characterization of 21 microsatellites developed from Propithecus deckeni deckeni. Molecular Ecology Resources, 8(4), 773–776.

    Article  PubMed  CAS  Google Scholar 

  • Luikart, G., & Cornuet, J.-M. (1998). Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology, 12(1), 228–237.

    Article  Google Scholar 

  • Lynch, M., & Ritland, K. (1999). Estimation of pairwise relatedness with molecular markers. Genetics, 152(4), 1753–1766.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Manel, S., & Holderegger, R. (2013). Ten years of landscape genetics. Trends in Ecology & Evolution, 28(10), 614–621.

    Article  Google Scholar 

  • Mayor, M., & Lehman, S. M. (1999). Conservation of Perrier’s sifaka (Propithecus diadema perrieri) in Analamera Special Reserve, Madagascar. Lemur News, 4, 21–23.

    Google Scholar 

  • Mayor, M. I., Sommer, J. A., Huebinger, R. M., Barber, R. C., & Louis, E. E. (2002). Characterization of seven microsatellite marker loci in a genus of Malagasy lemurs (Propithecus). Molecular Ecology Notes, 2(4), 385–388.

    Article  CAS  Google Scholar 

  • Mazet, O., Rodríguez, W., & Chikhi, L. (2015). Demographic inference using genetic data from a single individual: separating population size variation from population structure. Theoretical Population Biology, 104, 46–58.

    Article  PubMed  Google Scholar 

  • McGuire, S. M., Emodi, G. P., Shore, G. D., Brenneman, R. A., & Louis, E. E. (2009). Characterization of 21 microsatellite marker loci in the silky sifaka (Propithecus candidus). Conservation Genetics, 10(4), 985–988.

    Article  CAS  Google Scholar 

  • Meyers, D. M., & Ratsirarson, J. (1989). Distribution and conservation of two endangered sifakas in northern Madagascar. Primate Conservation, 10, 81–86.

    Google Scholar 

  • Meyers, D. M., & Wright, P. C. (1993). Resource tracking: Food availability and Propithecus seasonal reproduction. In J. Ganzhorn & P. M. Kappeler (Eds.), Lemur social systems and their ecological basis (pp. 179–192). New York: Plenum Press.

    Chapter  Google Scholar 

  • Minten, B., Randrianarisoa, J.-C., Randrianarison, L., & Food, C. (2003). Agriculture, pauvreté rurale et politiques économiques à Madagascar. Cornell Food and Nutrition Policy Program. http://www.hayzara.org/index.php/eng/content/download/496/4084/version/2/file/2003+-+Agriculture+pauvret%C3%A9+rurale+et+Politiques+Economiques+a+Madagascar.pdf Accessed 7 Nov 2014.

  • Mitchell, M. W., Locatelli, S., Clee, P. R. S., Thomassen, H. A., & Gonder, M. K. (2015). Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot. BMC Evolutionary Biology, 15(1), 1.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mittermeier, R. A., Louis, E. E., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A., et al. (2010). Lemurs of Madagascar (3rd ed.). Washington, DC: Conservation International.

    Google Scholar 

  • Moat, J., & Smith, P. (2007). Atlas of the vegetation of Madagascar/ Vegetation/atlas de la vegetation de Madagascar (Royal Botanic Gardens Kew). Kew Publishing. http://tna.europarchive.org/20080612120511/http://kew.org/publications/vegatlas_ai.doc. Accessed 25 Nov 2013.

  • Morris, W. F., Altmann, J., Brockman, D. K., Cords, M., Fedigan, L. M., Pusey, A. E., et al. (2011). Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates. The American Naturalist, 177(1), E14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Munson, L., Brown, J. L., Bush, M., Packer, C., Janssen, D., Reiziss, S. M., & Wildt, D. E. (1996). Genetic diversity affects testicular morphology in free-ranging lions (Panthera leo) of the Serengeti Plains and Ngorongoro Crater. Journal of Reproduction and Fertility, 108(1), 11–15.

    Article  PubMed  CAS  Google Scholar 

  • Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403(6772), 853–858.

    Article  PubMed  CAS  Google Scholar 

  • Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89(3), 583.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Nikolic, N., & Chevalet, C. (2014). Detecting past changes of effective population size. Evolutionary Applications, 7(6), 663–681.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nunney, L., & Campbell, K. A. (1993). Assessing minimum viable population size: demography meets population genetics. Trends in Ecology & Evolution, 8(7), 234–239.

    Article  CAS  Google Scholar 

  • Olivieri, G. L., 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.). Biological Conservation, 141(5), 1257–1271.

    Article  Google Scholar 

  • ONE (2013). Evolution de la couverture de forêts naturelles à Madagascar (2005- 2010). Antananarivo: Office National pour l’Environnement. www.pnae.mg/index.php/Autres/evolution-de-la-couverture-de-forets-naturelles-a-madagascar-2005-2010.html. Accessed 26 Nov 2015.

  • Palstra, F. P., & Fraser, D. J. (2012). Effective/census population size ratio estimation: a compendium and appraisal. Ecology and Evolution, 2(9), 2357–2365.

    Article  PubMed  PubMed Central  Google Scholar 

  • Paradis, E., Claude, J., & Strimmer, K. (2004). APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20(2), 289–290.

    Article  PubMed  CAS  Google Scholar 

  • Peakall, R. O. D., & Smouse, P. E. (2006). GENALEX 6: genetic analysis in excel. population genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288–295.

    Article  Google Scholar 

  • Peery, M. Z., Kirby, R., Reid, B. N., Stoelting, R., Doucet-Bëer, E., Robinson, S., et al. (2012). Reliability of genetic bottleneck tests for detecting recent population declines. Molecular Ecology, 21(14), 3403–3418.

    Article  PubMed  Google Scholar 

  • Pemberton, J. (2004). Measuring inbreeding depression in the wild: the old ways are the best. Trends in Ecology & Evolution, 19(12), 613–615.

    Article  Google Scholar 

  • Petit, R. J., Aguinagalde, I., de Beaulieu, J.-L., Bittkau, C., Brewer, S., Cheddadi, R., et al. (2003). Glacial refugia: hotspots but not melting pots of genetic diversity. Science, 300(5625), 1563–1565.

    Article  PubMed  CAS  Google Scholar 

  • Pimm, S. L., & Brooks, T. (2013). Conservation: forest fragments, facts, and fallacies. Current Biology, 23(24), 1098–1101.

    Article  CAS  Google Scholar 

  • Pimm, S. L., & Raven, P. (2000). Biodiversity: extinction by numbers. Nature, 403(6772), 843–845.

    Article  PubMed  CAS  Google Scholar 

  • Piry, S., Luikart, G., & Cornuet, J. M. (1999). Computer note. BOTTLENECK: A computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity, 90(4), 502.

    Article  Google Scholar 

  • Provan, J., & Bennett, K. D. (2008). Phylogeographic insights into cryptic glacial refugia. Trends in Ecology & Evolution, 23(10), 564–571.

    Article  Google Scholar 

  • Quéméré, E., Champeau, J., Besolo, A., Rasolondraibe, E., Rabarivola, C., Crouau-Roy, B., & Chikhi, L. (2010a). Spatial variation in density and total size estimates in fragmented primate populations: the golden-crowned sifaka (Propithecus tattersalli). American Journal of Primatology, 72(1), 72–80.

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Quéméré, E., Louis, E. E., Ribéron, A., Chikhi, L., & Crouau-Roy, B. (2010c). Non-invasive conservation genetics of the critically endangered golden-crowned sifaka (Propithecus tattersalli): high diversity and significant genetic differentiation over a small range. Conservation Genetics, 11(3), 675–687.

    Article  Google Scholar 

  • Quéméré, E., Amelot, X., Pierson, J., Crouau-Roy, B., & Chikhi, L. (2012). Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proceedings of the National Academy of Sciences of the USA, 109(32), 13028–13033.

    Article  PubMed  PubMed Central  Google Scholar 

  • R CoreTeam. (2014). R: A language and environment for statistical computing. http://www.R-project.org. Accessed 18 Nov 2014.

  • 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. American Journal of Primatology, 70(9), 860–870.

    Article  PubMed  Google Scholar 

  • Rakotoarisoa, G. (2010). Diversité génétique de Propithecus coquereli. PhD thesis, Univeristy of Antananarivo, Antananarivo.

  • Rakotoarisoa, G., Shore, G., Mcguire, S., Engberg, S., Louis, E., & Brenneman, R. (2006). Characterization of 20 microsatellite marker loci in Coquerel’s sifaka (Propithecus coquereli). Molecular Ecology Notes, 6(4), 1119–1121.

    Article  CAS  Google Scholar 

  • Razafindrakoto, A., Andriantompohavana, R., Wohlhauser, S., Rajaobelina, S., Louis, E. E., Jr., & Brenneman, R. A. (2007). Forest fragment and range survey of the Ambararata-Maromokotra Loky River locale of northeastern Madagascar for golden-crowned sifaka (Propithecus tattersalli). Lemur News, 12, 29.

    Google Scholar 

  • Razakamaharavo, V. R., McGuire, S. M., Vasey, N., Louis, E. E., Jr., & Brenneman, R. A. (2010). Genetic architecture of two red ruffed lemur (Varecia rubra) populations of Masoala National Park. Primates, 51(1), 53–61.

    Article  PubMed  Google Scholar 

  • Richard, A. F., Rakotomanga, P., & Schwartz, M. (1993). Dispersal by Propithecus verreauxi at Beza Mahafaly, Madagascar 1984–1991. American Journal of Primatology, 30(1), 1–20.

    Article  Google Scholar 

  • Roelke, M. E., Martenson, J. S., & O’Brien, S. J. (1993). The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Current Biology, 3(6), 340–350.

    Article  PubMed  CAS  Google Scholar 

  • Rousset, F. C. (2008). Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8(1), 103–106.

    Article  PubMed  Google Scholar 

  • Salmona, J. (2014). Conservation, distribution and population size update of endangered nocturnal lemur species from Northern Madagascar, Rufford Small Grant final report. Rufford Small Grant Final Report No. 1 (p. 21). https://www.researchgate.net/profile/Jordi_Salmona/publication/262334029_Conservation_distribution_and_population_size_update_of_endangered_nocturnal_lemur_species_from_Northern_Madagascar_Rufford_Small_Grant_final_report/links/0c9605374f966d7a1a000000.pdf. Accessed 26 Nov 2015.

  • Salmona, J. (2015). Comparative conservation genetics of several threatened lemur species living in fragmented environments. A glimpse through natural history of northern Madagascar lemurs. Ph.D Thesis (p. 330), Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Instituto Gulbenkian de Ciência, Oeiras Portugal.

  • Salmona, J., Salamolard, M., Fouillot, D., Ghestemme, T., Larose, J., Centon, J.-F., et al. (2012). Signature of a pre-human population decline in the critically endangered Reunion Island endemic forest bird Coracina newtoni. PLoS ONE, 7(8), e43524.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Salmona, J., Jan, F., Rasolondraibe, E., Zaranaina, R., Saïd Ousseni, D., Mohamed-Thani, I., et al. (2013a). Survey of the critically endangered Perrier’s sifaka (Propithecus perrieri) across most if its distribution range. Lemur News, 17, 9–12.

    Google Scholar 

  • Salmona, J., Zaonarivelo, J. R., & Banks, M. A. (2013b). Analamerana and Andrafiamena, site-based action plan for Perrier’s sifaka conservation. In C. Schwitzer, R. A. Mittermeier, N. Davies, S. E. Johnson, J. Ratsimbazafy, J. Razafindramanana, et al. (Eds.), Lemurs of Madagascar: A strategy for their conservation 2013–2016 (pp. 140–141). Bristol, UK: IUCN SSC Primate Specialist Group, Bristol Conservation and Science Foundation, and Conservation International.

    Google Scholar 

  • Salmona, J., Rasolondraibe, E., Jan, F., Besolo, A., Rakotoarisoa, H., Meyler, S. V., et al. (2014). Conservation status and abundance of the crowned sifaka (Propithecus coronatus). Primate Conservation, 28, 73–83.

    Article  Google Scholar 

  • Schwitzer, C., Arnoult, O., & Rakotosamimanana, B. (2006). An international conservation and research programme for Perrier’s sifaka (Propithecus perrieri Lavauden, 1931) in northern Madagascar. Lemur News, 11, 13.

    Google Scholar 

  • Schwitzer, C., Mittermeier, R. A., Davies, N., Johnson, S., Ratsimbazafy, J., Razafindramanana, J., et al. (2013). Lemurs of Madagascar: A strategy for their conservation 2013–2016 (p. 185). Bristol, UK: IUCN SSC Primate Specialist Group, Bristol Conservation and Science Foundation, and Conservation International.

  • Schwitzer, C., Chikhi, L., Donati, G., Irwin, M., Johnson, S. E., Mittermeier, R. A., et al. (2014a). Protecting lemurs–response. Science (New York), 344(6182), 358.

    Article  CAS  Google Scholar 

  • Schwitzer, C., Mittermeier, R., Johnson, S., Donati, G., Irwin, M., Peacock, H., et al. (2014b). Averting lemur extinctions amid Madagascar’s political crisis. Science, 343(6173), 842–843.

    Article  PubMed  CAS  Google Scholar 

  • Soulé, M. E. (1980). Thresholds for survival: maintaining fitness and evolutionary potential. Conservation Biology, 111, 124.

    Google Scholar 

  • Storz, J. F., & Beaumont, M. A. (2002). Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution, 56(1), 154–166.

    Article  PubMed  CAS  Google Scholar 

  • Tajima, F. (1989). The effect of change in population size on DNA polymorphism. Genetics, 123(3), 597.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Tulloch, A. I. T., Barnes, M. D., Ringma, J., Fuller, R. A., & Watson, J. E. M. (2015). Understanding the importance of small patches of habitat for conservation. Journal of Applied Ecology. doi:10.1111/1365-2664.12547.

    Google Scholar 

  • Vallet, D., Petit, E. J., Gatti, S., Levréro, F., & Ménard, N. (2008). A new 2CTAB/PCI method improves DNA amplification success from faeces of Mediterranean (Barbary macaques) and tropical (lowland gorillas) primates. Conservation Genetics, 9(3), 677–680.

    Article  CAS  Google Scholar 

  • van Oosterhout, C., Hutchinson, W. F., Wills, D. P., & Shipley, P. (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4(3), 535–538.

    Article  CAS  Google Scholar 

  • Vasey, N. (1997). How many red ruffed lemurs are left? International Journal of Primatology, 18(2), 207–216.

    Article  Google Scholar 

  • Vieilledent, G., Grinand, C., & Vaudry, R. (2013). Forecasting deforestation and carbon emissions in tropical developing countries facing demographic expansion: a case study in Madagascar. Ecology and Evolution, 3(6), 1702–1716.

    Article  PubMed  PubMed Central  Google Scholar 

  • Walker, F. M., Sunnucks, P., & Taylor, A. C. (2008). Evidence for habitat fragmentation altering within-population processes in wombats. Molecular Ecology, 17(7), 1674–1684.

    Article  PubMed  Google Scholar 

  • Waples, R. S., & Do, C. H. I. (2008). LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources, 8(4), 753–756.

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Wittke-Thompson, J. K., Pluzhnikov, A., & Cox, N. J. (2005). Rational inferences about departures from Hardy-Weinberg equilibrium. The American Journal of Human Genetics, 76(6), 967–986.

    Article  PubMed  CAS  Google Scholar 

  • Wootton, J. T., & Pfister, C. A. (2013). Experimental separation of genetic and demographic factors on extinction risk in wild populations. Ecology, 94(10), 2117–2123.

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank CAFF/CORE, the Direction Générale de l’Environnement et des Forêts, Madagascar National Park, the Fanamby NGO (in particular S. Rajaobelina V. Rasoloarison, P. Ranirison, and S. Wohlhauser), the Direction Régionale de l’Environnement et des Forêts région DIANA, and M. Banks for discussion and advices on Perrier’s sifaka. The field work was possible thanks to the continuous support of the Département de Biologie Animale et Ecologie, University of Mahajanga; the University of Antsiranana; and to a large extent, thanks to the participation of many great local guides and cooks whom we warmly thank for their help in the field and for sharing their incomparable expertise of the forest, Misaotra anareo jiaby. Finally we thank the Genomics Unit at the IGC, Sequencing Service, for their collaboration and L. Wilmé, R. Heller, E. Quéméré, and I. Carvalho for comments and discussion on the manuscript, Joanna Setchell and the editors of Biological Conservation and American Journal of Primatology as well as several anonymous reviewers who substantially helped improving the manuscript. Financial support for this study was provided by the Fundação para a Ciência e a Tecnologia (PTDC/BIA-BEC/100176/2008, PTDC/BIA-BIC/4476/2012, and SFRH/BD/64875/2009); the GDRI Madagascar; the Laboratoire d’Excellence (LABEX) entitled TULIP (ANR-10-LABX-41); the Rufford Small Grant Foundation, grant 10941-1; and the Instituto Gulbenkian de Ciência. C. Kun-Rodrigues and H. Teixeira were funded by an Optimus!Alive-IGC fellowship. This study was conducted in agreement with the laws of the countries of Portugal, France, and Madagascar.

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Correspondence to Jordi Salmona or Lounès Chikhi.

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The data set of microsatellite genotypes used in the study (Appendix S1) and the geographic coordinates of the individuals genotyped (Appendix S2) are available online.

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Salmona, J., Teixeira, H., Rasolondraibe, E. et al. Genetic Diversity, Population Size, and Conservation of the Critically Endangered Perrier’s Sifaka (Propithecus perrieri). Int J Primatol 36, 1132–1153 (2015). https://doi.org/10.1007/s10764-015-9881-x

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