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

Primates

Volumn 51, Issue 1, 2010, Pages 53-61

  Razakamaharavo, Vololoniaina R ^a   McGuire, Susie M ^b   Vasey, Natalie ^c   Louis Jr , Edward E ^b   Brenneman, Rick A ^b  

^a UNIVERSITY OF ANTANANARIVO   (Madagascar)

^b OMAHA'S HENRY DOORLY ZOO AND AQUARIUM   (United States)

^c PORTLAND STATE UNIVERSITY   (United States)

Author keywords

Anthropogenic pressure; Habitat fragmentation; Microsatellites; Population structure; Varecia rubra

Indexed keywords

ANTHROPOGENIC EFFECT; ENVIRONMENTAL DEGRADATION; FOREST ECOSYSTEM; GENE FLOW; GENOTYPE; HABITAT FRAGMENTATION; POPULATION BOTTLENECK; POPULATION GENETICS; POPULATION STRUCTURE; PRIMATE;

ANIMAL; ARTICLE; DEMOGRAPHY; ECOSYSTEM; GENETIC VARIABILITY; GENETICS; GENOTYPE; MADAGASCAR; PROSIMIAN; TREE;

ANIMALS; DEMOGRAPHY; ECOSYSTEM; GENETIC VARIATION; GENOTYPE; LEMURIDAE; MADAGASCAR; TREES;

MADAGASCAR; MASOALA NATIONAL PARK; MASOALA PENINSULA;

MASOALA; STREPSIRHINI; VARECIA; VARECIA VARIEGATA;

EID: 77949774493     PISSN: 00328332     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10329-009-0171-0     Document Type: Article

References (76)

1. Allnutt TF, Powell GVN, Ferrier S, Ricketts TH, Steininger MK, Manion G (2004) Quantifying biodiversity loss in Madagasusing biological inventories, environmental data and a 50-year record of deforestation. Society for Conservation Biology Meetings, New York, 30 July-22 August 2004.
2. 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.
3. 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.
4. Balloux F (2004) Heterozygote excess in small populations and the heterozygote-excess effective population size. Evolution 58(9): 1891-1900.
5. 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.
6. 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.
7. 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.
8. Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24(3): 621-631.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. Frankham R, Ballou JA, Briscoe DA (2004) Introduction to conservation genetics. Cambridge University Press, Cambridge, p 536.
17. Garza JC, Williamson E (2001) Detection and reduction population size using data from microsatellite DNA. Mol Ecol 10: 305-318.
18. 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.
19. 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.
20. 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.
21. Goudet J (1995) FSTAT, a computer program to test F-statistics. J Hered 86: 485-486.
22. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2. 9. 3). Updated from Goudet 1995.
23. Goudet J, Perrin N, Wasser P (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Mol Ecol 11: 1103-1114.
24. Green C, Sussman RW (1990) Deforestation history of the eastern rain forests of Madagascar from satellites images. Science 248: 212-215.
25. 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.
26. 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.
27. 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.
28. Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38: 209-216.
29. Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for parental exclusion. Mol Ecol 14: 599-612.
30. 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.
31. Jenkins MD (ed) (1990) Madagascar: an environmental profile. IUCN Conservation Monitoring Centre, Gland.
32. 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.
33. 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.
34. Luikart G, Cornuet J-M (1999) Estimating the effective number of breeders from heterozygote excess progeny. Genetics 151: 1211-1216.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. Myers N (1988) Threatened biotas: "hotspots" in tropical forests. Environmentalist 8: 1-12.
42. Myers N (1998) Lifting the veil on perverse subsidies. Nature 392: 327-328.
43. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Conserv Biol 12: 516-520.
44. 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.
45. Nelson R, Horning N (1993) Cover forest/non-forest classification of Madagascar from AVHRR data. Int J Remote Sens 14(8): 1445-1446.
46. Nicoll ME, Lagrand O (1993) AVHRR-LAC estimates of forested area in Madagascar, 1990. Int J Remote Sens 14(8): 1463-1475.
47. 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.
48. Paetkau DW, Calvert W, Stirling I, Strombeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4: 347-354.
49. 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.
50. 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.
51. 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.
52. Petter JJ, Albignac R, Rumpler Y (1977) Faunne de Madagascar 44: Mammifères lémuriens (Primates prosimiens). ORSTOM/CNRS, Paris.
53. 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.
54. 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.
55. Pollack E (1987) On the theory of partially inbreeding finite populations. I. Partial selfing. Genetics 117: 353-360.
56. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
57. 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.
58. 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.
59. 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.
60. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94: 9197-9201.
61. 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.
62. Raymond M, Rousset F (1995) GENEPOP (Version3. 1): population genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
63. 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.
64. 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.
65. 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.
66. Tattersall I (1977) Distribution of Malagasy lemurs. Part 1: the lemurs of northern Madagascar. Annal N Y Acad Sci 293: 160-169.
67. 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.
68. 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.
69. Vasey N (1997b) How many red ruffed lemurs are left? Int J Primatol 18(2): 207-216.
70. Vasey N (2002) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns. Am J Phys Anthropol 118(2): 169-183.
71. 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.
72. 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.
73. 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.
74. 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.
75. Weir B, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6): 1358-1370.
76. 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.